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Gumbs lists mindfulness activities and practices at the end of Chapter 20. Meditation practices and mindful breathing practices. They are titles after her chapters and she gives the reader a main takeaway from each chapter.

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WE need to make time to rest. In a capitalistic society, there isn't much time to do so. Especially if you are poor. We live in a nation with a hustle culture. We live too fast. Our schools and our economy are on a quarter system, always looking ahead. Gumbs argues that we can learn how to take pro[er rest, from Seals.

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Slowing down attributes to mindfulness. Slowing down is listening. Slowing down is knowing. Slowing down is to change your heart. - Chapter 17

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"There are several practices of marine mammals that resonate withBlack Freedom movement strategies and practices". (Gumbs, Chapter 16)

I agree with this and have posted videos in earlier slides in this pallet that agree with this line of thought.

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"In 1995, a Spotted Dolphin got stranded on the shore in Texas. Texan scientists, of course, detained them, but eventually let them loose but with a wire on their dorsal fin to spy on other dolphins in the gulf and beyond. The scientists called it help." Gumbs likens this to when humans sign up for social media accounts and give the platform permission to track and monitor their activity on and off the app.

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Neurosci Biobehav Rev. Author manuscript; available in PMC 2021 Aug 1.

Published in final edited form as:

Abstract

Sex differences in brain and behavior of animals including humans result from an interaction between biological and environmental influences. This is also true for the differences between men and women concerning sexual orientation. Sexual differentiation is mediated by three groups of biological mechanisms: early actions of sex steroids, more direct actions of sex-specific genes not mediated by gonadal sex steroids and epigenetic mechanisms. Differential interactions with parents and conspecifics have additionally long-term influences on behavior. This presentation reviews available evidence indicating that these different mechanisms play a significant role in the control of sexual partner preference in animals and humans, in other words the homosexual versus heterosexual orientation. Clinical and epidemiological studies of phenotypically selected populations indicate that early actions of hormones and genetic factors clearly contribute to the determination of sexual orientation. The maternal embryonic environment also modifies the incidence of male homosexuality via immunological mechanisms. The relative contribution of each of these mechanisms remains however to be determined.

Keywords: Homosexuality, biological mechanisms, sexual differentiation, testosterone, organizing effects of steroids, twin concordance, genome-wide associations, older brother effect, fraternal birth order effect

1. Introduction

I began investigating the endocrine controls of behavior in the early 1970ies using mainly avian species (ducks first, and then chicken, ring doves, Japanese quail, and various species of songbirds) ( Balthazart, 2017) and quickly became interested in the topic of sex differences and their development during ontogeny. Following the seminal paper of Phoenix and collaborators ( Phoenix et al., 1959) establishing the notion of organizing effects of sex steroids, research coming from several laboratories had clearly demonstrated that in rodents (mostly rats) the early action of testosterone respectively masculinizes and defeminizes the expression of male- and female-typical behaviors ( Forger et al., 2015; Gerall et al., 1992; McCarthy et al., 2009). However, Elizabeth Adkins-Regan and her collaborators at Cornel University were at that time establishing the model of sexual differentiation in quail by demonstrating that contrary to what is observed in rats, estrogens demasculinize the expression of male typical copulatory behavior in this species (for review ( Balthazart et al., 2017)).

This model provided a clear conceptual framework integrating the various mechanisms that contribute to generate adult subjects of two sexes that differ in multiple ways related to morphology, physiology and behavior (see Fig. 1 ). This information is available in many textbooks and reviews. I shall just provide here a brief overview mostly to define key concepts and the way I will use them since some of them are sometimes employed with slightly different meanings in the literature.

This organizing role of sex steroids was until the end of the 20 th century considered as the main factor organizing sex differences. However, investigations of a gynandromorphic zebra finch, Taeniopygia guttata ( Agate et al., 2003) followed by extensive studies of the four core genotypes in mice in which gonadal sex is disconnected from chromosomal sex ( Arnold, 2017; Arnold and Chen, 2009) clearly established that genes located on the sex chromosomes (or genes located on autosomes but differentially expressed in the two sexes) can also, independent of gonadal steroids, affect the sexual differentiation of an individual. These effects are often called "direct genetic effects" even if "effects not mediated via gonadal steroids" would be more appropriate.

Even more recently, evidence has accumulated supporting a role for inflammatory signaling molecules and for immune cells in the process of brain masculinization and its behavioral consequences ( McCarthy, 2019; McCarthy et al., 2017). This work will be reviewed in a separate chapter prepared by McCarthy for this special issue.

Additionally, in humans but also to some degree in other animals (e.g., See ( Meaney and Szyf, 2005; Moore, 1984, 1992; Moore and Power, 1992; Weaver et al., 2004)) various factors of the physical and social environment affect in a more or less enduring manner some behavioral traits. These factors determine what is, in humans specifically, called the gender, which I consider here as a partially social construct adding a layer of social influences on the sex, envisioned essentially as the result of various biological influences.

2. Sexual orientation as a sexually differentiated trait

Most adult humans are sexually attracted by members of the other sex and are thus heterosexual. There is however a significant minority estimated between 3 and 10% depending on the sex of the subjects and on the study methods, who are attracted and interested in having sexual interactions with persons of the same sex; they often identify as gay/lesbian ( Kinsey et al., 1953; Kinsey et al., 1948; Mosher et al., 2005). In the context of the sexual differentiation theory, homosexuality can be viewed as the reversal of sexual attraction observed in the largest fraction of the population. It is thus tempting to assume that sexual orientation is determined by the same mechanisms that control the differentiation of other sexually differentiated traits. Schematically, attraction to females (gynephilia) would be determined by early exposure to the action of testosterone while attraction to men (androphilia) would result from the absence of exposure to this hormone, although alternate views have been proposed (see ( Jordan-Young, 2010), p 159).

My interest for human sexual orientation relates to a quest animating many basic scientists for identifying the translational value of research in animals. The prominent sex differences affecting expression of sexual behavior in rodents (and birds) that have been the object of intense investigations are not present in humans. Male rats mount, intromit and ejaculate following standardized behavior patterns and females reliably adopt the lordosis posture whereas human sexual behavior takes a variety of forms that are not specifically associated with one sex or the other (see ( Nelson an Kriegsfeld, 2017)). In contrast, two dimensions of sexuality, namely sexual orientation and gender identity, are clearly differentiated in humans. The sex difference affecting these two dimensions of sexual behavior are associated with an effect size larger than 6 while most other behavioral sex differences in humans are associated with an effect size smaller than 1 ( Hines et al., 2016b).

The origins of the sex difference in sexual orientation (homosexual or heterosexual, this is in fact the same question) have been the topic of heated debates. Some researchers, usually psychologists or sociologists, consider that the orientation is essentially learned or imposed by raw models in the society (behaviorism and constructivism) while Freud and his followers have popularized theories indicating that homosexuality would reflects some form of arrest in psycho-sexual development caused by inadequate interactions with one or both parents ( Bailey et al., 2016).

3. Sexual orientation in rodents

Unlike other aspects of human sexuality that have no equivalent in animals (e.g., gender identity), sexual orientation can easily be studied in non-human mammals by giving them a choice between a male or female sexual partner and recording toward which of these partners the animal will orient his/her sexual behavior.

Lesion and stereotaxic implantation studies demonstrated that the sexual orientation of males, more commonly called sexual partner preference for animals, is controlled, like male copulatory behavior, by the medial part of the preoptic area. Lesions of this brain area switch the preference of a male from a female to a male partner ( Paredes and Baum, 1995; Paredes et al., 1998).

This preference for a partner of the same or the other sex is also reversed in both sexes by the early hormonal treatments that have been shown to sex-reverse copulatory behavior. Studies of Julie Bakker and Kos Slob at the University of Rotterdam (NL) initially demonstrated that inhibition of aromatase (the transformation of T into E2) during the two weeks surrounding birth in male rats largely switches their preference from a female partner to a male partner ( Bakker et al., 1993a; Bakker et al., 1993b, 1996). Similar effects of neonatal endocrine manipulations were later confirmed in male ( Olvera-Hernandez et al., 2015) and female rats ( Bodo and Rissman, 2008; Henley et al., 2009). Importantly the effects of these early hormonal manipulations seem to last the entire life of the subjects, they have to take place during a critical period of development, and the same treatments in adulthood have no effect on sexual partner preference. Recent work has additionally identified interactions between these early hormonal treatments and the sexual experience that subjects receive ( Olvera-Hernandez et al., 2019).

Taken together these data indicate that sexual partner preference is largely determined in rodents and sheep by the early hormonal environment in particular by testosterone, eventually acting via its estrogenic metabolites. Clinical and epidemiological data indicate that the same mechanism is still present in humans and that gynephilia is enhanced by the fetal or early neonatal action of testosterone while androphilia would result from the absence of such androgenic effects. These endocrine effects however only explain part of the human sexual orientation. Genetic and immunological influences have also been clearly identified and they do not appear, based on current knowledge, to depend only on changes in the early endocrine environment. Together these hormonal, genetic and immunological effects seem to play a major role in the determinism of human sexual orientation. These effects have been reviewed multiple times by me ( Balthazart, 2011, 2012a, b, 2016; Balthazart and Young, 2014) and others ( LeVay, 1997, 2010; LeVay and Hamer, 1994). We will therefore only briefly summarize these data and then focus on a few studies that were recently published that add critical evidence for the role of these biological mechanisms in the control of sexual orientation.

4. Is human sexual orientation reflecting organizing effects of sex steroids?

Two types of experimental evidence, clinical and epidemiological studies, indicate that hormones have an influence on adult sexual orientation.

4.1. Clinical studies

Three human pathologies support the notion that significant modifications of the embryonic endocrine environment affect the incidence of homosexuality independent of the sex of rearing. Firstly, girls suffering from congenital adrenal hyperplasia (CAH) are exposed in utero to abnormally high levels of androgens that masculinize their genital structures. Even if their endocrine condition is normalized by pharmacological means, their genital morphology is surgically "corrected" soon after birth and they are subsequently raised as girls, these girls will later on demonstrate masculinization of a variety of behavioral traits (e.g., aggressive play and toy selection)( Berenbaum, 1999; Berenbaum and Hines, 1992; Hines, 2004, 2006). They will also display a significantly increased incidence of homosexual (or at least not strictly heterosexual) orientation (up to 40% compared to less than 10% in control populations; See Fig. 2 ( Hines, 2006; Meyer-Bahlburg et al., 2008; Money et al., 1984).

Even if alternative explanations can and have been proposed for some of these observations, the most parsimonious explanation remains that embryonic hormones play a substantial role in the control of adult sexual orientation and that the sex of rearing is unable to completely counter the endocrine influences experienced prenatally.

4.2. Indirect markers of the prenatal endocrine milieu

On another hand, epidemiological studies indicate that homosexual and heterosexual populations differ in a number of established sex differences that are known, or at least strongly suspected, to be controlled by prenatal testosterone in animal species and often also in humans. This approach provides indirect information about the hormonal milieu to which an individual with a given sexual orientation was exposed during his/her embryonic life, given that it is nearly impossible, for practical reasons, to obtain this information in a direct manner.

These sex differences concern morphological, physiological and behavioral traits that are too numerous to be reviewed here in detail (See ( Balthazart, 2012a, b; Balthazart and Young, 2014; LeVay, 2010) for detail and references). Morphological differences include 1) the relative length of the index (D2) to the ring finger (D4) (shorter, masculinized ratio in lesbians compared to heterosexual women), 2) the relative length of long bones in the legs, arms, and hands (shorter bones in gay men and women who are attracted by men compared to men and lesbians who are attracted by women), and the volume of several brain structures including 3) the surprachiasmatic nucleus (larger in gay than in heterosexual men), 4) the anterior commissure (larger in gay than in heterosexual men) and finally 5) the Interstitial Nucleus of the Anterior Hypothalamus number 3 (INAH3; 2-3 times larger in heterosexual men than in gay men ( LeVay, 1991) and with a trend to a higher density of neurons in gay than in heterosexual men ( Byne et al., 2001)).

Functional differences relate to 6) aspects of the inner ear physiology, the socalled oto-acoustic emissions (less frequent and of lower amplitude in lesbians compared to heterosexual women; see Fig. 3 ), 7) the feedback of steroids on the secretion of luteinizing hormone (presence of a weak positive feedback after injection of a large dose of estrogens in gay but not in heterosexual men), and 8) the brain activation as detected by positron emission tomography (PET) in response to male or female typical odors (reaction of gay men to male odors contrary to heterosexual men and lack of reaction of lesbians to male odors contrary to heterosexual women). A number of behavioral traits related to visuo-spatial (males [M]>females [F]) and verbal (F>M) tasks, aggressiveness (M>F), and lateralization (M more often left-handed than F) that are putatively influenced by prenatal testosterone have also been reported to be different between homosexual and heterosexual populations and also indirectly support a role of prenatal sex hormones but data are less conclusive and will not be reviewed here (see ( Balthazart, 2012a, b; LeVay, 1997, 2010) for more detail).

4.3. Intrasex phenotypic diversity

This result is quite surprising since the 2D:4D ratio is clearly sexually differentiated and affected by prenatal testosterone in mammals ( Bailey et al., 2005; Brown et al., 2002a; Roney et al., 2004; Zheng and Cohn, 2011), birds ( Burley and Foster, 2004; Lombardo et al., 2008; Romano et al., 2005), reptiles ( Rubolini et al., 2006) and amphibians ( Kaczmarski et al., 2015), even if this is a very imprecise marker of prenatal androgenization. This ratio is for example masculinized in CAH girl who have been exposed to an excess of testosterone in utero ( Brown et al., 2002c; Okten et al., 2002) and it is usually feminine in genetic males bearing a mutation of the androgen receptor, preventing all effects of the steroid, the complete insensitivity syndrome ( Berenbaum et al., 2009). The 2D:4D ratio is admittedly a noisy reporter of prenatal androgen exposure with a limited effect size for the sex difference (Cohen d around 0.5, see ( Breedlove, 2017)) that does not permit to predict the sexual orientation of a specific individual but is reasonably reliable at the population level. It has a number of significant drawbacks (see ( Balthazart and Court, 2017) for detail) but why it is not feminized in gay men raises the question of whether male homosexuality is or is not influenced by the prenatal androgen action.

It is also possible that male homosexuality results from a deficit in androgen action specifically in the brain while androgens circulating concentration and action in the periphery on the growth of long bone (and thus the 2D:4D ratio) are left intact. But then why would this discrepancy between central and systemic action of androgens not be present also in females?

A more likely explanation in my eyes, relates to the phenotypic heterogeneity of male and female homosexuals. It has been reported that the 2D:4D ratio is more reliably masculinized in " butch" (more masculine) than in " femme" (more feminine) lesbians ( Brown et al., 2002b). One could thus wonder whether a same dichotomy also exists in gay men and explains why variable 2D-4D ratio are reported based on differences in the degree of masculinization in the sampled population.

Ashlyn Swift-Gallant at the Memorial University of Newfoundland recently reviewed literature indicating that, in both mice and human, the organizing effects of androgens are not necessarily linear. It is classically admitted that exposure to androgens during development promotes male-typical behaviors and male-typical sexual preference (gynephilia) whereas lack of such exposure or exposure to very low levels promote female-typical behaviors and androphilia ( Swift-Gallant, 2019). Studies in mice have however accumulated showing that when androgen stimulation is very high, due to injection of large doses of exogenous steroid or to androgen receptor overexpression, male-typical behavior is still expressed but sexual preferences may be altered and same-sex attraction is enhanced (e.g., ( Dela Cruz and Pereira, 2012; Henley et al., 2010; Swift-Gallant et al., 2016a; Swift-Gallant et al., 2016b); see ( Swift-Gallant, 2019) for a general review of this evidence). She also presented evidence that homosexual sexual orientation in men might result from an early developmental exposure to both lower and also higher androgenic stimulation as compared to heterosexual men ( Swift-Gallant, 2019). This raises the possibility that early exposure to high androgenic stimulation may contribute to explain the homosexual orientation of gay men who prefer an insertive anal role (called tops) while those who prefer receptive anal sex (bottoms) or show no preference (versatiles) would have been exposed to low androgen stimulation, based on indirect retrospective markers of androgen exposure. This conclusion is however not based on measures of the 2D:4D ratio as a marker of prenatal androgen exposure but rather to a differential incidence of left-handedness.

5. Genetic contributions

Taken together, the data discussed in the previous section support the notion that prenatal androgenization plays a significant role in the control of human sexual orientation. However changes in sexual orientation as a result of prenatal endocrine disorders always concern only a fraction of affected individuals (usually a maximum of 30 to 40%). Furthermore, all markers of the prenatal hormone milieu that have been associated with homosexuality are noisy markers that only explain a limited part of the variance in orientation. In addition, if variations in endocrine exposure during ontogeny explain differences in sexual orientation, the origin of these variations needs to be identified.

It was suggested that a decreased androgenization might be the consequence of intense stress in pregnant women based on the fact that retrospective studies indicated an increased incidence of male homosexuality in men born in Berlin during the last two years of World War II ( Dorner et al., 1980; Dorner et al., 1983). However, even if this potential mechanism is supported by a host of studies in rodents ( Ward, 1972, 1984; Ward and Ward, 1985; Weisz et al., 1982), no additional evidence based on human studies has since been collected.

Individual genetic differences could obviously explain differences in steroid production or action. In addition, animal research has during the last two decades demonstrated that genes can affect the adult phenotype in a "direct" manner i.e., by mechanisms that do not involve changes in steroid exposure (see section 3). A substantial body of research has therefore been dedicated to the potential genetic bases of homosexuality.

5.1. Heritability within families and twins comparisons

Homosexual twins separated at birth are too rare to allow drawing firm conclusions ( Eckert et al., 1986) but the comparison of monozygotic versus dizygotic twins ("true" versus "false" twins) provides key information about the genetic bases of homosexuality. Monozygotic twins indeed share essentially the same genetic material while dizygotic twins are not genetically more similar than brothers issued from different gestations.

Variability between studies could come from random fluctuations or bias in sampling but could also relate to the degree of morphological in utero interaction between the twins, a factor that has, to my knowledge, never been considered in these studies. Monozygotic twins can indeed develop with two separate chorions and two separate amniotic sacs, or with two amniotic sacs but one single chorion or with one amniotic sac and one chorion for both ( Bermudez et al., 2002; Cordero et al., 2005). The degree of interactions between these types of twins and the possibilities of exchange of biological material (hormones, cells) are therefore quite variable and might impact the degree of concordance in sexual orientation.

More recent work has revised these estimates towards lower values ( Bailey et al., 2016) but clearly confirms the systematic difference in concordance of sexual orientation between the two types of twins (See Fig. 4 ). Some studies have also extended this difference to lesbians.

Two types of studies based on different methodologies to recruit subjects have addressed this question. Targeted studies recruit homosexual populations explicitly via advertisements or direct contacts. In contrast in registry studies, the population of interest is randomly selected based on preexisting registries. The first of these two approaches is vulnerable to sampling bias because potential subjects will presumably decide to participate or not based in part on their twin's orientation, which could lead to an overrepresentation of concordant pairs (participating may create tension between twins if the pair is discordant) ( Kendler and Eaves, 1988). In addition, for purely statistical reasons, pairs of homosexual twins are more likely to be contacted than twins with a different orientation ( Torrey, 1992), which could also inflate their representation.

The observed results clearly confirm these suspicions: the percentage of concordance is almost always higher in targeted than in registry studies and the difference between monozygotic and dizygotic twins is larger (52 versus 17% compared to 25 versus 13%). This highlights the challenges of studies analyzing such a complex phenomenon in humans. This being said, it has to be noted that the difference between the two types of twins always goes in the same direction; this is true in studies of males, of females and in studies analyzing both sexes. These data therefore support the idea that sexual orientation has, at least in part, a genetic basis unless one postulates effects on sexual orientation of difference in education between the two types of twins, but such effects have never been reported to this date.

5.2. The Linkage to Xq28

Although solid data support the conclusion that genes significantly influence sexual orientation, the search for the specific genes that are implicated has proved extremely difficult. A pedigree study identified an excess of gay uncles or first cousins (13.5 %) in the maternal lineage of homosexual men, as compared to the paternal lineage or to the general population ( Hamer et al., 1993). This heritability was pointing to a control based on genes located on the X chromosome that specifically inherited from the mother, even if alternative mechanisms are possible. Hamer and collaborators therefore recruited pairs of homosexual brothers without evidence of paternal inheritance (subjects were excluded if the father was homosexual) and examined by linkage analysis 22 markers distributed along the X chromosome. Pairs of homosexual brothers were found to share markers located in the terminal region of the X chromosome called Xq28 ( Hamer et al., 1993). This linkage was significant (33 pairs out of 40) but based on a relatively limited sample size.

Until recently, three studies had attempted replicating this finding, some with positive ( Hu et al., 1995; Sanders and Dawood, 2003), some with negative ( Rice et al., 1999) results. The analysis of these combined results still yielded a significant probability of this association with Xq28 but there was only a statistical trend if the initial positive study is excluded (see ( Bailey et al., 2016; Bocklandt and Vilain, 2007; Dawood, 2015).

With the advances in sequencing techniques, data related to this question began to accumulate around the beginning of this century. In 2005 Mustanski and collaborators published a first full genome analysis of 456 individuals from 146 families with two or more gay brothers ( Mustanski et al., 2005a). They reported associations of homosexuality with loci located on chromosomes 7, 8 and 10 but failed to replicate a clear linkage with Xq28. As discussed in that paper, this discrepancy could be due to methodological problems.

In 2015, Sanders and collaborators published a DNA linkage analysis based on more than 400 homosexual brothers (908 individuals) confirming the Xq28 linkage ( Sanders et al., 2015) suggesting that this chromosomal region still represents an interesting target for future investigations.

To date, no investigation has related a specific gene located in Xq28 to homosexuality. However, the human genome has now been fully sequenced and this work has identified a few interesting candidate genes (see ( Sanders et al., 2015) for discussion). For example, the arginine-vasopressin (AVP) receptor 2 (AVPR2) is located in Xq28 and AVP is known to play a key role in the control of social and affiliative behaviors ( Balthazart and Young, 2014). Modifications in the AVPR2 gene or in its expression could therefore have an impact on sexual orientation, although expression of this gene is limited in the brain and more present in peripheral structures such as the kidney.

Another Xq28 gene mentioned by Sanders and collaborators is the cyclic nucleotide gated channel alpha 2 (CNGA2), a gene that is expressed in the human brain and is critical in mice for the control of odor-evoked sociosexual behaviors, including odors related to the Major Histocompatibility Complex (MHC) ( Mandiyan et al., 2005; Spehr et al., 2006). The contribution of olfaction to human sexual orientation is not firmly established but differential hypothalamic responses to olfactory compounds with presumed pheromonal activity have been identified in gay compared to straight men ( Savic et al., 2005) and in lesbian compared to heterosexual women ( Berglund et al., 2006) as well as in gender dysphoric children, a condition associated with a high probability of being homosexual when adult ( Burke et al., 2014). Odors, in particular MHC-related odors, and the CNGA2 gene located in Xq28 may thus have relevance to sexual orientation in humans ( Havlicek and Roberts, 2009; Milinski et al., 2013; Wedekind et al., 1995).

Interestingly, genes of the melanoma-associated antigen (MAGE-A) family are also located in Xq28. MAGE-A11, a gene in this family, encodes for a protein that has been recognized as a co-activator for the androgen receptor and is namely transcribed in the prostate ( Karpf et al., 2009). MAGE-A11 prostatic expression is markedly upregulated by castration (100-1500 fold) by an epigenetic mechanism based on the hypomethylation of a CpG island in the promoter of the gene. This provides a mechanism potentially explaining the increased androgen sensitivity in prostate cancers after prolonged androgen deprivation ( Karpf et al., 2009). This Xq28 gene that is also expressed in multiple parts of the human brain including the olfactory bulbs, the hypothalamus, amygdala and prefrontal cortex (see: http://biogps.org/#goto=genereport&id=4110) could help to explain homosexuality. A mutation or an epigenetic modification of its expression taking place in the brain should indeed result in a decreased brain androgen sensitivity and thus androgen action, a factor that has been postulated to take place during early development in gay males (see section 4).

This mechanism would additionally provide a "bridge" between studies that tried to explain homosexuality by genetic or by hormonal factors (see sections 4 and 5 of the present review) ( Bocklandt and Vilain, 2007; Ngun and Vilain, 2014). To represent a viable mechanism explaining male homosexuality, a change in MAGE-A11 expression would, however, have to change sensitivity to testosterone specifically in the brain, since no decrease in somatic androgen-sensitive structures, such as penile size, is systematically associated with masculine homosexuality (if anything a larger penis is present in gay men but the interpretation of these data is questionable; ( Bogaert and Hershberger, 1999)). Such a mechanism would also beg the question of how this change in expression of the androgen receptor co-regulator can be heritable. A mutation would obviously be transferred to the next generation but this is less clear for an epigenetic modification of expression as observed in the prostate after androgen deprivation, even if recent work has identified trans-generational inheritance of epigenetic marks and correlated physiological changes ( Klosin et al., 2017; Morgan and Bale, 2011) (see also next section).

5.3. Other loci associated with male homosexuality

Besides Xq28, the different studies performed so far have identified linkages to several other loci located at least 6 different chromosomes ( Ganna et al., 2019; Mustanski et al., 2005b; Sanders et al., 2017; Sanders et al., 2015). The large linkage study of Sanders and colleagues (908 individuals) namely confirmed a previously identified ( Mustanski et al., 2005b) linkage to the peri-centrometric region of chromosome 8 with a multipoint support peaking at 8q12 ( Sanders et al., 2015). The association of this locus with homosexuality was actually more significant than for Xq28. This chromosomal region contains several genes that could in theory be functionally linked to the homosexual preference. These genes include micro RNAs, transcription factors or genes known to be expressed in the brain including genes coding for factors related to neurotransmission, neuroendocrine function or brain development but no specific functional link can be highlighted at this point.

Genetic analyses of complex traits often have a limited power due to insufficient sample size. Given the complexity of homosexuality, this also applied to some extent to the Sanders et al. ( Sanders et al., 2015) study despite the inclusion of more than nine hundred subjects. In the summer 2019, an international collaboration between over 20 researchers published a much larger Genome Wide Association Study (GWAS) based on five cohorts of subjects totaling 492,678 genotyped individuals that should potentially not be subjected to this kind of limitation ( Ganna et al., 2019). However, given this large sample size, the phenotypic characterization of the subjects was limited to self-reports by the participants indicating whether or not they ever had same-sex sexual behavior, an obvious limitation but balanced by the extremely large sample size.

The study first confirmed the heritability (percentage of the trait attributable to genetic variations) of male and female homosexuality to be around 32% consistent with the results of previous twins studies ( Langstrom et al., 2010); related individuals were more likely than expected by random sampling to display concordant behavior.

The analysis of small nucleotide polymorphism (SNP) in these genomes discovered five loci that correlated with same-sex behavior. Two loci concerned both sexes while two were specific to males and one to females, suggesting that the genetic bases of homosexuality are different in men and women, which was indeed anticipated based on previous phenotypical studies ( Bailey et al., 2016). These five loci contain genes associated with olfaction (several olfactory receptor genes) and others related to the production of sex steroids, including TCF12, a heterodimerization partner for TCF21, a transcription factor critical for gonadal development in mice ( Ganna et al., 2019). These genes could represent links to homosexuality that seem related both to detection of sexual olfactory signals and alterations of the early steroid milieu but no specific link has been established to date.

Unexpectedly this study did not identify links with loci on the X chromosome but it must be remembered that the selection of subjects was here based on the mere presence/absence of same-sex behavior, not of a (more or less) exclusive homosexual preference and it is well-known that same-sex behavior can have other origins and is more widely distributed than exclusive homosexual preference. In addition, there was in the Ganna et al. study ( Ganna et al., 2019) no additional selection of the subjects who experienced same-sex behavior while Hamer and collaborators performed their study specifically on a population of subjects with no paternal (presumed maternal) inheritance ( Hamer et al., 1993). These methodological differences potentially explain the discrepancy in results.

The limited magnitude and observed variability of these associations with genes (see ( Ngun and Vilain, 2014) for additional descriptions of these associations) indicate that each of these genes only has a limited effect. The control of sexual orientation is, as might be expected for such a complex behavioral trait, associated with an oligogenic inheritance, i.e. a stochastic variation in the linkage with a specific locus while multiple loci are implicated. Practically this means that although the heritability of homosexuality is unquestionable and probably explains around 30 % of the variance in sexual orientation, the idea of a prenatal genetic test for homosexuality is impossible since the small magnitude of effect of each single loci would make such a test essentially useless. There is therefore no reason to ban research on the genetic bases of homosexuality and it should even be encouraged since there is factual evidence showing that there is a positive correlation between the individual's opinion on the causes of sexual orientation and their view about homosexuality: people who accept the idea that biological factors are important more often hold positive attitudes and believe there is nothing wrong about same-sex sexual orientation ( Bailey et al., 2016).

6. Epigenetic effects and the older brother effect

Together, data reviewed in the two previous sections provide evidence for biological controls of sexual orientation including hormonal and genetic factors. The contribution of these factors is however only part of a multifactorial causation that has not been fully uncovered at this time. Hormonal factors only explain part of the variance ( section 4) and the same is true for genetics ( section 5). This is clearly illustrated by the fact that monozygotic twins who share the same genome are only concordant for sexual orientation in at best 50-60% of the cases and usually much less (see Fig. 4 ). Additional causal factors thus need to be identified.

6.1. Epigenetic modulation of androgen action

At the endocrine level, it has been pointed out that in humans ( Bocklandt and Vilain, 2007; Mustanski et al., 2005b) and even in rats ( Rahman and Wilson, 2003; Weisz and Ward, 1980) that are best studied, during most of the embryonic life testosterone concentrations overlap between males and females even if males have on average higher concentrations. The difference in plasma testosterone concentrations is therefore an ambiguous sexual signal that cannot explain alone the sex-specific phenotypes. For example, the undifferentiated genital tubercle develops into a phallus under the influence of testosterone while a vulva and clitoris will develops in the absence of this steroid but this sexual differentiation of the external genitalia takes place in rats and humans during a period of embryonic life when testosterone concentrations overlap between the sexes ( Mustanski et al., 2005b; Perera et al., 1987; Reyes et al., 1974). Given that a discordance between genetic sex and sex of the genitalia is extremely rare, it becomes necessary to invoke additional factors that should be in action to organize the sexually differentiated phenotype.

In this context, Rice and colleagues described complex genetic and epigenetic mechanisms acting very early during fetal development that contribute to increase the sensitivity to testosterone in males and decrease it in females (see Fig. 5 ) ( Rice et al., 2012).

Specifically, testosterone action is modulated by a variety of mechanisms at multiple levels in the circulation and at the level of target cells. First, the sex hormone binding globulin (SHBG) that binds testosterone in the blood and therefore restricts its uptake by target cells is approximately 50% more concentrated in female than in male human fetuses ( Hammond et al., 1983) and this should decrease the sensitivity to testosterone in the XX subjects ( Hammond, 1995). Second, expression of the 5α-reductase-2 gene coding for the enzyme that catalyzes the transformation of testosterone into 5α-dihydrotestosterone is three times higher in the urogenital swelling and genital tubercle that will produce the penis of XY than in XX fetuses ( Wilson et al., 1993) and there is evidence that this enzymatic difference is not controlled by androgens ( Boehmer et al., 2001). Since it is firmly established that the sexual differentiation of the genital structures in males depends on the 5α-reduction of testosterone - mutations of the enzyme result in intermediate or feminine genital structures ( Imperato-McGinley, 1994; Imperato-McGinley and Zhu, 2002) - this enzymatic sex difference clearly contributes to the differentiation of the genital phenotype even in the presence of overlapping concentrations of circulating testosterone in male and female fetuses. Sex differences in androgen receptors and in their co-activators and co-repressors could additionally modulate responses to androgens in the target cells, including in neuronal structures that mediate sexual orientation or gender identity. Some studies actually identified differences in the gene structure of sex steroid receptors ( Fernandez et al., 2014; Henningsson et al., 2005) in transgender individuals and the same might be true in relationship with sexual orientation. These changes in gene structure likely modify the expression of the corresponding receptors and thus the sensitivity of target structures to circulating steroids. Sex steroid receptors also use different co-activators and co-repressors in different organs and thus in the brain to control transcription ( Charlier, 2009; Chen, 2000; Shibata et al., 1997) and it is conceivable that different epigenetic marks transmitted across generations potentially affect subsets of sexually dimorphic traits. This could explain why a control by androgens of sexual orientation could be effected in the absence of any effect of the genitalia.

The organizational actions of androgens on sexual orientation could thus be canalized towards a specific endpoint by the cooperation of multiple mechanisms enhancing or decreasing androgen action in specific targets. This canalization ( sensu ( Waddington, 1942)) is potentially mediated by micro RNAs that are known to modulate sex differences in mRNA concentrations in the mouse brain ( McCarthy and Nugent, 2015) and by epigenetic marks ( Nugent et al., 2015) that have now been demonstrated to be heritable across one and possibly more generations ( Bale, 2015; Klosin et al., 2017; Morgan and Bale, 2011; Rodgers et al., 2015) (See ( Kaiser, 2014)). This idea is supported by the observation that, in most cases, girls affected by congenital adrenal hyperplasia are born with genital structures are only partly masculinized ( Hall et al., 2004) and although they display an increased incidence of homosexuality, almost 50% of them are still heterosexual ( Money et al., 1984). All this despite the fact that they have been exposed throughout most of their fetal life starting at the seventh week of gestation to an excess of adrenal androgens sometimes equivalent to the concentrations observed in fetal males ( New, 2004; Speiser and White, 2003; Trakakis et al., 2009).

Rice and collaborators have presented a mathematical simulation demonstrating the feasibility of the control of sexual orientation via sexually antagonistic epigenetic marks modulating androgen-sensitivity in a sex- and tissue-specific manner (see ( Rice et al., 2012) for a full presentation). By sex-reversing brain sensitivity to androgens epigenetic marks could sex reverse sexual orientation. These marks may or may not escape erasure in the primordial stem cells and zygote, and, if occasionally inherited, they would explain the limited but clearly demonstrated heritability of homosexuality, as well as the difficulty in identifying clear genetic markers of homosexuality (see section 5).

6.2. The asymmetrical inactivation of the X chromosome

6.3. The older brother effect

Thanks to the extremely large sample size in these aggreate studies, the authors were able over the years to rule out by multiple regression analyses the most obvious biological factors that were potentially implicated such as the age of the mother or of the father, the social influence of other boys living in the family or other peculiarities in the education within a family ( Bogaert and Skorska, 2011). The FBO effect ended up being the best-documented phenomenon associated with male homosexuality but its bases remained unclear.

The effect was clearly related to the multiple male pregnancies experienced by a women since it was not present for example in a family where the father had divorced and remarried a woman who had no male children before. The fact that it was associated with a decreased body and brain weight at birth suggested that the developmental pathway to homosexuality triggered by older brothers was in fact initiated during prenatal life ( Blanchard, 2004). Based on the available evidence, the authors came to the conclusion that the only possible mechanism had to be based on a progressive immunization against a male antigen of the mother bearing male embryos. In this scenario, antibodies would accumulate in the mother's blood over successive pregnancies and increasingly interfere with the development of the male embryos, similar to what happens in the hemolytic disease of the newborn where a rhesus negative (Rh-) mother mounts an immune response against the Rh factor if gestating to a Rh+ fetus and eventually causes hemolytic disease in subsequent Rh+ fetuses (see ( Bogaert and Skorska, 2011)). To be viable, this maternal immune hypothesis (MIH) had to fulfill several conditions: a) some embryonic material should enter the mother circulation and this material should cause immune responses in females against male proteins, b) these proteins should be important for brain development and this role should be affected by specific antibodies against them, and finally c) antibodies to these male proteins should persist in the mother's blood so that an incremental immune response could build up after multiple male pregnancies.

These very specific predictions allowed selecting, based on existing biomedical knowledge, a list of 4 male-specific proteins fulfilling these criteria ( Bogaert and Skorska, 2011) and recently a study experimentally tested the hypothesis by quantifying in the blood of women with diverse reproductive histories antibodies directed against the two most likely candidate proteins namely protocadherin 11 Y-linked (PCDH11Y) and neuroligin 4 Y-linked (NLGN4Y). These antibodies were quantified in blood samples coming from 54 mothers of gay sons, including 23 who had previously given birth to a straight son, and control samples of 72 mothers of heterosexual sons, 16 women with no sons and 12 men ( Bogaert et al., 2018).

This research demonstrated that overall, women have a higher blood concentration of anti-NLGN4Y antibodies than men but more importantly that, after controlling for the number of pregnancies, mothers of gay sons, especially those with older brothers, had significantly higher concentrations of antibodies against NLGN4Y levels than control women, including mothers of heterosexual sons (i.e., women with no sons < mothers of heterosexual sons < mothers of gay sons with no older brothers < mothers of gay sons with older brothers) ( Fig. 6 ).

After an initial antigen exposure antibodies often disappear relatively rapidly from the blood with a half-life of just a few weeks ( Crotty and Ahmed, 2004). Interestingly, the antibodies and NLGN4Y that were quantified here were still present many years after the last pregnancy and birth of a son. This should be made possible due to the existence of long-lived plasma cells that replenish the supply of antibodies or to memory B cells that could be re-stimulated by the antigen via male microchimerism (see ( Bogaert et al., 2018) for discussion).

7. Social Factors

We focused in this review on the biological mechanisms that have been shown to contribute to the determinism of sexual orientation. In contrast, it is often claimed that sexual orientation, and in particular homosexuality, is controlled by the social environment during childhood and this view is broadly shared in the general public. This approach has been described and evaluated in detail by a recent review ( Bailey et al., 2016).

In this context, psychoanalytical theories have constantly held dysfunctional relationships between the parents and their child (emotionally distant fathers and/or overbearing mothers) responsible for the development of homosexuality. These hypotheses are however only based on speculative interpretations of anecdotal evidence. Scientific evaluation of these theories has returned little positive evidence ( Bailey et al., 2016) except for the fact that pre-homosexual children tend to have more distant relationships with their parents, especially their father. It should be noted that these children also often tend to display gender nonconforming behavior, which may likely be the cause, not the consequence, of the difficult relationship with their father ( Kane, 2006).

This being said, it is admittedly difficult to conceptualize how the action of a single hormone or few genes could control a trait as complex as sexual orientation. One partial possible solution to this problem is suggested by a study of Melissa Hines and colleagues on young girls suffering from congenital adrenal hyperplasia (CAH). She found that these girls exposed prenatally to an excess of androgens due to their genetic condition are less responsive than control girls to information indicating that particular objects are for girls or for boys ( Hines et al., 2016a). CAH girls who were repeatedly told or shown, via short video clips, that a given object or toy is for girls or for boys did not use this information later to select a given object or toy nor to state what they prefer while control girls did. This experiment therefore indicates that prenatal testosterone modifies processes involved in socialization of gendered behaviors. Whether this effect expands to sexual orientation remains however to be evaluated.

8. Conclusions

Additional investigations will be needed before we can provide a more complete and unifying theory of sexual orientation. At present, we are only left to speculate that either the different biological mechanisms (hormonal, genetic and immune) each explain a fraction of the cases and male homosexuality is a heterogeneous phenomenon that has multiple independent origins in different subjects, or alternatively that these different mechanisms interact and complement each other in some way to control a phenotype that is otherwise essentially homogeneous. Evidence has been presented indicating that this heterogeneity in the mechanisms influencing sexual orientation (hormones, genes, FBO) is indeed present ( Swift-Gallant et al., 2019). It has also been suggested that male homosexuality could be the result of opposite influences at the endocrine level and would be induced or at least favored by both lower and higher than usual exposure to androgens during prenatal life ( Swift-Gallant, 2019). This possibility should clearly be investigated further. It is intellectually easy to draw links between the endocrine and genetic mechanisms: a genetic mutation or variant can for example modify the secretion or action of sex steroids in the brain (e.g., MAGE-A11 gene located in Xq28 that would modify androgen action in the brain). The interaction between the immune mechanisms discussed here in the context of the FBO effect and the endocrine-genetic mechanisms is in contrast less obvious.

It may alternatively be hypothesized that even taken together these prenatal biological factors do not determine the sexual orientation but that they only control predispositions that must interact with specific aspects of the post-natal environment to fully crystallize a given sexual orientation. These postnatal factors remain to this date completely unidentified but the research of Melissa Hines on CAH girls ( section 7) suggests interesting tracks for future research.

To some extent, the Nature-Nurture debate thus remains open even if a lot of data indicate that sexual orientation is an essential trait of a person (Nature) while almost no scientific evidence has been collected demonstrating a role of the postnatal environment (Essentialism versus Existentialism or Constructivism). These two approaches however do not need to be mutually exclusive and any trait in an adult phenotype always results from an interaction between genetic or pre/perinatal biological influences and post-natal experiences. Furthermore, these two types of effects are not independent: the postnatal environment experienced by an individual is not shared with anybody including his/her brothers and sisters or even his twins. Based on a variety of determinisms, each individual lives into his/her own environment and is actively seeking specific stimuli and interactions (the " Umvelt" of Jakob von Uexküll). There is therefore no Nature-Nurture dichotomy in the mechanisms that control the development of an adult phenotype and this also presumably applies to sexually differentiated traits such as sexual orientation.

​

Early testosterone action organizes sex differences in brain and behavior

Human homosexual orientation is similarly affected by early testosterone action

Human sexual orientation is partly heritable but influenced by multiple genes

Incidence of male homosexuality increases by 33% for each older brother

There is more evidence supporting biological than social causes of homosexuality

Acknowledgments

Research of my laboratory on the sexual differentiation of sexual behavior was supported from 1993 to 2020 by NIMH grant MH50388 to Gregory F. Ball, Charlotte A. Cornil and myself. However my literature search concerning the biological bases of human homosexuality did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Footnotes

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References

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Articles

Frank S. Robinson stands up for the free market.

Capitalism's critics triumphantly proclaim that this rotten system of greed, exploitation, and social injustice is now discredited as a failure. 'Corporate' and 'capitalism' are curse words. I will offer a different view: that the free market has not failed, is not morally bad, and in fact serves deep human values. This is not to disregard its downsides, and, yes, victims. We must pay heed to them, and various reforms might help. But it's mistaken to imagine society as a whole being better off with some radically different system.

First, free market capitalism has not failed. We have suffered from big mistakes and abuses in financial and credit institutions. The banks, investment houses, trading firms, and mortgage outfits perform a function within the larger system, facilitating flows of money. That's analogous to your car's carburetor: it's needed to make the engine run, but it's not the engine. The economy's engine, the true heart of capitalism, is not Wall Street or the City: it's the production of goods and services, rightly called 'the real economy'.

That's what Adam Smith's 1776 book The Wealth of Nations was about: showing how a free market in products benefits society. Some today dismiss his theory as reflecting a na ïvely idealized view of commerce. Not so. Smith was in fact caustic about businessmen's venality; but his key point was that in a free market such self-interest leads them to provide goods we want efficiently and affordably (or else they couldn't be sold). The market is a vast information-driven system, matching up supply and demand - Smith's 'invisible hand'.

This classical idea of free market efficiency, as devolving from rational self-interest, has also been derided lately. Alan Greenspan, ex-Chairman of the U.S. Federal Reserve, notably spoke of his mistake in thinking that the self-interest of Wall Street operators would serve to counteract market excesses. Furthermore, science has shown that emotions can undermine rational decision-making, and often people don't even understand their own interests or desires.

This argument against market economics might be correct if people were never rational. Yet, though imperfectly we do employsome considerable rationality in how we pursue self-interest. And free market theory does not assume every economic decision is rational. It merely assumes that your free choice is more likely to improve your welfare than if you don't have any choice; and that society as a whole is better off the more such freedom there is.

Some banks and traders did make bets that in hindsight proved disastrous. Yet even if financial markets are more prone to go haywire than markets in goods and services, demonization of the former is overdone. Greece blamed those perennial scapegoats, 'speculators', for the shredding of its credit. Well, there was indeed speculation among bond traders that Greece's debts would prove unpayable. That was hardly irrational. The financial markets performed the desirable function of spotlighting Greece's unsustainable profligacy. 'Shoot the messenger' is not the proper response.

However, again, the real economy concerns not financial speculation, but the production of more down-to-earth goods and services. Even there, mistakes can be made - remember the Edsel car? - but by and large businesses pursue profit rationally, by meeting customer desires in an efficient manner. That is the essence of free market theory, and nothing in behavioral science or recent history disproves this theory or negates the fact that, in the big picture, it works. The real economy has stumbled, but words like 'collapse' are wildly overblown. Capitalism continues to chug along generating comfortable incomes for the great majority, and resources to help the rest.

No one believes the market is always right, or answers every societal concern. That's a straw man caricature. Government does play a necessary role - not running the economy but facilitating it, and ameliorating capitalism's acknowledged downsides.

Free market believers have been labeled simply deluded, because markets are never free. Perfectly free? Well, nothing ever is. That hardly refutes the belief that more freedom is better than less. We do accept laws to regulate human conduct - to prevent arson, murder, jaywalking, etc - and likewise, businesses too are restrained from harmful, antisocial conduct. Thus nobody advocates 'unrestrained' capitalism either. That's another straw man. In fact, businesses must be regulated to protect the free market's freedom - to keep markets open and competitive - with government as referee. That's what 'unfettered' capitalism should really mean.

Consumerism is Necessary

Free enterprise does do the job Adam Smith described, giving us a cornucopia of goods and services. This is often denigrated as 'materialist consumerism' - some sort of offense against virtue into which we're somehow manipulated. But Howard Bloom's book The Genius of the Beast (2009) explores how our purchases reflect deep, ineradicable emotional needs, most prominently the assertion of self-identity. We are highly social animals, and a lot of our spending is governed by its anticipated effect on our relationships. Businesses make money not, primarily, by conjuring up false desires, but by identifying and satisfying real ones. If you think about it, the bulk of your spending goes not on needless fripperies, but things you consider indispensable. (Ironically, critics of 'materialist consumerism' often also bemoan the inequality that keeps the poor from fully participating in it.) Moreover, the production of goods and services is what gives most of us the jobs and incomes enabling us to buy them. With no consumerism there would be no such jobs. A fine virtuous society we'd have then.

Sneer if you like at our cushy modern affluence - our comfortable homes, abundant food, recreation and entertainment, health and longevity - but please compare it against the lives of our forebears, which Thomas Hobbes characterized in Leviathan (1651) as "poor, nasty, brutish, and short." This vast uplift has occurred by the grace of free market economics. In the past century, average real worldwide incomes rose five-fold, or 500%. The average human today lives five times better than in 1900. That gain did not come from the world's socialist economies.

Now, some commentators denounce such economic growth as a perverted lust we could do without, urging us to embrace simpler lives. Easy to say, perhaps, when you're in our modern cocoon of comfy affluence. But for the world's poor, economic growth is their road out of squalor. Every percentage point of economic growth for a society tends to reduce the numbers in poverty by two percent. In the last two decades, a billion people have climbed from extreme poverty to a decent living standard. That is capitalism's most fundamental human value.

Competition is Freedom

Competition is an essential element of free market economics. Businesses never gain permanent advantage: there are always alternative ways to satisfy demand. Economist Joseph Schumpeter called business 'creative destruction' - a never-ending Darwinian struggle. Like a new predator in an ecosystem, an innovative new competitor can wreak destruction upon rival firms. The list of top companies is continually changing.

Thus in a genuinely free (i.e. competitive) market, corporations don't control the economy - they block one another from such power. It's mainly government intervention that confers such control on business, through protectionism against competition, for example. French consumers gripe that even French products are cheaper in Germany. Why? Because numerous French laws shield businesses from competition. They even have laws against price-cutting. This reflects French beliefs that competition is 'harsh', and its opposite is 'social solidarity'. In fact, the opposite of market competition is monopoly and privilege.

But when competitors battle for market share, the real winners are consumers, who pay less for more. Air travel is a perfect illustration. Once, flying was heavily regulated, and only for the rich. Deregulation and competition opened it to the masses. If airlines profit too, we shouldn't begrudge this. But in fact, thanks to competition, the industry's cumulative profits over its entire history total approximately zero. So here, all the benefit has gone to consumers, and none to the 'greedy capitalists' who made it possible. Talk about economic injustice!

Another example is TV. In my childhood, three major networks ruled supreme in America. Then along came cable and VCRs, cutting the heart out of their business model. A whole new video sale and rental industry sprang up. This was challenged by Netflix, with another way of serving consumers. And now Netflix's lunch may be eaten by Redbox, with a newer idea still. Creative destruction.

Profit is Productive

I recall a newspaper column decrying that the American healthcare system 'now' has 'making money' as its primary mission. Well, healthcare workers do need to make a living - just as the columnist provides columns to make a living. And why shouldn't you expect to pay for what you receive, so the providers earn profits?

The word 'profit' gets mixed up with 'greed'. But isn't it natural to prefer having more rather than less? Adam Smith's most famous line was that "It is not from the benevolence of the butcher, the brewer, or the baker, that we expect our dinner, but from their regard to their own interest." Greed is bad when it's fed at others' expense; but those tradesmen feed others, and so their desire to profit thereby is good, not bad. It leads them to provide your dinner, and to make it as tasty as possible so you'll come back tomorrow. And yet, while we do honor the worker who earns money by producing something, still many condemn the businessman who earns a lot of money by producing a lot of things.

Capitalism's critics say it does impel people to feed their greed at the expense of others, and of their own integrity: it's a rat race, where only the rats win. But some will always act like rats whatever the economic system. Fascism, socialism, and communism all engendered their own (far deeper) moral corruptions, without the free market's benefits. Democratic politics also impels people to make moral compromises, even to lie and cheat, to achieve their aims - but that is no argument against democracy. Things are even worse without it. Similarly, that businesses sometimes do bad things doesn't make capitalism intrinsically rotten. Just as most citizens earn their livings honestly, most businesses profit not by exploiting, but rather by serving people. Properly understood, the raison d'être of any business is not simply profit, but to profit by creating value for customers.

The essence of a free market economy is exchange. It's not a zero-sum game: when two people trade, each gets something she values or needs more. That makes society richer. In this kind of economy, you do what you're best equipped to do and trade for your other needs, circumstances allowing. This system enables the division of labor, the specialization, that also makes us all richer. And, as shown in Matt Ridley's book, The Rational Optimist (2010), trade speeds the dispersion of ideas. Indeed, mirroring biological trade - i.e. sex, which creates more diverse, adaptive, and successful organisms - economic trade is the equivalent of ideas sexually reproducing. The result is more and better ideas, and a richer world.

In addition, a trading ethos rewards moral behavior, because building trust among participants benefits all. A free market economy also fosters the virtues of prudence, diligence, foresight, and inventiveness. It encourages cooperation and collaboration to achieve desirable ends. And if you want a utopia where everyone is busy helping others, try a free market society, because that's how its members prosper - by giving others something they value, whether it's goods or services or labor.

The Market is Pro-Democracy

The most important moral dimension of free market economics is that it is, indeed, free: it involves people seeking to flourish in their own ways. Any alternative has required coercion, forcing people to relinquish what they personally strive for. This isn't just about material self-interest. As Hegel explained, such freedom enables us to satisfy not merely our animal needs, but our deepest desires for dignity and self-worth.

Moreover, as The Economist said on January 16, 2010 (p.60), "democracy has never endured in countries with mainly non-market economies" because their concentration of political and economic might "sucks the air away" from the diversity of power centers that coexist in a free economy. Those who believe corporate power is a problem should think twice about merging it with the vast power already wielded by government. Would we want a society where the state is everything - the state our one shepherd, and we its sheep?

The market is also democratic in its results. Rewards are mostly not garnered through political or hereditary privilege, but from people's willingness to part with cash for value received. What counts most is not who you are, but what you do. It's precisely because the market is so 'vulgarly democratic' that the elitist Left hates it so, as Irving Kristol remarked in Neoconservatism: The Autobiography of an Idea, p.208 (1995).

This 'vulgar democracy' is just what America was set up to achieve. Older societies were based around landed aristocracy and/or might-makes-right - not so good for ordinary people. America was instead organized around free commerce, which its founders believed would make for a better kind of human being, with all the stalwart virtues I've mentioned - self-disciplined, industrious, innovative, ambitious - with the resulting promotion of the general welfare. And free enterprise has not only made America prosperous, but a vibrant, dynamic, and progressive society as well.

Wealth is Good

The chief indictment of capitalism centers upon inequality.

Let's clarify this issue. Poverty is a bad thing. Wealth is the opposite to poverty. But some people apparently believe wealth somehow causes poverty, and hence wealth is bad too.

This reflects a zero-sum concept of capitalism, with a few individuals profiting at others' expense, as though there's only a fixed amount of wealth in the world, the rich take more than their share, and every dollar gripped by a capitalist makes some peasant a dollar poorer. But wealth is expandable. And although of course some people gain wealth parasitically, most is gained by productiveness, which increases society's overall riches - it's not taken, but earned, through making others better off, not worse off. Thus it's wrong to think that wealth causes poverty.

Wealth is created by productive human effort, it doesn't fall like manna from Heaven. So we need the rich. More precisely, we need the opportunity for gaining riches, which motivates people to the efforts that make us all better off. When everybody is working to get ahead, it's one big human betterment machine.

A recent book by Gar Alperovitz and Lew Daly, Unjust Deserts, makes a counter-argument: that the true source of wealth is not individuals, but society itself. Its infrastructure, educational system, and accumulation of knowledge, supplies the platform for the production of riches. Hence, they contend, everyone deserves equal shares in the wealth it produces.

It's true that society makes wealth possible, and that this justifies disproportionately taxing the rich, which we already do (over half of U.S. income tax revenue comes from the top 5% of payers; almost a third from the top 1%). But does everyone deserve an equal share irrespective of their contributions? That unjustly devalues individual effort. And if you're guaranteed an equal share regardless of how hard you work, why work hard? That was the real downfall of communism. The proletarians used to say, "We pretend to work, and they pretend to pay us."

It's also been argued, by Rob Buitenweg, in Human Rights, Human Plights in a Global Village(2007), that all wealth ultimately derives from force, manipulation, exploitation, etc - so that social justice requires seizing and redistributing the riches. Since you're reading this, your wealth is probably in the top few percent globally. Did you get it by ripping off the poor? Or mainly by doing good things for which you profited, or were deservedly paid? Admittedly, the rich can exploit their power to gain undue advantage. It's unrealistic to imagine any social model where no one has undue influence. It's certainly not socialism or communism. But at least in a free economy power is greatly constrained by competition. If you're profiting unduly, someone will find a way to stymie you by offering a better deal. Further, in a democracy, the rich are ultimately at the mercy of the masses through voter-driven legislation. That's why the rich pay disproportionate income taxes.

'Social justice' language is problematic because while some poverty may be rooted in injustice, much is just misfortune, and so uplifting the poor should not hinge on blaming their plight on the rich: it is instead simply humane. And what is the so-called social justice alternative to capitalism? Some in this field talk (vaguely) of a 'sharing society' where we all take care of each other. That's a noble idea, but the problem, again, is that there won't be that much to share if people aren't motivated to produce it by the prospect of advancing themselves.

Leftists worry too much about wealth distribution, and not enough about generating wealth in the first place. They want to cut open the goose that lays golden eggs (and you know how that turned out). In the resulting society, the poor would therefore be even worse off than under capitalism, which at least generates lots of resources for helping them. The real redistributionist challenge is to spread not the fruits of productiveness, but productiveness itself - to create the opportunities for people to prosper through their own efforts. And people are happier when they accomplish their own prosperity than when receiving unearned largesse.

Self-created prosperity is indeed what capitalism has achieved. In developed capitalist societies, the great majority earn decent living standards, and even our 'poor' should actually be rated as 'rich' on any comparative global or historical assessment.

Success is Just

A leading egalitarian philosopher was John Rawls, who in A Theory of Justice (1972), posed the question of what kind of society you'd choose under a 'veil of ignorance' - that is, not knowing what advantages or disadvantages you'd have in it. Rawls opined that people's advantages are basically undeserved luck, which should be tolerated only if the system involved benefits the less advantaged even more.

In reality, success in life is molded by both luck and pluck. Many born with lucky advantages squander them, while many born disadvantaged nevertheless prosper through hard work, enterprise, and drive. Yet having such personal qualities can also be considered luck; and that's the playing field Rawls would need to level. A better concept for a level playing field is not everyone achieving the same score, but to apply the same rules to everyone. Equalizing the score would require holding back the stronger players; but society does not gain by squelching people with talent and drive, or redistributing away the fruits of their efforts. Instead, we're all best served if such individuals are encouraged to make the most of their gifts. That's how we all best benefit from the prizes given out in life's lottery.

Rawls argued that choosing a society from behind the 'veil of ignorance' implies that any social contract must be egalitarian, because nobody would agree to risk his or her own poverty. However, many rational people would freely accept the risk of poverty if doing so means better outcomes overall. I'd opt for the society where the most people have the greatest opportunity to thrive. That means one with the greatest possible freedom to better oneself, not one with an equality fetish which kills the incentive for productiveness, making us all poor.

What really matters is one's absolute quality of life, not whether it's equal to someone else's. Society is better concerned with the size of the pie than of the slices. Capitalism expands the pie, so the poor can get more without anyone getting less. And there is far more social and economic justice in a free market society, where people benefit from their contributions, than in a society seeking equality by stripping its most productive members of the fruits of their sweat. Where is the morality in one set of people presuming to redistribute what others have earned? How can their opinions of what constitutes social justice be objectively validated?

Capitalism is as Good as it Gets

Capitalism is often portrayed as sacrificing some in order to benefit others, in a cold-hearted utilitarian calculus. No economic system will ever work to everyone's benefit. But capitalism at least gives most people the opportunity to flourish, and the resultant society is the richest attainable, even for the losers.

The Left talks about the 'contradictions of capitalism', but the only contradiction is that individual striving for advantage serves the common good. It's anti-capitalism that's contradictory - the idea of achieving justice by taking away what people have earned. And that this also nurtures poverty rather than solving it.

Capitalism is not perfect. No economic system ever can be, and the quest for utopia has produced rivers of blood and tears. But if we accept human imperfection, as we must, a free market economy is as good as it gets.

© Frank S. Robinson 2011

Frank S. Robinson is a former administrative law judge, and the author of five books, most recently The Case for Rational Optimism (Transaction, 2009). His blog is rationaloptimist.wordpress.com.

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Your complimentary articles Articles Capitalism's critics triumphantly proclaim that this rotten system of greed, exploitation, and social injustice is now discredited as a failure. 'Corporate' and 'capitalism' are curse words. I will offer a different view: that the free market has not failed, is not morally bad, and in fact serves deep human values.

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Trauma Bonding of Humans Compared to Dolphins

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Trauma Bonding of Humans Compared to Dolphins

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How are some relationships formed over shared trauma? How do these relationships begin, and what do they grow into? Is this the same as trauma-bonding? (Answer: not quite)
Are we sometimes pathologizing or stigmatizing the sharing of trauma? Or perhaps setting up well-meaning and caring yet strict social norms around the specific words, phrases, contexts, times, etc in which trauma can be expressed- which spur anxiety? Could it be possible that the excess demands of "perfect" social behaviors people place on themselves, thus experiencing painful social anxiety, comes from a fear of "saying too little or too much"? Of "saying the wrong thing"? And can we move towards a space of recognizing trauma as a very real part- emphasis on both real, and part- of our life, so as to integrate rather than fragment?

The magnificent human brain has evolved such that we form social, emotional human-to-human connections in a plethora of ways- (which can be wholly attributed to how here are many ways of being human and many ways for a human to be).

One such way of forming friendships and other relationships is sometimes colloquially called "trauma bonding" - that is, friendships formed when two people talk about experiences of past trauma together and becoming friends through this deeply layered experience which can be deeply empathetic, heavy, eye-opening, perspective-providing and emotion-arousing all at once.
(Please note: thisIS NOT TO BE CONFUSED WITH the official definition trauma bonding- which is the bond formed with someone who traumatizes you - which some would also call "Stockholm syndrome"- which is abusive and problematic and is to be addressed the second it is recognized).
So, bonding over trauma. I wonder at what point one decided an "appropriate level and nature of self disclosure" that became gold standard for all of humanity. As I see it- and this is an ongoing personal exploration based on lived experience, human observation, clinical work, reading mannnyy narratives of lived experience, experiencing the art of artists known to struggle with trauma and more -
Trauma is an extremely real part of our lives and narratives. Individual differences in the extent and intensity of trauma endured contribute to individual differences in the amount of trauma that composes a person's reality.
So for some people, to "trauma bond" (to form fast friendships with the first few exchanges largely centering difficult traumatic experiences) is simply an act of speaking their truths. Maybe it is a way of saying- hey, This is who I am. This is how I am who I am. This is what I am afraid of becoming. This is who I have become despite and because of being afraid. This is how I have survived. This is how I continue to survive.

This is not to say that there can't be unhealthy forms of forming relationships based purely on the exchange of trauma alone. Where trauma is used to one-up, to manipulate the other through endless trust exercises, to gaslight. Where trauma olympics are played with good intents but with often painful outcomes. This is also not to say that trauma is an essential part of one's identity- just that it is A part.

There's a different point I'm trying to explore with you all-

Which is that trauma is very much a part of one's experience, that I don't believe there is something wrong with someone who has integrated their experiences of trauma into their identity. That maybe we are sometimes pathologizing, stigmatizing or policing the way in which trauma is expressed and narrated in social (both real and virtual) contexts.

For many, the stigmatization and policing of trauma narratives of lived experience could be the salt to another old wound; that of being unable to talk of mental health and ill-health at all due to cultural, religious, social, economic and other toxic societal narratives that perpetrate the myth of perfection. And for those who grew up witnessing their and/or loved one's mental/emotional decline due to the stigma, being told that their trauma is too much, is not valid, is not meant for certain spaces, should be talked about in this way and that - needless to say, will only magnify pain.

I am observing how assuming that we are only "whole" without the trauma, and/or thinking of the traumatized parts of ourselves as "not the real me", and/or expecting the outcomes of traumatic events to be separate from our "everyday" life - becomes an act of violence against the soul. I experience this split between "the traumatized self" and the "real self" as an act of cognitive dissonance, as an act of fragmenting instead of reintegrating the many internal and external narratives that make one human. Of declaring that the parts of the self that deserve to be called "the true self" do not include the parts that are hurting and in need of love.

And I recognize that the fear of becoming all of our trauma coupled with the discomfort of returning to the misery that the trauma caused, can discourage us from wanting to acknowledge those parts of us that are perhaps a little more worn, bruised and still tender. But while slicing away that little brown lumpy part of a banana doesn't take away from enjoying the rest of the banana, slicing away parts of our traumatized self to align with societal standards will only work to separate us from our own selves.

Maybe there's a way for trauma to dance through the dingy alleys of our daily life such that it slithers from street to sidewalk without causing an emotional traffic jam with casualties. Maybe in orally and physical sharing experiences of trauma we will find a shared language which transcends words and labels and becomes an invitation to reintegration;

The integration of our many individual traumatized, non-traumatized, resilient, creative and other parts into our whole selves;

The integration of us many individual human beings into the larger fabric of humanity;

The integration of the human world into the grand tapestry that is nature and the cosmos.

Maybe that is why we bond over shared traumatic experiences - to experience a sense of belongingness. Maybe that's how we know we're healing; when we feel like we belong (to our own selves, to our people, to our planet and to our universe).

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On Human Relationships Forged by the Sharing of Trauma

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How are some relationships formed over shared trauma? How do these relationships begin, and what do they grow into? Is this the same as trauma-bonding? (Answer: not quite) Are we sometimes pathologizing or stigmatizing the sharing of trauma? Or perhaps setting up well-meaning and caring yet strict s

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Resiliency Among Black Americans & Pantroipcal Dolphins 

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Resiliency Among Black Americans & Pantroipcal Dolphins 

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Taxpayer-funded institutions are now adding their voices to the movement against "systemic racism"-the invisible legacy of slavery and discrimination that supposedly determines the destiny of black Americans. The Smithsonian National Museum of African American History and Culture last month posted a graphic on its website outlining the "Aspects and Assumptions of Whiteness & White Culture in the United States." The document maintained that "white people and their traditions, attitudes and ways of life have been normalized over time" and "we have all internalized some aspects of white culture-including people of color."

From the sounds of it, these "assumptions" are the types of things that would be debilitating and deleterious to minorities should they adopt and practice them in their lives. Assumptions such as "hard work is the key to success," "the nuclear family . . . is the ideal social unit" and "plan for [the] future" are offered as examples of "white dominant culture." In fact, the qualities attributed to "whiteness" are the same principles and values that have empowered blacks in America to succeed despite lingering discrimination and bigotry. The museum removed the graphic after a public outcry, saying "it's not working in the way we intended."

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Opinion | The Resilience of the Black American

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Taxpayer-funded institutions are now adding their voices to the movement against "systemic racism"-the invisible legacy of slavery and discrimination that supposedly determines the destiny of black Americans. The Smithsonian National Museum of African American History and Culture last month posted a graphic on its website outlining the "Aspects and Assumptions of Whiteness & White Culture in the United States."

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For reasons we don't yet understand, in the eastern tropical Pacific the spotted dolphin swims with yellowfin tuna. In the early 1960's, fishing for yellowfin tuna by hook and line was replaced by mile-long purse seine nets, and fishermen began "setting on dolphin" to catch the tuna. Historically, millions of dolphins have been killed in the purse seine tuna fishery, with the spotted dolphin accounting for 80% of the casualties. There are still two to four million spotted dolphins in the eastern tropical Pacific population, but no species can endure such massive losses indefinitely-hopefully the current trend of reducing the by-catch will continue.

Physical Description

Spotted dolphins are difficult to describe because their size and coloring vary according to their geographic location. Found only in tropical waters, and subtropical waters, there are two recognized species: the worldwide species, the pantropical spotted dolphin, Stella attenuata and the Atlantic species, Stenella frontalis. The spotted dolphin's body is covered with spots and becomes more densely spotted with age. In the eastern Pacific, coastal forms are the most heavily spotted, while those found in the Hawai'ian Islands and in Japanese waters and the eastern Indian Ocean have moderate spotting. The spotted dolphin has a long slim beak containing 35 to 48 small conical teeth in each side of the upper jaw and 34 to 47 small, conical teeth in each side of the lower jaw.

Surface Characteristics

Color

Color varies according to geographical location, age, and the individual. Generally speaking, these animals go through five color phases:

1. newborn calves are dark gray with a white belly and no spots

2. the color changes to two-tone, sharply divided, dark on top, light on belly and no spots

3. adolescent phase when dark spots begin to appear on the lower part of the body

4. light spots appear on the dark upper portion of the body

5. dark ventral (underside) spots merge almost into a solid color with pink shading on the forward part of the belly

Fins and Fluke

Its beak is black and the lips and tip of the beak are white. A dark link extends from the middle of the lower jaw to the flipper and both eyes are circled in black with a black connecting line from each eye across the beak.

The dorsal (top) fin is tall and curved; the flippers are small and pointed. The flukes are small and pointed at the tips with a small median notch.

Length and Weight

Length averages about 7 feet (2.1 m); weight averages 220 pounds (100 kg). Calves are 32 to 36 inches (80 to 90 cm) at birth.

Feeding

Spotted dolphins feed on many varieties of fish and squid found near the surface of the water. In the eastern Pacific, pregnant females feed more on squid and nursing females tend to feed more on fish. The reason for this is unknown.

Mating and Breeding

This species reaches maturity between 6 and 8 years of age or when the animal is about 6.5 feet (2 m) in length. Mating and calving take place throughout the year; the calving interval is believed to be about every two years, but in stressed populations mating takes place at an earlier age and calving at shorter intervals, a response to the enormous mortalities suffered from being entangled in nets by the tuna fishery. Gestation is 11 1/2 months and calves are nursed for 11 months.

Range Map

Distribution and Migration

This species reaches maturity between 6 and 8 years of age or when the animal is about 6.5 feet (2 m) in length. Mating and calving take place throughout the year; the calving interval is believed to be about every two years, but in stressed populations mating takes place at an earlier age and calving at shorter intervals, a response to the enormous mortalities suffered from being entangled in nets by the tuna fishery. Gestation is 11 1/2 months and calves are nursed for 11 months.

Natural History

These animals are highly social and are sometimes found in herds of thousands, especially in offshore forms, though groups of several hundred are more common. Herds contain both sexes and all ages. Pantropical spotted dolphins are often seen in the company of other dolphin species, particularly spinner dolphins.

Status

The spotted dolphin is the species, which has suffered the most in the incidental take in the purse seine nets of the tuna fishery. From 1959 to 1978, it has been estimated that over 4,000,000 spotted dolphins dies in tuna nets. For reasons unknown, yellowfin tuna and spotted dolphins travel together in the eastern tropical Pacific, an area that extends from Mexico south to Chile and west to Hawai'i and Samoa. One theory is that they feed on the same food but at different levels. Tuna fishermen watch for the dolphins, then set their nets and encircle both dolphins and tuna, killing dolphins in the process. In 1972 the Marine Mammal Protection Act was passed and through improved fishing techniques and the required practice of having government observers aboard the tuna boats to monitor the number of dolphins killed, the mortality rate dropped to about 20,000 a year in the U.S. fleet. However, these rules do not apply to foreign tuna fleets and many dolphins die each year in some unregulated fisheries. In addition, several thousand are killed each year for food in drive fisheries in Japan.

Bibliography

Jefferson, T.A., M.A. Webber, R.L. Pitman. 2015 Marine Mammals of the World: A Comprehensive Guide to Their Identification, 2nd Edition. Elsevier/AP.

Leatherwood, S. and R. Reeves Whales and Dolphins San Francisco: Sierra Club Books, 1983.

Leatherwood, S., R. Reeves, W. Perrin and W. Evans. Whales, Dolphins and Porpoises of the Eastern North Pacific and Adjacent Arctic Waters. U. S. Dept. of Commerce: NOAA Technical Report, NMFS Circular 444, July 1982.

Acknowledgements

Illustrations courtesy Uko Gorter, copyright ©2017 all rights reserved.
FACT SHEETS MAY BE REPRINTED FOR EDUCATIONAL OR SCIENTIFIC PURPOSES

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For reasons we don't yet understand, in the eastern tropical Pacific the spotted dolphin swims with yellowfin tuna. In the early 1960's, fishing for yellowfin tuna by hook and line was replaced by mile-long purse seine nets, and fishermen began "setting on dolphin" to catch the tuna.

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Strength in numbers

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Introduction

Complex social structure is prominent in many mammals including primates (Chapman and Rothman 2009), elephants (Wittemyer et al. 2005), hyaenas (Smith et al. 2008), bats (Popa-Lisseanu et al. 2008) and cetaceans (Mann et al. 2000), and plays an important role in population dynamics and behavioural patterns. It governs the way the spread or containment of behaviours is facilitated, e.g. through social learning (Heyes 1994; Laland 2004). This may lead to behavioural diversity not only among, but within populations, where different population segments exhibit different behaviours (Mann and Sargeant 2003; Cantor and Whitehead 2013). Understanding this is not only interesting biologically, but may help conservation efforts (Whitehead 2010), because not all population segments necessarily respond to, or interact with, human activities the same way, or at the same time. There is concern over the effects of anthropogenic disturbance to populations, yet it is difficult to assess population-level impacts without understanding what proportion of animals may be affected.

Bottlenose dolphins ( Tursiops sp.) are well-studied social mammals (Wells et al. 1987; Smolker et al. 1992; Lusseau et al. 2003; Connor et al. 2006; Lusseau 2006). Most information on their social structure comes from studies in Sarasota, Florida (Wells et al. 1987; Wells 2003) and Shark Bay, Australia (Connor et al. 1999; Mann et al. 2000), but many populations remain poorly studied. They are generally described as fission-fusion species, where group composition changes frequently (Connor et al. 2000), but we argue that their social structure varies considerably among populations. For example, dolphins in Florida appear to feature marked sex-age segregation, where males form paired alliances, females form bands and nursery groups and juveniles form smaller groups (Wells et al. 1987). In Shark Bay, males form hierarchical alliances (Connor et al. 1999, 2011; Randić et al. 2012). At the other end of the spectrum, dolphins in Doubtful Sound, New Zealand, form mixed-sex groups with strong associations not only within, but also between sexes (Lusseau et al. 2003). This shows that patterns cannot be generalised and that our understanding of bottlenose dolphin social structure remains incomplete.

Social network analysis allows groups of social animals to be studied as a network of nodes and ties (Wey et al. 2008; Krause et al. 2009a). When coupled with information on behaviour and interactions with human activities, it is a powerful tool in the study and conservation of social animals. Common bottlenose dolphins ( T. truncatus) inhabit the Gulf of Trieste and adjacent areas of northern Adriatic Sea, where they have been studied since 2002 (Genov et al. 2008, 2017). Here, we examine the social structure of local dolphins and assess whether different population segments show differences in behaviour and interactions with human activities.

Materials and methods

Data collection

Data were collected between February 2003 and September 2011 in the Gulf of Trieste and adjacent waters, northern Adriatic Sea (Fig. ). Based on mark-recapture abundance estimates, about 40-100 dolphins use this area annually, the majority carrying natural marks suitable for long-term identification (Genov et al. 2008; Genov 2011). The study area, survey methods and photo-identification procedures are described in detail in Genov et al. ( 2008). In short, boat surveys were complemented with land-based surveys to maximise the probability of encountering and photographically capturing dolphins. Survey coverage varied among years, due to weather, dolphin distribution and logistical constraints (Table ). Each year we attempted to survey the entire area as homogeneously as possible. Surveys were done predominantly during summer (July-September), but periodically also in other months. Due to typical summer weather, surveys were commonly done in the morning and early afternoon, ceased in the early afternoon due to wind and resumed in late afternoon. Southern portion of the Gulf of Trieste, including waters along the Slovenian coast and Piran Bay, was surveyed consistently over the years and received more coverage than the outer edges of the study area (Fig. ), due to the location of the home port and the land-based observation point. This sub-area, encompassing a roughly 5 km radius around the Piran peninsula, was regularly surveyed by both boat-based and land-based surveys and can be considered 'core study area' for the purposes of some of the results presented later on.

Table 1

Year

Survey effort

Nr. groups observed

Nr. individuals identified

Boat [km (morning/afternoon)]

Land [hours + minutes (morning/afternoon)]

Photographs of dorsal fins were obtained during focal follows and allowed individual identification (Würsig and Jefferson 1990). Members of a dolphin group were considered associated. Group was defined as dolphins observed behaving in a generally coordinated fashion (moving in the same direction or staying in the same area, usually engaged in the same general activity). In practice this meant that group members were always within about 100 m from the nearest other dolphin. Field observations and photo-identification showed that group composition rarely changed during several hours of observation (Genov et al. 2008).

Sex was determined by (a) observations of mother-calf pairs (adults consistently accompanied by calves were assumed to be mothers and, therefore, females); (b) photographs of the genital area or (c) molecular methods from biopsy sampling carried out opportunistically within Slovenian waters (permit 35601-102/2010-4 by the Slovenian Environmental Agency). Skin and blubber samples were obtained using a 68-kg draw weight crossbow, using custom-made bolts and stainless steel sampling tips with length of 25 mm and internal diameter of 7 mm. Tips were sterilised using 96% ethanol and burning prior to being used. Dolphins were sampled in the dorso-lateral area below the dorsal fin, at distances of 4-10 m. All biopsy attempts were accompanied by concurrent photo-identification. Sampling was only attempted on adults without accompanying offspring. Skin samples were removed and excised with sterilised forceps and surgical scissors, placed in 96% ethanol and stored at − 20 °C until analysis. Samples were analysed as described in Gaspari et al. ( 2015).

Numerous trawlers operated in the area year-round. They can be divided into (a) single bottom trawlers and (b) pelagic/mid-water pair trawlers. Bottom trawlers were typically 9-15 m long, operated alone and trawled nets on the seabed, targeting several demersal species. Pair trawlers were typically 30 m long, operated in pairs and trawled nets in mid-water. They mostly targeted European anchovies ( Engraulis encrassicolus) and sardines ( Sardina pilchardus). Dolphins interacted with both trawler types (Genov et al. 2008). Interaction was defined as dolphins following operating trawlers, approximately 200-400 m from stern (closer for bottom trawlers and further for pair trawlers, but the exact distance could vary), and typically alternating long dives (> 1 min) with sequences of short dives (5-30 s).

Data restrictions

Only high-quality photographs (sharp image, fin perpendicular to the camera lens, entire fin visible and not obstructed by water spray or other animals, fin height < 7% of the frame height) were used. Association patterns were analysed for well-marked individuals only (123 individuals). However, as individuals with low encounter rates can introduce biases (Chilvers and Corkeron 2002; Whitehead 2008b), we only considered those encountered on ≥ 4 occasions and in ≥ 2 different years. This restricted the analysis to animals with some meaningful level of site fidelity and removed transient individuals, to ensure an accurate representation of the social network. Although most authors limit analyses to animals with some arbitrary number of total sightings (Quintana-Rizzo and Wells 2001; Chilvers and Corkeron 2002; Pace et al. 2012), we further limited this to animals encountered in more than 1 year. This was because several animals seen multiple times were only seen in a single year and, therefore, considered visitors/transients. Our restriction criteria resulted in 38 individuals used in the analysis. This subset represents regular individuals ('residents') and is considered representative for this local population. Thirty-two animals (84.2%) were seen ≥ 5 times and 18 (47.4%) ≥ 10 times. Mean number of sightings per individual was 14 (SD 11.3, range 4-41). Multiple encounters during same day were only included if they were of different groups. Mother-dependent calves were excluded due to non-independence.

Testing association patterns and network analysis

To minimise bias and facilitate comparisons, the half-weight association index (HWI) was used (Cairns and Schwager 1987). Although an attempt was made to photograph all members of each group, this was not always possible and the HWI accounts for this. It was recently suggested that a new index accounting for gregariousness (HWIG) may be more suitable (Godde et al. 2013). We also analysed associations using HWIG, but found little difference in results. Therefore, and to facilitate comparisons with previous studies, only HWI results are presented.

Analyses were performed in program SOCPROG 2.4 (Whitehead 2009). To test whether dyads (pairs of individuals) associated more often than expected by chance, we used the Manly-Bejder permutation technique (Manly 1995; Bejder et al. 1998) with extensions (Whitehead 1999; Whitehead et al. 2005) and corrections (Krause et al. 2009b). We used day as a sampling period. We generated 20,000 permutations (associations within samples) to ensure stability of P values. We also performed another round of permutations, with sampling period of 5 days, because permutations are often impossible (or perform poorly) with too few associations within a period.

We used standardised lagged association rates (SLAR, Fig. ) to estimate the probability of dyads associated at a given time still being associated after a time lag and assess the stability of associations (Whitehead 1995). Precision (SE) was estimated by jack-knifing on each sampling period (Whitehead 2008a). To test for preferred/avoided associations, we compared SLAR to null association rate, which represents expected values for random associations (Whitehead 1995). A moving average enabled the optimal adjustment between precision and smoothing. Exponential models of social organisation developed by Whitehead ( 1995) were fitted to SLAR. Model selection was based on minimising the Quasi-Akaike Information Criterion (QAIC) (Burnham and Anderson 2002).

We calculated the social differentiation ( S) to evaluate the level of variation in dyadic probability of association, i.e. how differentiated the network was (Whitehead 2008a). We calculated the correlation between true and estimated association indices ( r) to evaluate if data accurately represented the true social network (Whitehead 2008b). To investigate existence of clusters and delineate units within the network, we carried out modularity analyses (Newman 2004) by applying the eigenvector method of Newman ( 2006), the knot-diagram analyses and the modularity-G (Whitehead 2008a). With this approach the animals were assigned to clusters so that the separation between clusters was maximised (Whitehead 2008a). To evaluate if association rates were similar within/between clusters, and within/between sexes, we compared mean association rates via two-tailed Mantel test.

To facilitate comparisons with other studies, we calculated several network metrics-HWI, Affinity, Betweenness, Closeness, Clustering coefficient, Eigenvector centrality, Reach and Strength (Wey et al. 2008; Whitehead 2008a)-for the entire network, individual clusters and for individuals (Table ). These are measures of how well-connected and central individuals are (Whitehead 2008a).

Table 2

A social network diagram (Fig. ) was created using NetDraw 2.123 (Borgatti 2002) to illustrate relationships and network structure. Nodes with highest associations are grouped together, while those with fewer links remain on the periphery. We created one diagram with all associations, regardless of strength (Fig. a), and one displaying only those with HWI greater than twice the overall mean (Fig. b), believed to represent meaningful associations (Durrell et al. 2004; Gero et al. 2005; Wiszniewski et al. 2012).

Social structure was also represented with hierarchical average linkage cluster analysis (dendrogram, Fig. ). Since dendrograms can be over-interpreted, especially if the society is not hierarchically arranged, we used strength of cophenetic correlation coefficient (CCC) to indicate whether the data interpretation was valid (Whitehead 2008a).

Sex composition

To further examine potential sex segregation, we selected sightings involving at least two known-sex animals (including sightings with no or single known-sex individual would introduce a bias in estimating sex composition). In this sub-sample, we determined the proportion of male-only, female-only and mixed-sex groups.

Results

Association patterns

We photographed 132 dolphin groups, but the restriction criteria resulted in 115 encounters of 38 individuals included in analysis. All individuals were observed in the core study area, but could also be encountered elsewhere.

Network metrics are shown in Table . Correlation between true and estimated association indices ( r ± SE = 0.840 ± 0.040, based on bootstrap with 10,000 replications), suggests that the data accurately describe the true social network (Whitehead 2008b). P values stabilised after about 9000 permutations. Standard deviation of the calculated (observed) associations was significantly higher than that of permuted data (observed SD = 0.236, random SD = 0.228, P < 0.001), as was the CV (observed CV = 1.259, random CV = 1.226, P < 0.001), indicating that associations were non-random (Gowans et al. 2001; Lusseau et al. 2003). Figure shows that most dolphins had preferred associates, with one pair (NUI-TEA) always recorded together. CCC of 0.96 suggests a good fit and thus a good representation of true social structure (Whitehead 2008a). SLAR was best described by the so-called 'constant companions and casual acquaintances' model (Fig. , Table ). SLAR line never reached the null association rate, indicating the absence of random associations and a high probability of dyads associated even after a prolonged time lag.

Table 3

Division of social network

Although the network was fluid overall, social differentiation estimate using likelihood method ( S 1.076, SE 0.025) indicates a well-differentiated society (Whitehead 2008a). Average linkage cluster analysis (Fig. ) and network analysis (Fig. ) both showed a clear division into three distinct clusters, with one individual (AAR) not fully belonging in any. Modularity analysis assigned individuals to clusters with significantly higher associations within than between clusters (two-tailed Mantel test: t = 21.25, P = 1.0). Modularity-G division (peak at 0.464) suggests that the best division is with an association index of 0.043. The modularity-G peak suggests that with this division, there is much more total association within clusters than would be expected for randomly determined clusters. Since modularity values > 0.3 suggest a meaningful division (Newman 2004), the value of 0.464 provides compelling evidence of a structured network.

Dolphins formed two main clusters, A (19 individuals) and B (13 individuals), with strong associations, and a smaller cluster C (6 individuals) with much weaker associations (Table ). Mean HWIs were similar between A and B and lower in cluster C (Table ). Dolphins were predominantly found with other members of the same cluster, although group sizes varied. Cluster A and B dolphins were usually seen in large groups (> 10 and up to 45 individuals). Cluster A dolphins rarely interacted with those from cluster B (4/115 encounters, or 3.5%). These interactions never involved the majority of both clusters. Instead, while one (either A or B) featured the majority of animals, the other was represented by few (1-4).

Cluster C contained individuals that occasionally interacted with clusters A and B, but were typically seen with other cluster C animals, on their own, or with transient dolphins. They were predominantly found in small groups (2-3) or alone. They had no particularly strong bonds with anyone. Individual AAR did not fit into any cluster well (Fig. ), but was placed in cluster C based on modularity, extremely low mean HWI of 0.01, an eigenvector value close to zero, and other network metrics.

Of 115 encounters, 55 (47.8%) included only cluster A animals, 10 (8.7%) included only cluster B animals and 37 (32.2%) included only cluster C animals. Three encounters (2.6%) included a mix of clusters A and B, 6 (5.2%) of clusters A and C, 3 (2.6%) of clusters B and C and 1 (0.9%) of all three clusters.

Network metrics

Affinity, Clustering coefficient, Eigenvector centrality, Reach and Strength were comparable between clusters A and B and lower in cluster C. Individuals in A and B had more associates and formed more stable associations with them than those in C. Conversely, cluster C had a higher Closeness, which is a different measure of centrality-as cluster C animals interacted with both A and B, their shortest paths to all other individuals were shorter than for other two clusters. Finally, cluster B had the lowest Betweenness centrality, which is likely a combination of cluster size and how often its members interacted with other clusters.

Sex segregation and sex differences

Twenty-five animals were sexed (13 females, 12 males). We found no evidence of sex segregation. Cluster A contained 6 females, 7 males, and 6 unknown sex animals; cluster B contained 5 females, 4 males, and 4 unknown sex animals; and cluster C contained 2 females and 4 unknown sex animals (Fig. ).

Among groups where sex of at least two animals was known ( n = 60), 76.7% were mixed-sex. This is likely an underestimate, as groups classified as 'single-sex', but involving unsexed individuals, could in fact be mixed. Among groups composed only of cluster A dolphins ( n  = 44), 81.8% were mixed-sex. We could not estimate this for clusters B and C, as the number of encounters with at least two sexed animals was insufficient.

Mean HWI was higher for male-male pairs (HWI ± SD = 0.25 ± 0.07) than male-female pairs (0.21 ± 0.05) and female-female pairs (0.15 ± 0.06), but differences between sexes were not significant (two-tailed Mantel test: t = − 0.916, P  = 0.16).

Temporal habitat use patterns

When we examined temporal (diel) occurrence patterns, an interesting trend became apparent. Clusters A and B overlapped spatially, but not temporally. They were almost never seen together, apart from four encounters mentioned earlier. Furthermore, while both regularly used the core study area, they used it at different times of day: cluster A was predominantly sighted in morning hours (07:00-13:00) and cluster B only in late afternoon hours (18:00-21:00). This trend was consistent in the core study area without deviation, although cluster A could be found elsewhere in the afternoon and cluster B could be found elsewhere in the morning. To test if there was any real pattern, we first looked at hours of occurrence of the two clusters for the entire study area. Next, to avoid bias resulting from different spatial preferences of dolphins or the spatial coverage of our survey effort, we looked at hours of occurrence in the core study area only (i.e. the area regularly covered by both boat-based and land-based surveys). For those few occasions when animals from more than one cluster were together, we assigned a group to a given cluster if it was predominantly composed of that cluster. When considering the entire study area and groups composed only or predominantly of cluster A dolphins, 55 encounters (93.2%) were between 07:00 and 13:00, and only 4 encounters (6.8%) after 13:00 ( n = 59). Looking at the core study area only, all encounters (100%) of cluster A groups were before 13:00 ( n = 18, Fig. ). When considering the entire study area and groups composed only or predominantly of cluster B dolphins, 5 encounters (33.3%) occurred before 13:00, while the remaining 10 (66.7%) occurred after 18:00 ( n = 15). Looking at the core study area only, all encounters (100%) of cluster B groups were recorded after 18:00 ( n = 8; Fig. ). The temporal use of the entire study area differed significantly between clusters A and B, as did the use of the core study area (Fisher's exact test: P  < 0.001).

Cluster C groups did not display such patterns. In the entire study area, 23 (62.2%) encounters of cluster C groups were before 13:00, while 14 (37.8%) were after 13:00 ( n = 37). In the core study area, 20 (66.7%) were before 13:00, while 10 (33.3%) were recorded after ( n  = 30).

Interactions with trawlers

Forty-eight interactions with trawlers were recorded during the study, of which 35 were during dolphin encounters considered in the analysis. Encounters involving trawler interactions accounted for 29.6% of dolphin encounters. Twenty-two (62.9%) of these interactions were with pelagic pair trawlers and 13 (37.1%) with bottom trawlers (one encounter involved interactions with both).

Majority of interactions with trawlers involved cluster A dolphins, with one individual (MOR) present in more than 50% of all interactions (Fig. ). Mean number of interactions with any trawlers per individual in cluster A was 10.6 (SD 6.1, range 3-24). Twenty-eight interactions involved only cluster A dolphins (82.4%), 4 involved cluster A and cluster C dolphins (11.8%), 1 involved only cluster C dolphins (2.9%) and 1 involved cluster B and cluster C dolphins (2.9%). No interactions involved only cluster B dolphins.

Cluster B dolphins were never observed interacting with pair trawlers, while four individuals apparently interacted with a bottom trawler on one occasion. Mean number of interactions with any trawler per individual in this cluster was 0.31 (SD 0.48, range 0-1).

Dolphins from cluster C interacted with trawlers at intermediate level. Only one animal from cluster C (ALE) ever interacted with pair trawlers. This happened on one occasion, when the individual was with cluster A dolphins. On another occasion, the same individual was observed diving ( sensu Bearzi et al. 1999) with another unidentifiable adult, when active pair trawlers passed by. The animals appeared to ignore them and continued diving in the same location. Other animals from cluster C were either never observed interacting with trawlers, or only observed interacting with bottom trawlers (Fig. ). Mean number of interactions with any trawlers per individual in this cluster was 1 (SD 0.01, range 0-3).

Discussion

General social structure

Gulf of Trieste dolphins appear to live in two general kinds of social units: (a) large mixed-sex groups with strong, long-lasting associations and (b) small groups with weaker, temporally unstable associations. This does not appear to be age-dependent. Two largest clusters featured strong bonds, while seldom interacting with the other cluster. This structuring was also evident in the field. These two clusters showed high levels of group stability, which persisted through the study years and beyond (T. Genov, personal observation), although exact group membership could vary. Gregariousness, connectedness and strength of associations (indicated by HWI, Affinity, Clustering coefficient, Eigenvector centrality and Strength) were quite high and relatively similar between the two, as was the number of associates (Reach; Table ). In contrast, these metrics were substantially lower in cluster C, where animals showed no strong association preferences. Because they were occasionally observed with animals from other clusters, their Closeness was highest (Table ).

When including all associations (Fig. a) the network was reasonably well-connected, with no individual 'bottlenecks' between clusters, which were inter-connected via several but not particularly numerous individuals. Such 'social brokers' (Lusseau and Newman 2004) may maintain population cohesiveness and prevent complete cluster isolation, possibly having disproportionate influence on the population connectedness, as found in killer whales (Williams and Lusseau 2006), macaques (Flack et al. 2005) and squirrels (Manno 2008). However, when considering only 'meaningful' associations, greater than twice the mean HWI (Durrell et al. 2004; Gero et al. 2005; Wiszniewski et al. 2012), structuring becomes striking and clusters completely separated (Fig. b).

Associations were temporally relatively stable (as supported by SLAR and field observations), although stability varied with different levels of social organisation. Cluster A in particular (but also B) seemed to contain 'core' membership (first-level unit) and other 'tiers' that joined core members to form higher-level units. In such multi-level systems, seen also in African elephants (Wittemyer et al. 2005) clusters can sub-split during times of ecological constraints and fuse again when conditions are favourable or promote cooperation. We sometimes observed cluster A dolphins forming smaller groups (≤ 10), which often joined into groups of 30 + animals. Group composition during encounters was also surprisingly stable, more than in the closest other known local population in the Adriatic Sea (Bearzi et al. 1997) or in most other populations worldwide (Connor et al. 2000; Lusseau et al. 2006). Once encountered, groups were unlikely to change during observations, which could last several hours (Genov et al. 2008). This population is rather small (Genov et al. 2008; Genov 2011) and some authors hypothesised that community size influences group stability in fission-fusion societies, with smaller communities leading to decreased fission-fusion flexibility (Lehmann and Boesch 2004; Augusto et al. 2012).

In several Tursiops populations, social structure involves sex/age segregation (Wells et al. 1987; Connor et al. 2000; Fury et al. 2013). Here, structuring did not appear sex-related, as clusters contained both sexes. We found no evidence of male alliances. Although male-male associations were stronger than male-female or female-female associations, this was not significant, with stronger male-female than female-female associations. Most encountered groups contained both sexes (regardless of season), which suggests that mixed-sex groups were not related to reproductive state. Likewise, although more than half of all groups contained calves, adult-only groups were common. Reproductive state or presence of calves, therefore, fails to explain these patterns.

Presence of large mixed-sex groups resembles Doubtful Sound bottlenose dolphins in New Zealand (Lusseau et al. 2003). Lusseau et al. ( 2003) hypothesised that ecological constraints, such as variable productivity, drive social organisation. In such environments, groups may need to rely on individuals with long-term knowledge about spatio-temporal distribution of prey sources, which might explain lack of sex segregation and greater population connectedness (Lusseau et al. 2003). The northern Adriatic is characterised by large spatio-temporal variability in nutrient input and productivity (Fonda Umani et al. 2005; Mozetič et al. 2010, 2012), and our study area contains relatively uniform bottom topography. With lack of major prey-aggregating bottom features, spatio-temporal distribution of prey is likely highly variable, which may promote network connectedness. Clusters A and B both contained individuals which appeared 'older' based on their external appearance. These animals may possess long-term knowledge needed to tackle such constraints and thus play a key role in their community.

Temporal segregation

Several studies found spatial segregation in Tursiops (Chilvers and Corkeron 2001; Chilvers et al. 2003; Lusseau et al. 2006; Fury et al. 2013; Carnabuci et al. 2016). In Moray Firth, Scotland, this segregation appeared season-dependent (Wilson et al. 1997). During summer, part of the population moved into inner parts of the Firth and was replaced by dolphins from outer parts. However, clusters in our study overlapped spatially, but not temporally, and we found differences on a daily, rather than seasonal level. Such intraspecific diel temporal partitioning does not appear to have been documented in cetaceans previously, nor in other mammals (Kronfeld-Schor and Dayan 2003), with one exception recorded in the use of running wheel in captive mice (Howerton and Mench 2014). Whether this pattern results from competitive exclusion, avoidance of aggressive interactions, or different foraging tactics, remains unknown. Given that prey resources in the marine environment are patchy and variable, prey resource defence is not a likely explanation (Ramp et al. 2010). Lack of sex segregation also dismisses access to females as an explanation. We are currently working to determine if genetic relatedness correlates with the social partitioning observed here.

We considered potential confounding factors. If the distribution of cluster A was linked to trawlers, which only operated during certain hours, this would explain the pattern. However, pair trawlers operated in the morning and afternoon, and bottom trawlers operated day-long (including evenings). Cluster A regularly used trawling areas even in the absence of trawlers, with no difference in group composition. More importantly, no trawlers operated in the core study area. Finally, cluster A dolphins did not always follow trawlers, even if trawlers were around. Trawlers, therefore, fail to explain temporal partitioning.

We also considered lower sample size for cluster B. Caution is needed when making inferences from small sample sizes, but temporal patterns here appear quite striking. The presence of a temporal (rather than spatial) pattern suggests the observed associations were not an artefact of space use (animals being together just because they use the same space), but due to genuine social preferences. Further, due to long-term and extensive survey effort (Table , Fig. ), this pattern is unlikely to be an artefact of effort. Surveys in recent years (2012-2017, analysis pending) further support this, with both clusters continuing this pattern, and even occurring in the same area within a single day, but at different times (Morigenos, unpublished data).

Finally, it remains to be determined if segregation is specific to this area, or if it occurs in other areas used by the animals. The range of this local population is unknown (Genov et al. 2016), but evidence from photo-ID (Genov et al. 2009) and genetics (Gaspari et al. 2015) suggest it is a distinct unit.

Interactions with trawlers

Two clusters displayed behavioural differences related to trawling. Cluster A dolphins often interacted with pair trawlers and occasionally bottom trawlers, while cluster B dolphins did not ('trawler dolphins' vs. 'non-trawler dolphins', Chilvers and Corkeron 2001). Fishing has a major impact on cetaceans worldwide, not only through incidental mortality (Read et al. 2006), but also through prey depletion (Bearzi et al. 2008), habitat degradation (Turner et al. 1999) and ecosystem change (Worm et al. 2006). More subtly, fishing activities can affect, or be affected by, cetacean behaviour. In Queensland, Australia, bottlenose dolphins were found to form two communities, where one fed in association with trawlers and the other did not (Chilvers and Corkeron 2001; Chilvers et al. 2003). Following fishery closure, dolphins restructured and homogenised their network, suggesting that structuring was fishery-induced (Ansmann et al. 2012). Our study shows similarities, but also important differences. First, in the population studied by Ansmann et al. ( 2012), dolphins fed on discards, while our dolphins followed operating trawlers, presumably feeding actively inside/behind the net (Genov et al. 2008; Kotnjek 2016). Second, structuring in our study related to temporal rather than spatial segregation, and did not appear only fishery-related. Another study in the Mediterranean Sea related dolphin association patterns to bottom trawling and fish farming, but animals mixed more frequently than ours (Pace et al. 2012).

Human activities can likely alter behaviour and social structure of mammals (Rutledge et al. 2010; Ansmann et al. 2012) and this may well be the case here. However, causal links are unclear and it is difficult to ascertain what came first. The inherent social structure itself, and social learning, may lead to differential behaviour and interactions with anthropogenic activities, without these activities changing the social system in the first place. It is interesting to note that the pair trawler fishery in our area closed in 2012. This did not appear to change associations or temporal patterns, but cluster A did appear to increase rates of interactions with bottom trawlers (Morigenos, unpublished data).

Diet information for this population is limited, but dietary preferences may explain different fishery-related foraging tactics. Both clusters were observed taking mullets ( Mugil/ Liza sp., Genov et al. 2008, Morigenos, unpublished data) and both regularly feed in the core study area. Their diets, therefore, overlap, but to an unknown extent. However, the apparent 'switch' of cluster A to bottom trawlers after the closure of pair trawler fishery suggests that behavioural specialisation and hunting techniques, rather than prey preference, may be more likely. Our further research aims to provide better insight into the feeding ecology of this population through stable isotope analysis.

Whether interactions with trawlers increase fitness (by maximising energetic intake and minimising expenditure) or decrease it (through increased bycatch), is unknown. Both clusters produce new offspring and appear stable, and there is no evidence of trawler-related bycatch in this area.

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Behavioural and temporal partitioning of dolphin social groups in the northern Adriatic Sea

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Complex social structure is prominent in many mammals including primates (Chapman and Rothman 2009), elephants (Wittemyer et al. 2005), hyaenas (Smith et al. 2008), bats (Popa-Lisseanu et al. 2008) and cetaceans (Mann et al. 2000), and plays an important role in population dynamics and behavioural patterns.

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Amazing video captures birth of SeaWorld's last captive orca

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The Brutal History Of Exploring The Amazon

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Stellers Sea Cow - Hydrodamalis gigas - Extinct Sirenia