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The benefits of social behavior as a whole aid in the survival rates of organisms as group interactions will foster protection amongst the group as well as increased rates of reproductive success and reduction in predation levels. With a group of organisms working collectively together, they are able to monitor each individual member of the group and ensure they do not get left behind or are at risk of being in danger to external forces and/or predators. Social behavior often proves to be more sustainable than independent social behavior as the travel rates in gathering food tend to cover more territory and have more success in obtaining their prey. With the increasing number of threats presenting themselves (whether human or environmental), organisms in group settings are able to communicate dispersal signals or choose to combat collectively as a group to challenge and eliminate the danger. Similar signals are also able to be transmitted in terms of mating, competition, and danger as well and having a group present to oversee these factors poses a better chance of survival for each member of the group.

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Abstract

Social relationships-both quantity and quality-affect mental health, health behavior, physical health, and mortality risk. Sociologists have played a central role in establishing the link between social relationships and health outcomes, identifying explanations for this link, and discovering social variation (e.g., by gender and race) at the population level. Studies show that social relationships have short- and long-term effects on health, for better and for worse, and that these effects emerge in childhood and cascade throughout life to foster cumulative advantage or disadvantage in health. This article describes key research themes in the study of social relationships and health, and it highlights policy implications suggested by this research.

Keywords: relationships, social support, social integration, stress, cumulative disadvantage

Captors use social isolation to torture prisoners of war-to drastic effect. Social isolation of otherwise healthy, well-functioning individuals eventually results in psychological and physical disintegration, and even death. Over the past few decades, social scientists have gone beyond evidence of extreme social deprivation to demonstrate a clear link between social relationships and health in the general population. Adults who are more socially connected are healthier and live longer than their more isolated peers. This article describes major findings in the study of social relationships and health, and how that knowledge might be translated into policy that promotes population health. Key research findings include: (1) social relationships have significant effects on health; (2) social relationships affect health through behavioral, psychosocial, and physiological pathways; (3) relationships have costs and benefits for health; (4) relationships shape health outcomes throughout the life course and have a cumulative impact on health over time; and (5) the costs and benefits of social relationships are not distributed equally in the population.

WHAT DO WE MEAN BY "SOCIAL RELATIONSHIPS"?

Social scientists have studied several distinct features of social connection offered by relationships ( Smith and Christakis 2008). Social isolation refers to the relative absence of social relationships. Social integration refers to overall level of involvement with informal social relationships, such as having a spouse, and with formal social relationships, such as those with religious institutions and volunteer organizations. Quality of relationships includes positive aspects of relationships, such as emotional support provided by significant others, and strained aspects of relationships, such as conflict and stress. Social networks refer to the web of social relationships surrounding an individual, in particular, structural features, such as the type and strength of each social relationship. Each of these aspects of social relationships affects health. We discuss the broad effects of these features of relationships for health, and, for ease of discussion, we use the terms "social relationships" and "social ties" interchangeably throughout this article.

SOCIAL RELATIONSHIPS BENEFIT HEALTH

Many types of scientific evidence show that involvement in social relationships benefits health. The most striking evidence comes from prospective studies of mortality across industrialized nations. These studies consistently show that individuals with the lowest level of involvement in social relationships are more likely to die than those with greater involvement ( House, Landis, and Umberson 1988). For example, Berkman and Syme (1979) showed that the risk of death among men and women with the fewest social ties was more than twice as high as the risk for adults with the most social ties. Moreover, this finding held even when socioeconomic status, health behaviors, and other variables that might influence mortality, were taken into account. Social ties also reduce mortality risk among adults with documented medical conditions. For instance, Brummett and colleagues (2001) found that, among adults with coronary artery disease, the socially isolated had a risk of subsequent cardiac death 2.4 times greater than their more socially connected peers.

In addition to mortality, involvement in social relationships has been associated with specific health conditions as well as biological markers indicating risk of preclinical conditions. Several recent review articles provide consistent and compelling evidence linking a low quantity or quality of social ties with a host of conditions, including development and progression of cardiovascular disease, recurrent myocardial infarction, atherosclerosis, autonomic dysregulation, high blood pressure, cancer and delayed cancer recovery, and slower wound healing ( Ertel, Glymour, and Berkman 2009; Everson-Rose and Lewis 2005; Robles and Kiecolt-Glaser 2003; Uchino 2006). Poor quality and low quantity of social ties have also been associated with inflammatory biomarkers and impaired immune function, factors associated with adverse health outcomes and mortality ( Kiecolt-Glaser et al. 2002; Robles and Kiecolt-Glaser 2003). Marriage is perhaps the most studied social tie. Recent work shows that marital history over the life course shapes a range of health outcomes, including cardiovascular disease, chronic conditions, mobility limitations, self-rated health, and depressive symptoms ( Hughes and Waite 2009; Zhang and Hayward 2006).

HOW DO RELATIONSHIPS BENEFIT HEALTH?

Once the clear link between social relationships and health was established, scientists devoted themselves to explaining how this occurs. Generally speaking, there are three broad ways that social ties work to influence health: behavioral, psychosocial, and physiological.

Behavioral Explanations

Health behaviors encompass a wide range of personal behaviors that influence health, morbidity, and mortality. In fact, health behavior explains about 40 percent of premature mortality as well as substantial morbidity and disability in the United States ( McGinnis, Williams-Russo, and Knickman 2002). Some of these health behaviors-such as exercise, consuming nutritionally balanced diets, and adherence to medical regimens-tend to promote health and prevent illness, while other behaviors-such as smoking, excessive weight gain, drug abuse, and heavy alcohol consumption-tend to undermine health. Many studies provide evidence that social ties influence health behavior (see a review in Umberson, Crosnoe, and Reczek 2010). For example, Berkman and Breslow's (1983) prospective study in Alameda County showed that greater overall involvement with formal (e.g., religious organizations) and informal (e.g., friends and relatives) social ties was associated with more positive health behaviors over a ten-year period. Being married ( Waite 1995), having children ( Denney 2010), and ties to religious organizations ( Musick, House, and Williams 2004) have all been linked to positive health behaviors (although, notably, as we will discuss below, marriage and parenthood have also been associated with behaviors that are not beneficial to health-including physical inactivity and weight gain).

Social ties influence health behavior, in part, because they influence, or "control," our health habits ( Umberson et al. 2010). For example, a spouse may monitor, inhibit, regulate, or facilitate health behaviors in ways that promote a partner's health ( Waite 1995). Religious ties also appear to influence health behavior, in part, through social control ( Ellison and Levin 1998). Social ties can instill a sense of responsibility and concern for others that then lead individuals to engage in behaviors that protect the health of others, as well as their own health. Social ties provide information and create norms that further influence health habits. Thus, in a variety of ways, social ties may influence health habits that in turn affect physical health and mortality.

Psychosocial Explanations

Research across disciplines and populations suggests possible psychosocial mechanisms to explain how social ties promote health. Mechanisms include (but are not limited to): social support, personal control, symbolic meanings and norms, and mental health. While most studies focus on only one or two of these mechanisms, it is clear that connections between mechanisms are complex, and that these interconnections may explain the linkage between social ties and health better than any single mechanism ( Thoits 1995; Umberson et al. 2010).

Social support refers to the emotionally sustaining qualities of relationships (e.g., a sense that one is loved, cared for, and listened to). Hundreds of studies establish that social support benefits mental and physical health ( Cohen 2004; Uchino 2004). Social support may have indirect effects on health through enhanced mental health, by reducing the impact of stress, or by fostering a sense of meaning and purpose in life ( Cohen 2004; Thoits 1995). Supportive social ties may trigger physiological sequelae (e.g., reduced blood pressure, heart rate, and stress hormones) that are beneficial to health and minimize unpleasant arousal that instigates risky behavior ( Uchino 2006). Personal control refers to individuals' beliefs that they can control their life outcomes through their own actions. Social ties may enhance personal control (perhaps through social support), and, in turn, personal control is advantageous for health habits, mental health, and physical health ( Mirowsky and Ross 2003; Thoits 2006).

Many studies suggest that the symbolic meaning of particular social ties and health habits explains why they are linked. For example, meanings attached to marriage and relationships with children may foster a greater sense of responsibility to stay healthy, thus promoting healthier lifestyles ( Nock 1998; Waite 1995). Studies on adolescents often point to the meaning attached to peer groups (e.g., what it takes to be popular) when explaining the influence of peers on alcohol, tobacco, and drug use ( Crosnoe, Muller, and Frank 2004). The meaning of specific health behaviors within social contexts may also vary. For example, Schnittker and McLeod (2005) argue that racial-ethnic identity may correspond with the meaning of certain health behaviors, such as consuming particular foods or avoiding alcohol, in ways that promote and sustain those behaviors. Moreover, the notion of "meaning" may help explain health behavior contagion across social networks: for example, the spread of obesity across social networks appears to be influenced by perceptions of social norms about the acceptability of obesity and related health behaviors (e.g., food consumption, inactivity) among network members who are socially close, rather than members who are simply geographically close ( Christakis and Fowler 2007; Smith and Christakis 2008). In a more fundamental way, greater social connection may foster a sense of "coherence" or meaning and purpose in life, which, in turn, enhances mental health, physiological processes, and physical health ( Antonovsky 1987).

Mental health is a pivotal mechanism that works in concert with each of the other mechanisms to shape physical health ( Chapman, Perry, and Strine 2005). For instance, the emotional support provided by social ties enhances psychological well-being, which, in turn, may reduce the risk of unhealthy behaviors and poor physical health ( Kiecolt-Glaser et al. 2002; Thoits 1995; Uchino 2004). Moreover, mental health is an important health outcome in and of itself. The World Health Organization identifies mental health as an essential dimension of overall health status ( World Health Organization 2007). However, the prevalence of mental disorders and their consequences for individuals and societies are often underappreciated by policy makers and private insurers. Data from the National Comorbidity Survey Replication indicate that 26.2 percent of noninstitutionalized U.S. adults suffer from a mental disorder in a given year ( Kessler et al. 2005). As the leading cause of disability in both low- and high-income countries, mental disorders account for over 37 percent of the total years of healthy life lost due to disability ( Mathers et al. 2006).

Physiological Explanations

Psychologists, sociologists, and epidemiologists have contributed a great deal to our understanding of how social processes influence physiological processes that help to explain the link between social ties and health. For example, supportive interactions with others benefit immune, endocrine, and cardiovascular functions and reduce allostatic load, which reflects wear and tear on the body due, in part, to chronically overworked physiological systems engaged in stress responses ( McEwen 1998; Seeman et al. 2002; Uchino 2004). These processes unfold over the entire life course, with effects on health. Emotionally supportive childhood environments promote healthy development of regulatory systems, including immune, metabolic, and autonomic nervous systems, as well as the hypothalamic-pituitary-adrenal (HPA) axis, with long-term consequences for adult health ( Taylor, Repetti, and Seeman 1997). Social support in adulthood reduces physiological responses such as cardiovascular reactivity to both anticipated and existing stressors ( Glynn, Christenfeld, and Gerin 1999). Indeed, continuously married adults experience a lower risk of cardiovascular disease compared with those who have experienced a marital loss, in part due to the psychosocial supports conferred by marriage ( Zhang and Hayward 2006).

THE DARK SIDE OF SOCIAL RELATIONSHIPS

While social relationships are the central source of emotional support for most people, social relationships can be extremely stressful ( Walen and Lachman 2000). For example, marriage is the most salient source of both support and stress for many individuals ( Walen and Lachman 2000), and poor marital quality has been associated with compromised immune and endocrine function and depression ( Kiecolt-Glaser and Newton 2001). Sociological research shows that marital strain erodes physical health, and that the negative effect of marital strain on health becomes greater with advancing age ( Umberson et al. 2006).

Relationship stress undermines health through behavioral, psychosocial, and physiological pathways. For example, stress in relationships contributes to poor health habits in childhood, adolescence, and adulthood ( Kassel et al. 2003). Stress contributes to psychological distress and physiological arousal (e.g., increased heart rate and blood pressure) that can damage health through cumulative wear and tear on physiological systems, and by leading people of all ages to engage in unhealthy behaviors (e.g., food consumption, heavy drinking, smoking) in an effort to cope with stress and reduce unpleasant arousal ( Kassel, Stroud, and Paronis 2003). The propensity to engage in particular risky health behaviors in response to stress appears to vary over the life course. For example, stress is associated with more alcohol consumption in young adulthood and greater weight gain in mid-life ( Umberson et al. 2010). Relationship stress also undermines a sense of personal control and mental health, both of which are, in turn, associated with poorer physical health ( Mirowsky and Ross 2003).

It may seem obvious that strained and conflicted social interactions undermine health, but social ties may have other types of unintended negative effects on health. For example, relationships with risk-taking peers contribute to increased alcohol consumption, and having an obese spouse or friend increases personal obesity risk ( Christakis and Fowler 2007; Crosnoe et al. 2004). This "social contagion" of negative health behaviors operates via multiple mechanisms ( Smith and Christakis 2008). One key mechanism is social norms. Perceived social norms about drinking behavior influence alcohol consumption among young adults ( Thombs, Wolcott, and Farkash 1997), and friendship norms about dieting influence unhealthy weight control ( Eisenberg et al. 2005). Unsupportive social ties may also present barriers to improving health behaviors and outcomes. For example, Nagasawa and colleagues (1990) found that negative social environments and their perceived barriers predicted poor compliance to medical regimens among diabetes patients.

Caring for one's social ties may also involve personal health costs. For example, providing care to a sick or impaired spouse imposes strains that undermine the health of the provider, even to the point of elevating mortality risk for the provider ( Christakis and Allison 2006). Caring for a sick or impaired spouse is associated with increased physical and psychiatric morbidity, impaired immune function, poorer health behavior, and worse health for the provider ( Schulz and Sherwood 2008). Moreover, the recipient of care may be negatively affected by interpersonal interactions with stressed caregivers ( Bediako and Friend 2004). Middle-aged adults, particularly women, often experience exceptionally high caregiving demands as they contend with the challenge of simultaneously rearing children, caring for spouses, and looking after aging parents ( Spain and Bianchi 1996). The combination of smaller families (to share in the care-giving of aging parents) and an aging population mean that the multigenerational demands of social ties may become more pronounced in the future.

CUMULATIVE ADVANTAGE AND DISADVANTAGE

All Americans are not at equal risk for risky health behaviors, morbidity, and premature mortality. Throughout life, we are exposed to social conditions that promote or undermine health, and over time these exposures accumulate to create growing advantage or disadvantage for health in socially patterned ways. Thus, social variation in relationships/health processes provides information that may be used to address social disparities in health.

The most salient social ties for health vary over the life course, with parents having the greatest influence on children's health, peers becoming particularly important in adolescence, intimate partners becoming most important in adulthood, and adult children taking an elevated role in later life ( Umberson et al. 2010). The principal explanatory mechanisms may also vary over the life course. For example, stressful family interactions may have their greatest impact on children's health, while peer pressure and the social meaning of health habits (e.g., pressure to experiment with tobacco, alcohol, and drugs) may have their greatest impact in adolescent relationships, and social control of health habits may be most important in adult relationships.

Some effects of social ties are more immediate, while others slowly build over time. For example, at any given point in time, ongoing social ties affect mental health and health behavior-for better or for worse. These effects may or may not dissipate over time, but recent work on the effects of distressed, disrupted, and emotionally unsupportive childhood environments on adult health shows that these effects reverberate throughout the life course ( Crosnoe and Elder 2004; Palloni 2006; Shaw et al. 2004). Certainly, chronic isolation or strain in social ties take an increasing toll over time on a host of health indicators including allostatic load ( Seeman et al. 2002), blood pressure ( Cacioppo et al. 2002), physical health ( Umberson et al. 2006), and mortality risk ( Berkman and Syme 1979).

COSTS AND BENEFITS OF SOCIAL RELATIONSHIPS: INEQUALITIES

Both quantitative (size and diversity) and qualitative (benefits and costs) aspects of social ties are demographically patterned and socially constructed. Regarding size, women tend to have larger confidant networks than men, as do whites compared with blacks, better-educated adults compared with less-educated, and, to a lesser extent, younger adults ( McPherson, Smith-Lovin, and Brashears 2006). Moreover, the diversity of social ties varies in patterned ways with, for example, better-educated adults engaged in more diverse personal networks ( McPherson et al. 2006). Sociodemographic variation in quantitative aspects of social ties may partly explain parallel variation in health disparities because both size ( Brummett et al. 2001) and diversity ( Cohen et al. 1997) of social ties enhance health. People with a greater number of ties have a larger pool of confidants from which to connect and to receive social support and health-relevant information.

In general, we know little about how the benefits and costs of social ties vary across sociodemographic groups, but some evidence suggests that there is variation. Most attention has been devoted to gender differences, particularly in the context of marriage. Historically, marriage has conferred more health gains for men than for women. Men not only experience greater health benefits through the positive lifestyle and health behaviors that often accompany marriage ( Waite 1995), they also experience fewer costs from spousal caregiving, childrearing, caring for aging parents, and balancing work/family demands ( Spain and Bianchi 1996). The availability, costs, and benefits of social ties may also vary by race. For instance, blacks are less likely to be married than whites. Yet evidence regarding costs and benefits is mixed. African Americans may experience more marital strain ( Broman 1993; Umberson et al. 2005; cf. Kiecolt, Hughes, and Keith 2008) and receive fewer economic gains from marriage compared to whites ( Willson 2003), yet some studies find African Americans have historically received more health benefits from marriage than whites ( Kiecolt et al. 2008; Liu and Umberson 2008). Disparities in the quantity and quality of social ties exist across socioeconomic statuses as well. More educated adults have a larger number of close confidants and may experience less stress in their relationships. For instance, women with a high school degree or less are roughly twice as likely to divorce within 10 years of their first marriage compared with women having at least a bachelor's degree ( Martin 2006). Notably, differential access, benefits, and costs to social ties across sociodemographic groups are not immutable; recent work shows that these differentials have changed significantly over time ( Liu and Umberson 2008; McPherson et al. 2006).

SOCIAL TIES: AN INVESTMENT IN POPULATION HEALTH

Research shows that social ties influence multiple and interrelated health outcomes, including health behaviors, mental health, physical health, and mortality risk. Thus, a policy focus on social ties may prove to be a cost-effective strategy for enhancing health and well-being at the population level ( McGinnis et al. 2002; Mechanic and Tanner 2007). Social ties may be unique in their ability to affect a wide range of health outcomes and to influence health (thus cumulative health outcomes) throughout the entire life course. Moreover, interventions and policies that strengthen and support individuals' social ties have the potential to enhance the health of others connected to those individuals. For example, reducing strain and improving health habits of a married person may benefit the health of both partners, as well any children they care for.

Recent work also shows that some health outcomes can "spread" widely through social networks. For example, obesity increases substantially for those who have an obese spouse or friends ( Christakis and Fowler 2007), and happiness appears to spread through social networks as well ( Fowler and Christakis 2008). These findings suggest that the impact of social ties on one person's health goes beyond that person to influence the health of broader social networks. Thus, policies and interventions should capitalize on this natural tendency for health-related attitudes and behaviors to spread through social networks by incorporating these amplification effects into the mechanics of interventions and their cost-benefit estimates ( Smith and Christakis 2008).

Finally, enhanced relationship/health linkages can be viewed as preventive medicine. While social ties may serve to improve health outcomes for those who develop serious health conditions, social ties may help prevent these conditions from developing in the first place. Policies that promote and protect social ties should have both short-term and long-term payoffs. If social ties foster psychological well-being and better health habits throughout the life course, then social ties can add to cumulative advantage in health over time-a worthwhile goal for an aging population. Better health means reduced health care costs as well as better quality of life for Americans, regardless of their age.

PUBLIC POLICY: SOCIAL TIES AND HEALTH OF THE POPULATION

Social ties and their connection to health have important implications for health policy. Indeed, some existing social policies and programs implicitly and indirectly incorporate social ties as mechanisms for enhancing population health and well-being. For example, many programs concerned with health of the elderly (e.g., home health services and meal deliveries) direct attention to the impact of social isolation/connection on health. Healthy People 2010, a nationwide health promotion plan developed by the Department of Health and Human Services, recognizes that social ties play an important role in influencing health habits ( U.S. Department of Health and Human Services 2000). The Healthy Marriage Initiative recognizes that marriages characterized by supportive interactions benefit the health of children as well as spouses ( U.S. Department of Health and Human Services n.d.). The Family Medical Leave Act (FMLA) allows eligible employees to take up to 12 weeks of unpaid, protected leave over a 12-month period to attend to certain medical and family-related needs, such as the birth of a child or caring for an immediate family member ( U.S. Department of Labor 2009).

Yet in some cases these policies and programs do not benefit the populations that need them the most, or they unintentionally undermine the health of the target population and others in their social network. For example, FMLA may benefit those who receive care, but it also may be financially prohibitive for caregivers who do not have an employed spouse or enough savings to support them through the time off work, yet those with the fewest financial resources and social ties may need assistance the most. Further, in rare cases, experimental programs have reported worse health outcomes among subgroups of participants. A randomized experiment of the effects of support groups for women with breast cancer found that, compared to women in the control group, the physical functioning of women who participated in the peer discussion group improved if they reported low levels of emotional support from their partners at baseline, but it deteriorated if they reported initially high levels ( Helgeson et al. 2000). Another psychosocial intervention tested individualized emotional and instrumental support services in an effort to improve one-year survival outcomes of adults recovering from myocardial infarction. This study found that, compared to a control group, men in the intervention group exhibited similar mortality rates while women exhibited higher mortality rates during the one-year follow-up ( Frasure-Smith et al. 1997). Thus, we must develop a policy foundation that integrates scientific evidence on the linkages between social ties and health, and that foundation must do two things: (1) ensure that policies and programs benefit the populations that need them; and (2) maximize health-related benefits for recipients while minimizing costs for providers and recipients.

POLICY FOUNDATION

Poor mental and physical health and unhealthy behaviors exact a huge toll on individuals, families, and society. Solid scientific evidence establishing the causal impact of social ties on health provides the impetus for policy makers to ensure that U.S. health policy works to protect and promote social ties that benefit health. Scientific evidence supports the following premises, and it is from this empirical footing that we can build a policy foundation for promoting both social ties and health:

Social ties affect mental health, physical health, health behaviors, and mortality risk.

Social ties are a potential resource that can be harnessed to promote population health.

Social ties are a resource that should be protected as well as promoted.

Social ties can benefit health beyond target individuals by influencing the health of others throughout social networks.

Social ties have both immediate (mental health, health behaviors) and long-term, cumulative effects on health (e.g., physical health, mortality), and thus represent opportunities for short- and long-term investment in population health.

Although social ties have the potential to benefit health, policy efforts must recognize that social ties also have the potential to undermine health, and that the link between social ties and health may vary across social groups. For example, gender, race, and age are associated with different levels and types of responsibilities, strains, and resources in social ties that then influence personal health habits as well as the health of significant others. In order to be effective, policies and interventions must account for the ways in which social constraints and resources influence health across social groups ( House et al. 2008). Moreover, care must be taken to develop strategies that increase the power of social ties to enhance individual health without imposing additional strains on care providers. Thus, we suggest two additional policy components for the basic foundation suggested above:

Caveat: social ties-overburdened, strained, conflicted, abusive-can undermine health.

The costs and benefits of social ties are not distributed equally in the population (e.g., age, socioeconomic status, gender, race variation).

POLICY GOALS

How can policy makers use the scientific findings on social ties and health to advance population health and reduce social disparities in health? They can begin by addressing six fundamental goals.

Promote Benefits of Social Ties

Support and promote positive features of social ties (e.g., supportive interactions, healthy lifestyle norms). For example, Health and Human Service's Healthy Marriage Initiative is designed to promote positive marital interactions that may foster mental and physical health of couples and their children. This initiative uses a multifaceted approach, including public awareness campaigns on responsible parenting and the value of healthy marriages, as well as educational and counseling services delivered through local organizations such as schools and faith-based organizations. This goal should also speak to policies that deny marriage to same-sex couples. The absence of legal marriage may reduce the benefits of committed partnerships for the health of individuals in gay and lesbian relationships ( Herek 2006; King and Bartlett 2006; Wienke and Hill 2009).

Do No Harm

Avoid policies, programs, and interventions that increase relationship burdens and strains or that undermine positive features of relationships. For example, many programs for the sick and elderly increase caregiving responsibilities for family members-responsibilities that may impose stress on caregivers and on family relationships. This problem is exacerbated by hospital and insurance policies that force family members to provide medical care at home. These costs are borne more heavily by women, minorities, and those with fewer socioeconomic resources. Policy efforts should recognize that specific programs may benefit some groups but harm others.

Reduce Social Isolation

This addresses one of the most fundamental findings from research on social ties and health: The most socially isolated Americans are those at greatest risk of poor health and early mortality ( Brummett et al. 2001). Policies can reduce the risk of social isolation in the first place by enhancing our educational system to impart social-emotional skills, interests in civic engagement, and meaningful employment ( Greenberg et al. 2003); by ensuring that all communities are economically developed and contain public places to safely congregate and exercise ( Mechanic and Tanner 2007); and by fostering stable marriages and families for all Americans. Notably, some groups are more likely than others to experience social isolation. For example, widowhood increases the risk of social isolation. Women are more likely than men to be widowed, and widowhood affects a higher proportion of African Americans than other races, and at earlier ages; among those aged 65 to 74, 24.3 percent of African Americans are widowed compared to 14.8 percent of whites ( U.S. Census 2009). Coordinated programs could help identify socially isolated adults, perhaps through their physicians, and they could mobilize local resources to offer social and instrumental support to these individuals.

Reduce Harm

Prevent and alleviate negative features of social ties. For example, work to reduce strains for those who provide care to children, sick or impaired significant others, and the elderly, remaining cognizant of unintended effects on caregivers. In addition, prevent or alleviate harm caused by negative social ties, such as abusive parent-child relationships and strained marriages.

Coordinate Policies and Programs

Many existing policies and programs, at least implicitly, address some aspect of social ties in relation to health. These existing strategies can be mapped onto a general strategy of promoting positive relationship/health linkages. This will make gaps and overlaps between strategies more apparent, and it will allow greater coordination of services for helping professionals and for citizens seeking services.

Provide Help Where Help Is Most Needed

Some populations are at greater risk for illness and disease than others, and these groups should receive higher priority in policy efforts. In particular, some populations are more likely to be socially isolated (e.g., the poor and the elderly), and some are more likely to be burdened by caring for others in their social networks (e.g., women, especially African American women). Existing policies should also be re-evaluated to ensure that they help the populations that need them most. For instance, the FMLA may be entirely unhelpful for low-income adults who have no alternative source of income and are more likely to be without alternative sources of instrumental and emotional support.

FUTURE RESEARCH

Social scientists can advance this policy agenda by addressing several specific issues. First, it is important to identify individuals most at risk, as well as explanations for heightened risk. Individuals who are socially isolated may be at the greatest health risk. Several studies suggest that the relationship between social ties and health is nonlinear so that individuals with no social ties or very few social ties exhibit the most pronounced risk of poor health ( Brummett et al. 2001; Cohen et al. 1997; Seeman et al. 2002). Despite the considerable evidence linking social isolation to poor health outcomes, the causal mechanisms are poorly understood. We need to investigate the possibility that differences between socially isolated and socially integrated adults-in health behaviors, emotional and instrumental support networks, physiological responses to anxiety, or other mechanisms-explain the linkage. Sociologists should direct attention to the social distribution of isolation and the possibility that the consequences of social isolation vary across social groups.

Second, the broader social context-as structured by age, class, race, and gender-influences the formation and quality of social ties as well as the processes through which social ties affect health. However, the ways in which these structural variables shape social ties are not well understood, and few studies consider how these structural variables might modify relationship/health linkages. Likewise, social ties may shape the way that structural variables influence health. For instance, marital status may alter the inverse association between educational attainment and mortality risks, at least for men ( Montez et al. 2009). This type of research is needed in order to identify at-risk populations as well as explanatory mechanisms linking social ties to health outcomes across social groups.

Third, past work on social ties and health habits tends to emphasize the benefits of social ties for health, yet research on stress clearly shows that strained social ties undermine health. Given the ability of social ties to have both positive and negative effects on health, existing research has likely underestimated the true impact of social ties on health. Future research should consider how the positive and negative facets of social ties work together to influence health outcomes, as well as consider how this balance may vary over the life course and across social groups.

A growing body of theoretical and empirical work illustrates how social conditions foster cumulative advantage and disadvantage for health over the life course. This may be a case of the rich getting richer while the poor get poorer, in that strained and unsupportive relationships in childhood launch into motion a cascade of factors-such as increased risk for depression, low personal control, and poor health habits-that lead to poorer health and more strained and less supportive relationships across the life course. Scholars should consider this cascading process, and they should identify at-risk populations as well as the most important modifiable risk and protective factors in their social relationships. Scholars should also help to clarify when social ties impact health habits, as well as identify which social ties are most important to health at different life stages.

In addition, future research will benefit from methodological considerations, including a greater focus on prospective survey designs and corresponding longitudinal analyses, dyadic information about social relationships, and qualitative data. Prospective designs are essential in order to consider how relationship/health linkages and explanatory mechanisms unfold over time. This approach fits with the life course notion that determinants of current health originate early in life and accumulate across the life span ( Ben-Shlomo and Kuh 2002). Taking full advantage of prospective surveys through longitudinal data analysis and wider application of multilevel modeling could shed more light on the social processes involved in building, sustaining, and benefiting from social ties across the life course.

Most studies on social ties and health use individual-level data, as surveys typically collect information from one member per household. However, social ties, by definition, involve more than one person. Studies that include dyads show that individuals in the same relationship often experience and report on their relationship in quite different ways ( Proulx and Helms 2008). Independent reports, as well as discrepancies between reports, may be linked to health outcomes. We should take advantage of existing longitudinal data sets that include more than one focal individual. New data collection efforts should go beyond the individual to include data from a range of linked social ties. As recent work shows, including reports from several network members may reveal important relationship/health linkages that go beyond one individual ( Smith and Christakis 2008).

Finally, most research on social ties and health has relied on assessment of quantitative data sources. Quantitative data are essential for identifying patterns between variables in the general population and, particularly, for revealing how social location (e.g., as defined by life course stage, race, and gender) is associated with regularity in social experiences (e.g., relationships and health). However, population-level data are limited in their ability to reveal rich social contexts that allow us to analyze the meanings, dynamics, and processes that link social ties to health over time. Thus, blending qualitative and quantitative methods provides the opportunity to build on the strengths of both methodologies and to address how structure and meaning coalesce to shape health outcomes at the population level ( Pearlin 1992). Information obtained from qualitative data may also suggest new explanations (e.g., new psychosocial mechanisms or connections between mechanisms) for relationship/health linkages, and for group differences in those linkages, and those explanations can be further explored using population-level data.

CONCLUSION

Solid scientific evidence shows that social relationships affect a range of health outcomes, including mental health, physical health, health habits, and mortality risk. Sociologists have played a major role in establishing these linkages, in identifying explanations for the impact of social relationships on health, and in discovering social variation (e.g., by age and gender) in these linkages at the population level. The unique perspective and research methods of sociology provide a scientific platform to suggest how policy makers might improve population health by promoting and protecting Americans' social relationships. Recent and projected demographic trends should instill a sense of urgency in developing policy solutions. Specifically, the confluence of smaller families, high divorce rates, employment-related geographical mobility, and population aging means that adults of all ages, and in particular the elderly, will be at increasing risk of social isolation and shrinking family ties in the future ( Cacioppo and Hawkley 2003).

Acknowledgments

An earlier version of this article was presented at the 2009 annual meeting of the American Sociological Association. This research was supported by National Institute on Aging grant RO1AG026613 (PI: Debra Umberson), National Institute of Child Health and Human Development grant 5 R24 HD042849 (PI: Mark D. Hayward) and 2 T32 HD007081 (PI: Robert A. Hummer) awarded to the Population Research Center at the University of Texas at Austin.

Biographies

Debra Umberson is professor of sociology and a faculty associate in the Population Research Center at the University of Texas at Austin. Her research focuses on relationships and health across the life course. Her current research, supported by the National Institute on Aging, considers how different types of relationships influence health behaviors over the life course.

Jennifer Karas Montez is a doctoral candidate in the Department of Sociology and Population Research Center at the University of Texas at Austin. Her research concerns socioeconomic and gender disparities in health and mortality in later life, and examines how social, behavioral, and biological mechanisms interact across the entire life course to produce those disparities.

References

Mathers Colin D, Lopez Alan D, Murray Christopher JL. The Burden of Disease and Mortality by Condition: Data, Methods, and Results for 2001. In: Lopez AD, Mathers CD, Ezzati M, Jamison DT, Murray CJL, editors. Global Burden of Disease and Risk Factors. The World Bank and Oxford University Press; 2006. pp. 45-240. Retrieved January 29, 2010 ( [http://files.dcp2.org/pdf/GBD/GBD03.pdf) Google Scholar]

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Social Relationships and Health: A Flashpoint for Health Policy

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Social relationships-both quantity and quality-affect mental health, health behavior, physical health, and mortality risk. Sociologists have played a central role in establishing the link between social relationships and health outcomes, identifying explanations for this link, and discovering social variation (e.g., by gender and race) at the population level.

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To begin the courtship process, a male will dangle his legs with a fish and begin to fly while calling and circling over to his nest.

The males will also begin to feed the females as she asks for food through her body movements by positioning her body horizontally while puffing up her crest feathers and having her wings stay close to her body.

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Mating displays have evolved as a form of adaptation in order to improve success in reproduction.

With the presence of natural selection, individuals who are able to perform attractive displays often gain a competitive advantage in attracting mates of their species.

Overtime, preferences over certain displays become prevalent which leads to more complex displays being developed as the organisms with these traits are more likely to pass on their genes through the use of reproduction.

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SEXUAL SELECTION, OR ADAPTATION TO MATING DEMANDS - In the Light of Evolution - NCBI Bookshelf

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In The Descent of Man, and Selection in Relation to Sex, Darwin defined sexual selection as the “advantage which certain individuals have over other individuals of the same sex and species, in exclusive relation to reproduction.” Darwin appreciated that sexual selection could be mediated by intrasex…

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Mating displays are behaviors designed to build attraction in order to mate with the opposite sex throughout the animal kingdom.

These displays are often multimodal, meaning that they consist of various signals that trigger different senses.

Signals consisting of olfactory and vibratory senses are extremely common and can be viewed in a variety of animals.

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Ethology. 2019 Aug; 125(8): 503-515.

Section Editor: Redouan Bshary

Abstract

Courtship displays are behaviours aimed to facilitate attraction and mating with the opposite sex and are very common across the animal kingdom. Most courtship displays are multimodal, meaning that they are composed of concomitant signals occurring in different sensory modalities. Although courtship often strongly influences reproductive success, the question of why and how males use multimodal courtship to increase their fitness has not yet received much attention. Very little is known about the role of different components of male courtship and their relative importance for females. Indeed, most of the work on courtship displays have focused on effects on female choice, often neglecting other possible roles. Additionally, a number of scientists have recently stressed the importance of considering the complexity of a display and the interactions between its different components in order to grasp all the information contained in those multimodal signals. Unfortunately, these methods have not yet been extensively adapted in courtship studies. The aim of this study was to review what is currently known about the functional significance of courtship displays, particularly about the role of multimodality in the courtship communication context. Emphasis is placed on those cases where a complete picture of the communication system can only be assessed by taking complexity and interaction between different modalities into account.

Keywords: elaborate displays, female preference, multisensory signals, sexual behaviour, sexual stimulation

1. INTRODUCTION

Courtship is the suite of behaviours displayed by an individual to attract and eventually reproduce with an individual of the opposite sex (Bastock, 1967). Because courtship takes place within the scope of competition among conspecifics of the same sex, it is generally assumed to have evolved through sexual selection mechanisms. Courtship is usually performed by males towards females, but often involves an interaction between the two sexes (Huxley, 1914; Ota, Gahr, & Soma, 2015; Soma & Iwama, 2017), or a reversal of the usual sex roles. Historically, male courtship behaviour has been studied far more than female behaviour, and as a result, most of the examples we provide in this review refer to male courtship. However, our arguments apply equally well to female courtship.

Courtship displays are extremely diverse. They are known to occur in many sensory modalities and can vary substantially even between closely related species (Andersson, 1994; Bastock, 1967). The most studied courtship displays in the animal kingdom are the visually conspicuous dances and acoustic calls of birds. Vibratory and olfactory signals are also very common, especially in arthropods (Hebets & Uetz, 1999; Houck & Reagan, 1990). Courtship can vary in its duration, with some species having only a few seconds courtship interaction before mating (Bastock & Manning, 1955), to several days of mutual interaction before copulation, as in the dwarf seahorse ( Hippocampus zosterae) (Masonjones & Lewis, 1996) or emperor penguin ( Aptenodytes forsteri)(Ancel, Gilbert, & Beaulieu, 2013). Secondary sexual characters and courtship are generally more conspicuous and intense in polygamous species, but are also present in socially monogamous species (Kirkpatrick, Price, & Arnold, 1990).

Past work focused mainly on the most conspicuous component of courtship signals (typically visual or auditory). However, with the possible exception of courtship occurring in environments in which some modalities cannot be transmitted, such as in complete darkness, most courtship displays occur in at least two sensory modalities and include more than one signal aimed at separate sensory systems of the receiver. Those components may occur sequentially at different times during courtship. This is the case when males use the first component to attract females from a distance, and then another when the female is at a closer range, for example in the ring‐necked pheasant Phasianus colchicus (Mateos & Carranza, 1999). Alternatively, the components can occur simultaneously, leading to very complex signals such as in birds performing conspicuous courtship composed of dances and calls (Andersson, 1994). We refer to these types of courtship as multicomponent if the components occur in the same sensory modalities, and multimodal or multisensory if they occur in two or more sensory modalities (Partan & Marler, 2005; Rowe, 1999). Complex multicomponent and multimodal courtship displays have now been described for a large number of taxa (Knörnschild, Feifel, & Kalko, 2014; Manica, Macedo, Graves, & Podos, 2017; Mowles, Jennions, & Backwell, 2017; Ota et al., 2015; Preininger et al., 2013), and for both sexes. For example, in the blue‐capped cordon‐bleu ( Uraeginthus cyanocephalus), Ota et al. ( 2015) documented a multimodal courtship display composed of visual, auditory and tactile components performed by both males and females during courtship interactions.

Courtship plays an essential role in reproduction as it is often required for copulation to occur, with the exception of sneaky and forced copulations. Yet the ultimate causes at work are still poorly understood, as the links between the multiple signals of complex, elaborate displays and fitness benefits are far from being clear. In particular, in the context of multicomponent courtship displays, it is still unclear what the role of each component is and why very elaborate behaviours have sometimes evolved in cases where simpler displays should suffice. As Candolin ( 2003) noted, courtship behaviour is usually studied as a simple structure, even though it almost invariably includes several components. Hundreds of studies have focused on single components of male courtship and investigated their relevance for female choice or female stimulation. With surprisingly few exceptions, studies on multimodal courtship rarely examine how females integrate multiple components to reach mating decisions, or whether courtship signals have effects beyond mate choice. The traditional "trait‐based" approach assesses the effects of individual signals sent by males on female preference and choice (Schacht & Grote, 2015). Experimentally, this is achieved via cue‐isolation experiments, where single stimuli are presented separately to the choosing sex, typically the female. This approach raises at least three issues. First, experiments of this type rarely accurately reflect the complexity of courtship interactions as they occur in nature. Even in cases in which single modality components may reach the receiver in isolation from the rest of the signal, this does not always occur in a symmetric way in the wild. For example, in audiovisual communication, the sender could be visually hidden but easily heard, whereas the opposite scenario is unlikely unless there is masking by strong background noise. Cue‐isolation experiments have rarely taken this into account and usually involve playback stimuli separated from other stimuli that typically would accompany them. Such experiments therefore often disregard the natural conditions in which the behaviour evolved. Second, by focusing on the role of courtship on female choice and preference, researchers often neglect other potential functions of courtship. For instance, few studies have examined the role of male courtship components on female sexual stimulation, which may have a strong influence on male reproductive success (Beach, 1975; Lehrman & Friedman, 1969). Finally, the trait‐based approach ignores information contained in the interaction between different components of courtship signals. An increasing number of theoretical (Candolin, 2003; Hebets & Papaj, 2005; Partan & Marler, 1999; Stein & Standford, 2008) and empirical studies (Ronald, Zeng, White, Fernandez‐Juricic, & Lucas, 2017; Stange, Page, Ryan, & Taylor, 2016; Taylor & Ryan, 2013) have shown that the response to multiple signals differs from the simple sum of the responses to each component taken separately. This emphasizes the potential additional value provided by the interaction between components (Taylor & Ryan, 2013).

Our overall goal is to provide a concise overview of what is known today about multimodal courtship displays, from both the empirical and theoretical point of view. For recent reviews about more general themes linked to the present paper, see Rosenthal ( 2017) for a thorough review of mate choice, Prum ( 2012) for a novel perspective on the role of beauty and attractiveness in sexual selection, and Ryan ( 2018) for a complete overview of the sensory bias theory. Because identifying the different functions of a particular behaviour is fundamental to understanding its evolution, the first aim of this paper was to review what is currently known about the general roles of courtship displays. Then, we will discuss how different signals can be composed to form complex multicomponent or multimodal courtship displays. Finally, with the help of recent theoretical work regarding multimodal communication, we will focus on assessing the function of complex behavioural signalling in the reproductive context to stress the importance of studying such signals as a complex unity.

2. FUNCTIONAL SIGNIFICANCE OF COURTSHIP

The most studied function of courtship is that of highlighting male quality and thus increasing reproductive success by enhancing the chances of the male to obtain a mate. However, courtship displays have other important functions.

2.1. Sex and species recognition

The ability of an organism to recognize members of its own species, and in particular of the opposite sex, is fundamental to produce offspring. In various taxa, closely related species might be morphologically very similar. In such cases, courtship behaviour can serve to identify members of a particular species, thereby reducing the risk of inter‐specific mating in sympatric species. In the Drosophila genus, several features of courtship songs vary between species and are thought to be responsible for maintaining sexual isolation between closely related species (Saarikettu, Liimatainen, & Hoikkala, 2005). Another example comes from a recent study on birds of paradise ( Lophorina genus), where the authors analysed the audiovisual courtship displays of individuals in New Guinea (Scholes & Laman, 2018). By highlighting differences in ornament exposition in the courtship displays of birds previously thought to belong to only one species, they could support previous molecular and morphological analysis (Irestedt, Batalha‐Filho, Ericson, Christidis, & Schodde, 2017) and confirm the existence of several allopatric species. As a further example, in field crickets of the Teleogryllus genus, male calls that serve to attract females are thought to be important for pre‐zygotic isolation (Hoy, Hahn, & Paul, 1977). Finally, in Heliconus butterflies, male multimodal courtship based on olfactory and visual signals is thought to be a powerful driver of reproductive isolation (Southcott & Kronforst, 2017). Similarly, in monomorphic species where the two sexes look alike, courtship and response to courtship provide important information about the sex of the potential partner, for example in the ring dove (Lehrman, 1964; Lovari & Hutchison, 1975). Even though reproductive isolation due to mate choice has been long seen as a main driving force of speciation (Lande & Kirkpatrik, 1988), in some cases, courtship might not be sufficient to maintain reproductive isolation. In Drosophila heteroneura and Drosophila silvestris, for example, experimental crosses between the two species showed that courtship behaviour has a minor role in reproductive isolation (Boakes, DeAngelis, & Andreadis, 1997) and that the isolation between the species is due to the failure of heterospecifics to perform courtship behaviour at all, rather than differences in courtship repertoire such as courtship duration (Boakes, Andreadis, & Witzel, 2000).

2.2. Sexual stimulation and synchronization of mating behaviour

In species with a distinct breeding season, the transition to reproductive status is triggered by environmental factors such as photoperiod, temperature or light intensity (Farner, 1964; Gemeno & Haynes, 2001). In some species, additional stimulation is sometimes necessary for mating to occur, and courtship and mating can induce the female to become physiologically responsive and eventually allow fecundation.

Within this context, a considerable amount of research has been carried out on web‐building spiders. In orb‐web spiders, one function of the abdominal wagging performed by the courting male on the female is thought to be an increase in pressure of the haemolymph which facilitates sperm transfer after copulation (Huber, 2004; Wignall & Herberstein, 2013). In the wolf spider ( Stegodyphus lineatus), courtship pre‐mating vibratory behaviour seems to stimulate the receptive female to mate (Maklakov, Bilde, & Lubin, 2003). In salamander of the Plethodontidae family, sexual pheromones delivered by males during courtship shorten the latency of females to mate and increase female sexual receptivity (Houck & Reagan, 1990; Houck et al., 2008). In the ring dove ( Streptopelia risoria), male courtship is responsible for hormonal and physiological changes that trigger oviduct growth in females, making reproduction possible (Lehrman, 1964). Lovvorn, Mossotti, Wilson, and McKay ( 2012) described the courtship behaviour of spectacled eiders ( Somateria fischeri) and hypothesized that the more likely role of courtship in this species was to accelerate female hormonal development in order for them to be ready to mate during the short time windows their polar habitat offers.

Courtship can also be useful for spatial synchronization of mating behaviour in species where individuals are spatially dispersed, for example as a means to attract females to a courting male's territory or to a breeding site. In field crickets, males use a long‐range calling song to attract distant females (Alexander, 1961). The use of long‐distance infrasound calls has also been proposed to attract females to mating leks in cetacean species where individuals can be several hundreds of kilometres apart (Herman, 2016).

2.3. Female choice process

According to sexual selection theory, females choose a sexual partner because of the relatively greater benefits potentially acquired through mating with this individual. Those benefits are traditionally classified as direct if females gain access to territory, help in parental care or other resources, and indirect if they are gained only by the offspring, for example, good genes and/or the capacity to attract mates (Andersson, 1994). With courtship, males may signal potential benefits to females, and females can assess these signals to make a mating decision. A large number of male morphological traits have been shown to play a role in the female choice process, among them size (Harari, Handler, & Landolt, 1999), symmetry (Little, Jones, DeBruine, & Feinberg, 2008) and colour (Kodric‐Brown & Nicoletto, 2001). Some studies examined the link between particular features of courtship and female preference and choice. Among the features under female selection, we find rate and intensity of postural (Mowles, Jennions, & Backwell, 2018) or auditory (McComb, 1991) displays, as well as total courtship duration (Seymour & Sozou, 2009) and overall courtship rate (Berson & Simmons, 2018). In the golden‐collared manakin ( Manacus vitellinus), females show a preference for good motor skills by choosing to mate with males who display faster and longer (Barske, Schlinger, Wikelski, & Fusani, 2011; Fusani & Schlinger, 2012). All those characters are thought to indicate physical ability or general qualities of the males that can be passed to the offspring.

Not all male characters necessarily reflect some intrinsic quality. In some species, males are known for exploiting female sensory biases to influence their decisions. Sensory bias theory states that the most successful courtship displays are those which best stimulate specific aspects of the female sensory system which evolved through natural selection (Fuller, Houle, & Travis, 2005; Rowe, 1999). Although the sensory bias hypothesis has been applied to specific morphological and acoustic traits involved in mate choice (see reviews by Ryan & Cummings, 2013), examples of its extension to more elaborate courtship displays are rather scarce. One example comes from a study on grasshoppers ( Chorthippus biguttulus) where the authors studied the shape of the female preference function after artificially adding a new element to a naturally simple male courtship and thereby making it more complex (Reichert, Finck, & Ronacher, 2017). They found a complex relationship between female preference and the timing and the type of novel elements added to the original song and concluded that sensory bias could in some cases promote the evolution of male courtship signals. Another example comes from different species of bowerbirds, where it has been found that male preference for the coloured decorations they use to adorn their bowers matches with female colour preferences for food items during foraging (Madden & Tanner, 2003). A more sophisticated case of exploitation of a courtship receiver's perception has been suggested in the case of the great bowerbird ( Ptilonorhynchus nuchalis), where males place objects in a particular size order when building the court in front of their display avenue, creating a visual illusion which might make the displaying male look larger than he really is (Kelley & Endler, 2017).

During the early discussions about mate choice within an evolutionary context, Wallace argued that courtship vigour was the primary focus of females, while Darwin thought that the choice for ornamentation prevailed (Hoquet & Levandowsky, 2015; Prum, 2012). Both of them were probably right, as ornaments and vigour are often closely related (Cornuau, Rat, Schmeller, & Loyau, 2012), as motor displays or specific postures are necessary to expose ornaments and to make them more conspicuous (Hebets & Uetz, 2000; Jones, Byrne, & Wallman, 2014).

2.4. Moderation of female aggression

Additionally, courtship may act as a moderator of female aggressiveness and is particularly important in species where female cannibalism is common. In these cases, males should greatly benefit from displaying a behaviour that may prevent them from being killed. In orb‐web spiders ( Argiope keyserlingi) for example, male shuddering behaviour during courtship seems to have an effect on female cannibalism (Wignall & Herberstein, 2013).

3. WHY SO MUCH COMPLEXITY IN COURTSHIP DISPLAYS?

The presence of complex communication signals raises questions about their advantage over simpler ones. Producing complex signals might be energetically more costly and might increase predation rate (Partan & Marler, 2005) (but see Clark, 2012 for an alternative view on the potential cost of courtship, and Munoz and Blumstein ( 2012) regarding the cost of multisensory signals in general). Although it is clear in some cases that multimodal signalling improves mating success (Berson & Simmons, 2018; Girard, Elias, & Kasumovic, 2015; Stafstrom & Hebets, 2013) or increases physiological responses in females (Friedman, 1977), the proximate and ultimate mechanisms involved are unclear and elaborate behavioural signalling still lacks a unitary and broadly accepted theoretical framework.

The evolution of multicomponent signalling has recently received a great deal of attention, and several hypotheses have been proposed (Partan, 2013). For example, Hebets and Papaj ( 2005) stressed the fact that selection pressure can also act on the composed signal and not only on its independent components. Following the classification first proposed by Guilford and Dawkins ( 1991), the authors distinguish between "content‐based" and "efficacy‐based" hypotheses as possible mechanisms of complex signalling evolution. While the former focuses on the information carried by the signal, typically identity or quality in the context of courtship displays, the latter includes mechanisms improving the production, transmission and reception of a signal, including factors in the signalling environment or the receiver's sensory system. Later, Rowe and Halpin ( 2013) applied this same classification to the specific case of aposematic signals. Candolin ( 2003) conceived a similar classification for cues used in mate choice in a large number of taxa, but did not specifically address courtship or courtship components other than those involved in mate choice. Table 1 lists empirical studies reporting evidence for the benefits of multimodal courtship displays.

Table 1

Function of multicomponent/multimodal signals

Sensory modalities involved

Species

References

Improve signal efficiency

Provide multiple information about male qualities

Trigger different females responses

Reach different receivers

Signal at different environmental scales

Signal good neuro‐muscular coordination

Interaction between components yields new information

3.1. Improving signal efficiency

Rather than carrying information for the receiver, some parts of a multicomponent signal can instead act to improve signal efficiency, which is defined as the probability that the receiver perceives the signal in an intended way. This can be achieved by improving the way the receiver perceives the signal (receiver psychology hypothesis), or by improving transmission in the environment (backup signals hypothesis).

3.1.1. Receiver psychology in the courtship context

The receiver psychology hypothesis states that some signal components function to facilitate improved perception, discriminability, assessment or memorization of the information contained in the main signal (Guilford & Dawkins, 1991; Rowe, 1999). For instance, a sound can function to draw attention to a visual display, or vice versa. In anurans, for example, vocal sac inflation during courtship calling helps females to detect and discriminate male signals, thereby increasing male attractiveness (Starnberger, Preininger, & Hödl, 2014). Receiver psychology in the courting context is particularly relevant in noisy environments where the assessment of mates is difficult. For example, in a study on sexual signalling in several Magicicada species, Cooley and Marshall ( 2001) hypothesized that some parameters of the auditory courtship display increase the discriminability of individual calls among a chorus. It has long been established that low‐intensity signals are detected faster when they occur in more than one modality (e.g., Gielen, Schmidt, & Heuvel, 1983). This seems to equally apply to multicomponent and multimodal signals. Indeed, in an experiment with swordtails ( Xiphophorus nigrensis), it was found that females were faster to approach one of two males when the males differed on two rather than only one visual signal (body size and courtship vigour) (Reding & Cummings, 2017).

3.1.2. Back‐up signals hypothesis

The back‐up signal hypothesis specifies that multicomponent signals carry redundant information to limit errors in signalling, allowing the receiver to assess the final message with more accuracy (Johnstone, 1996; Møller & Pomiankowski, 1993). In those cases, we expect different traits to be correlated as the multiple "back‐up" components are redundant if the receiver's response to each is the same. Bro‐Jørgensen ( 2010) hypothesized that even though one signal might be sufficient to communicate a message, temporal and/or spatial environmental variability could lead to the evolution of multicomponent sexually selected signals ("fluctuating environment hypothesis," Munoz and Blumstein ( 2012) and Partan ( 2017)). Multicomponent displays could prevent interference from unpredictable variation and thereby ensure signal transmission under varying environmental conditions. In such cases, it is predicted that back‐up signals would evolve. For example, Colyott, Odu, and Gleason ( 2016) found that removing one courtship component (it being either visual, auditory, chemical or tactile) in Drosophila saltans did not alter the females' decision to mate. This indicates at least some degree of redundancy between different components. In the satin bowerbird ( Ptilonorhynchus violaceus), Keagy, Savard, and Borgia ( 2012) found that females used multiple traits of the bower constructed by the male, such as the size of the sticks used, the symmetry of the bower, or the colouration of decorations, to better estimate a composite measure of male cognitive abilities. They additionally found that some of those traits were redundant, for example stick size and bower symmetry seem to convey the same information. In canaries ( Serinus canaria), female responses to male courtship are multimodal and composed of a visual (copulation solicitation display, CSD) and auditory part (female‐specific trill, FST and contact calls, CC) (Amy, Salvin, Naguib, & Leboucher, 2015). Salvin ( 2018) found that the number of modalities used by both males and females within courtship interactions affected the response of the other sex. For example, males responded to a female's behaviour during courtship only when they could see and hear the female and not when they could only hear them. However, no enhancement effect between female visual and auditory signals seemed to occur, and those two signals seemed to be redundant for males.

3.2. Multicomponent courtship for multiple pieces of information

In contrast to the above hypotheses, the multiple message hypothesis states that each component of the multimodal signal carries different information, and therefore, each component taken separately should trigger a different response (Johnstone, 1996; Møller & Pomiankowski, 1993). For example, theoretical work by Wilson, Dean, and Higham ( 2013) investigated which constraints would favour the evolution of multimodal signals over simpler signals and found that having multiple receivers or multiple qualities to display would all favour the emergence of multimodal signalling.

Most of the studies on multicomponent signals in the context of courtship displays focus on behavioural responses indicating female preference (Ronald et al., 2017; Taylor & Ryan, 2013), but less has been done on multicomponent courtship where separate components might have different functions (such as sexual stimulation of the female, cf. part 1 above).

3.2.1. Signalling different aspects of male quality

According to sexual selection theory, females choose a male who can increase their reproductive success or the quality of her offspring. In an interesting theoretical paper, van Doorn and Weissing ( 2004) showed that the evolution of multiple male ornaments was plausible if they displayed different aspects of male quality. Although they focussed on ornaments, the same evolutionary process could be involved in the behavioural components of courtship.

Surprisingly, very few studies have focused on the multiple aspects of male quality that courtship could potentially advertise. In some cases, multimodal signals have been found to display different aspects of a male's quality (multiple message hypothesis). Girard et al. ( 2015) found that in peacock spiders ( Maratus volans), different components of courtship, such as vibration vigour and display duration, advertise separate aspects of male quality and differentially predicted mating success. Another example comes from the satin bowerbird, where features of the bower and plumage related to courtship were found to reflect different aspects of male quality (Doucet & Montgomerie, 2003).

3.2.2. Triggering different female responses

There is also evidence that different parts of the male display can trigger differential responses in females. In the iguana Liolaemus pacho for example, chemical signals are thought to have a role in sex recognition (Vicente & Halloy, 2016), while other behaviours like head‐bobbing might have a role in attracting the attention of the receiver and communicating the signaller's location (Vicente & Halloy, 2017). In the sand goby ( Pomatoschistus minutus), the frequency and temporal pattern of sounds are thought to communicate species identity, whereas call intensity and the visual part of male courtship are more relevant for female choice (Pedroso, Barber, Svensson, Fonseca, & Amorim, 2013). In the orb‐web spider, as mentioned above, some of the courtship signals have an influence on female acceptance and probably reduce female aggressiveness (Wignall & Herberstein, 2013), while other signals might facilitate sperm transfer (Huber, 2004). In the lizard Anolis carolinensis, early investigations by Crews ( 1975) on the relative importance of each component of the male courtship display showed that physical movements of the male dewlap during courtship triggered hormonal changes and follicular growth in females, while dewlap colour was used by females for mate choice.

3.2.3. Reaching different receivers

In some cases, multimodal signalling can help the signaller to reach more than one receiver. Female preference has long been considered to be homogeneous within a studied population, as if a consensus had been reached about attractiveness of male attributes. A commonly used approach is therefore to use the mean female response of the population as the response variable. However, it is becoming more and more evident that mate preference varies greatly depending on a female's age, condition or environment (Burley & Foster, 2006; Jennions & Petrie, 1997). Female preference for male colouration can vary according to the level of predation risk (Godin & Briggs, 1996). It is thus likely that female preference for individual courtship components varies within a population. Displaying on different sensory channels, and having more than one information‐containing signal, would potentially allow a male to attract different types of females, thereby dealing with variation in female preferences. In the brown‐headed cowbird ( Molothrus ater), females differ in their preferences for individual components of the complex male courtship display as a function of their sensory acuity (Ronald, Fernández‐Juricic, & Lucas, 2018). In this species, the visual and auditory temporal resolution of females has an influence on which type of visual display and songs they prefer during male courtship, for example females with better auditory temporal resolution preferred shorter songs.

In other cases, some components might be relevant not only in the context of courtship, but also function as signals directed to other males or predators. In the flamboyant lizard ( Sarada superba), different colours of the same display elicit different responses in rival males and courted females, stressing the role of simultaneous selection pressures from intra‐ and inter‐sexual selection in the evolution of multimodal signals (Zambre & Thaker, 2017). In several bird of paradise species, display complexity is also driven by those two forces (Miles & Fuxjager, 2018a, 2018b). Female choice seems to influence sexual dichromatism, while male-male competition is related to carotenoid‐based ornaments. In the peacock ( Pavo cristatus), different signalling ornaments and behaviour have evolved in response to pressure coming from both intra‐ and inter‐sexual selection (Loyau, Saint Jalme, & Sorci, 2005) and in the ochre‐bellied flycatcher ( Mionectes oleaginous), male songs in leks are used both for courtship to females and intra‐sexual competition (Westcott, 1992). The case of co‐option of courtship behaviour from aggressive displays is also quite common in the animal kingdom (Berglund, Bisazza, & Pilastro, 1996). In the ring dove, for example, the bow‐coo display used as an aggressive display towards other males does not differ from the courting display males perform to attract females (Craig, 1909). When the courtship display and the aggressive display are similar, an additional signal component may act as an indicator of intention (Baptista, 1978). For example, in female red‐winged blackbirds ( Agelaius pboeniceus), the visual signals used for courtship and aggressive display by territorial females are similar, while two types of female song have been reported. This suggests that the auditory part of the signal allows a male to disambiguate the female's behaviour (Baptista, 1978; Beletsky, 1983).

3.2.4. Signalling at different geographical and temporal scales

Sometimes, having several courtship components can reduce the cost of mate choice by reducing the time females spend in close inspection of available males. For example, females can use one signal to choose which males are worth observing and then use another signal component for their subsequent choice among this subset of males. In other words, different cues are used for attraction and for mate assessment. Although the sequential assessment of cues to gain information from a conspecific is well documented in general (Uy & Safran, 2013), less evidence exists in the context of mate choice, and even less in the general context of courtship. In the fiddler crab for example, females first select certain males for their size and then assess them for their burrow quality in order to decide which male to mate with (Backwell & Passmore, 1996).

Regarding the specific case of courtship, in the ring‐necked pheasant ( Phasianus colchicus), different messages sent at separate times by males during courtship elicit different responses in females (Mateos & Carranza, 1999). The first signals are used to attract females' attention, whereas the "lateral" display triggers a copulation solicitation display from the female.

At a larger scale, some elements of courtship can attract the potential mate and guide her towards the sender. In the sage grouse ( Centrocercus urophasianus), females use the acoustic component of the display to determine whether to visit a male, but the display rate is a better indicator of the likelihood of mating (Gibson, 1996).

3.3. Information in complex signal structure and component interactions

Partan and Marler ( 1999) were the first to propose a classification of multimodal signals in animal communication. They pointed out that adding a second component to a unimodal signal could modulate the first component's effects on the receiver's behaviour (e.g., enhancement or suppression), or even create a new "emergent" response in the receiver. Their article was an important contribution to multisensory communication theory in the field of animal behaviour, because historically multicomponent signals were studied by analysing each component separately and not by taking the whole signal or the relationship between components into account. More recently, an increasing number of authors have emphasized the need for studying complexity itself, as the different components of a signal are likely to have evolved conjointly (Cooper & Goller, 2004; Groyecka et al., 2017).

Smith and Evans ( 2013) described an interesting heuristic for the study of multicomponent signals. In particular, they proposed a method to better understand and visualize how concomitant variation within and between two modalities influences the receiver's response. The resulting three‐dimensional surface plot (with the magnitude of each component signal represented on two axes and magnitude of female response on the third) was later used by Hebets et al. ( 2016) to study female preference in response to two courtship stimuli, using the multisensory wolf spider courtship display as a model. This type of graphical representation helps to visualize the complexity of a receiver response when exposed to different levels of components inside the same complex display. Here, we use a similar graphical representation to describe how two male courtship components can separately or jointly influence two female responses (Figure ​(Figure1). 1 ). The two‐plane multidimensional plots illustrate a theoretical case where two sensory modalities of male courtship (e.g., a visual and an auditory signal) can interact or not to influence two aspects of female response (e.g., female preference and female sexual stimulation).

One of the first examples of a behavioural response that derives specifically from a multisensory display comes from the study from Rowe and Guilford ( 1996) who investigated multicomponent anti‐predator warning signals found in prey. They found that neither the chemical released by the prey nor the warning colour they display could, when presented alone, trigger aversive behaviour in the domestic chick ( Gallus gallus domesticus) and that the repulsive effect emerged only when the two signals (visual and chemical) were combined. This stresses the importance of taking each component into account, as well as paying attention to the overall structure of the complex signal and the relation between its different components.

In the specific case of courtship, most of the studies reporting an interaction between signals do not directly concern interactions between different behavioural components of courtship, but rather the relative role of courtship behaviour and morphological traits (Reynolds, Gross, & Coombs, 1993). See Table ​Table2 2 for an overview of studies investigating multiple courtship components.

Table 2

Term

Definition

Example

References

Multicomponent courtship

Courtship with two or more distinct signals occurring in a single sensory modality

The vocal courtship of the túngara frog composed of whines and chucks

Partan and Marler ( 2005); Rowe ( 1999); Stange et al. ( 2016)

Multimodal/multisensory courtship

Courtship comprising two or more signals occurring in at least two different sensory modalities

The bowing display of a ring dove, including a visual signal (the bow) and the bow call

Partan and Marler ( 2005); Rowe ( 1999); Fusani, Hutchison, and Hutchison ( 1997)

Complex courtship

Courtship composed of multiple signalling elements, in one or more sensory modalities

The acrobatic dance of a manakin, jumping in a courtship arena while displaying brilliant plumage and snapping its wings

Fusani, Giordano, Day, and Schlinger ( 2007); Hebets and Papaj ( 2005);Miles and Fuxjager ( 2018a, 2018b); Perrot et al. ( 2016)

Female sexual stimulation

Physiological changes occurring in females following male courtship

Courtship‐induced follicular growth in ring doves

Friedman ( 1977)

3.3.1. Multisignalling as a marker of quality per se

Independently of its content, multicomponent signalling can intrinsically be a sign of the quality of the displaying individual. Indeed, complex courtship displays are often more energetically costly than single‐component displays and could therefore be under female selection for energetically demanding behaviour (Byers, Hebets, & Podos, 2010). For example, in Drosophilia virilis, courtship elicits a response from a female only if all elements of a sequence of signals are present. This might be a way for females to select those males that are able to send accurately timed and energetically costly signals (LaRue, Clemens, Berman, & Murthy, 2015). In the wolf spider ( Schizocosa ocreata), females prefer multimodal courtship signals over unimodal ones (Stoffer & Uetz, 2017). Additionally, in peacock spiders ( Maratus volans), Girard et al. ( 2015) found that total courtship effort (a variable capturing the time a male spends courting across different sensory modalities) positively affected female preference. We know that in some species, courtship is costly and condition dependent. In the fiddler crab ( Austruca lactea) for example, males produce a multisensory courtship display to attract females from a distance and then to court them when closer. Takeshita, Murai, Matsumasa, and Henmi ( 2018) showed that the male visual waving signal used to attract females was condition dependent and therefore could be used by females to assess the individual quality of potential partners.

In addition, the timing of different components of courtship does not occur randomly. Signal synchronization could itself indicate good neural control. In the Montezuma oropendolas ( Psarocolius montezuma), males synchronize the loudest note of their song with a specific visual courtship display (the bow and wing‐spread), which could indicate the quality of an individual motor's skills (Miles & Fuxjager, 2018a, 2018b). In the brush‐legged wolf spider ( Schizocosa ocreata), accuracy in the temporal synchrony of separate courtship signals increases female receptivity (Kozak & Uetz, 2016). In Túngara frogs ( Physalaemus pustulosus), females reject the courtship when the multimodal elements of the mating signal lack synchrony (Taylor, Klein, Stein, & Ryan, 2011). In the same species, synchronized visual and acoustic displays are more attractive to females than asynchronous signals (Taylor, Page, Klein, Ryan, & Hunter, 2017). However, an asynchronous multimodal signal is still more attractive than a unimodal signal. This underlines the complex relationship that can exist between all sensory modalities contributing to a signal and the information contained in their interactions and their relative timing.

3.3.2. Multimodal courtship displays are more than the sum of their parts

When we consider the response to a complex signal that involves several sensory modalities, we now realize that this response is not always additive. Experiments investigating multisensory integration in the midbrain have found clear evidence for super‐additive multisensory enhancement when comparing single neurons' responses to uni‐ and multimodal stimuli (Meredith & Stein, 1983). Multisensory responses have also been found in cells located in cortical areas of the rodent brain which were traditionally assumed to be entirely modality specific (Wallace, Ramachandran, & Stein, 2004). This may explain how a signal in one modality can influence the processing and perception of a signal in another modality. However, as only a few examples have been documented so far, it is not yet clear whether such cross‐modal effects are exploited in courtship displays.

A study on mate choice in Túngara frogs showed that two courtship signals which are not attractive individually, that is the two parts of the vocal signal, become attractive for the females when combined with a visual signal (the inflation of the vocal sac) (Taylor & Ryan, 2013). The multimodal integration of signals by females is therefore not additive but rather involves a complex emergence. In another recent paper on Túngara frogs, Stange et al. ( 2016) tried to assess the relative importance of each part of a multicomponent signal by manipulating the complexity of the courtship display. They found that female integration of the multicomponent male signal was not additive and that the preference varied with display complexity, that is with the number of components of the signal. This suggests the presence of some higher‐order interaction between the visual and acoustic components of the courtship that goes beyond a simple enhancement effect. Finally, in the brown‐headed cowbird ( Molothrus ater), the intensity of the visual component of male courtship modulates the attractiveness of male songs (Ronald et al., 2017). This study is an interesting example where two components of male courtship interact in a complex way to modify overall attractiveness. Examples of this kind are still scarce, but there is no doubt that the growing interest in multimodal signalling displays will allow more research to reveal similar interactions in the courtship displays of other species.

4. CONCLUSION

Over the past years, many authors have proposed new theoretical backgrounds for the study of the role and function of multimodal displays (Bro‐Jørgensen, 2010; Candolin, 2003; Partan, 2013; Rowe & Halpin, 2013). Even though courtship displays typically involve signals coming from more than one sensory modality, relatively little theoretical and experimental work exists on multimodal and multicomponent courtship displays, and most of the work so far has focused on auditory or visual courtship. Empirical studies are now needed to specifically test how the variation in different modalities and the interaction between them influence female response and choice in the context of courtship. In addition, we know very little about the neural mechanisms involved in multisensory processing in the courtship context. As mentioned above, uni‐sensory information from different sensory channels is integrated and transformed into multisensory responses in the midbrain (e.g., Gandhi & Katnani, 2011; Meredith & Stein, 1986) and cross‐modal stimuli yield faster responses and can be detected with higher accuracy than modality‐specific stimulus presentations (Gingras, Rowland, & Stein, 2009). Whether these neural and behavioural principles of multi‐sensory enhancement also hold in the context of multimodal courtship displays remains to be investigated.

Finally, courtship is often an interactive process between two sexes rather than the production of signals by a courting individual and its evaluation by a receiver. In a number of dynamic courtship interactions, the emitter modifies its signals on the basis of the response of the receiver. Therefore, many types of multimodal courtship can be fully understood only by analysing their variation across time and in response to signals coming from the receiver. This is a further level of complexity that we have only started to explore.

ACKNOWLEDGEMENTS

This work was supported by Leonida Fusani's Startup funding of the University of Vienna, Austria and by the Austrian Science Fund (FWF): W1262‐B29. We thank Walter Hödl for his useful comments on the manuscript.

Notes

Mitoyen C, Quigley C, Fusani L. Evolution and function of multimodal courtship displays. Ethology. 2019;125:503-515. 10.1111/eth.12882 [[ CrossRef] Google Scholar]

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# data[].attributes.attachment_link.title
Evolution and function of multimodal courtship displays

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Ethology. 2019 Aug; 125(8): 503-515. Section Editor: Redouan Bshary Courtship displays are behaviours aimed to facilitate attraction and mating with the opposite sex and are very common across the animal kingdom. Most courtship displays are multimodal, meaning that they are composed of concomitant signals occurring in different sensory modalities.

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Mating displays also tend to share a variety of characteristics such as: Competition/Aggression, Scent Signals, Ritualized Behaviors, Vocalizations, and Visual Displays.

In the case of Competition/Aggression, individuals of the same sex may showcase acts of aggression such as contests and combat in order to establish dominance and show the potential mating partner that they are a compatible match compared to the other organisms interested.

When scent signals are involved, some animals may release chemical signals or pheromones to cue their availability for mating.

Ritualized Behaviors often consist of acts such as: synchronized movements and dancing. Birds species often perform aerial displays or perform complex dances of courtship on the ground.

Vocal displays stem from complex calls and songs that animals create in order to attract mates or to send out specific messages indicating defense and hostility to those who want to challenge their state of courtship.

Visual Displays involve patterns, vibrant colors, and exaggerated body structures and often include colorful bird feathers, fish scales, or antler displays.

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These organisms have a long mating season that often occur in the months of April to November.

Their courtship process begins when a male and female turtle face one another and progressively move their heads from side to side.

Females in this case do not have to mate every year as she is able to store sperm inside of her body.

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In order to signal that she is ready for breeding, a female bobcat will begin to rub her body along a tree whilst spreading her urine around the nearby area.

Once she is approached by a male, they will begin to chase and wrestle one another.

This breeding behavior will then proceed to continue for over two weeks, resulting in the male leaving while the female is tasked with raising the young.

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Examples of Animal Courtship Behaviors Source 

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Examples of Animal Courtship Behaviors Source 

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1. Prairie voles
Prairie voles are almost the epitome of a happy, healthy animal relationship. The creatures, about the size of a hamster, only live one-two years, but they are monogamous during that time. Once they meet a member of the opposite sex, pheromones help them to ready for mating. After mating, they show love by huddling together and even have been seen breathing in unison, and studies have even shown they give "hugs and kisses" when one's partner is stressed.
Prairie voles are popular prey for snakes, hawks and the like, but about 80 percent of voles that lose a partner do not find another.
(10 animals you didn't know mated for life)

2. White-tailed deer
White-tailed deer are polygamous, meaning they mate with more than one deer of the opposite sex, don't build family units and don't bond.
Breeding season is called rut (learn more about that here), and it is centralized on scent. A buck will find a doe that is ready to breed and will stay with her for several hours or even days. Sometimes females will make a buck chase her before she will agree to mate.

3. Cottontail rabbits
Cottontail rabbits are also polygamous, and their courtships can be quite obvious to those that are paying attention. Prior to mating, males and females will "cavort," which includes running, racing, hopping or even fighting. Some scientists think these athletics are so the rabbits prove to each other that they are healthy and strong.

4. Trumpeter swan courtship rituals look like couples bowing to each other before a dance at a fancy ball. Swans select a life mate about two-four years old, and they will swim together, head bob, blow in the water and sing during this courtship time.

Trumpeter swans may not nest after courtship but can spend a couple of years together before the first attempt at procreation.

5. Osprey are almost always monogamous, although they will replace a partner if one gets sick or can't reproduce anymore. When courting at the nest site, a male will dangle his legs with a fish or nesting material in his talons and will fly overhead while calling and circling back to the nest.
During courtship, males will also feed females, and she will ask for food through her body movements --- holding her body horizontally, puffing up her crest feathers and keeping her wings close to her body. Courtship feeding doesn't occur at the same time as procreation though.

6. Coyotes
Coyotes are seasonally monogamous, and pairs may stay together longer than a year. Pairs may show courtship behaviors such as grooming each other, playing and wrestling, chasing each other or bumping and hip pushing each other. They will also sniff and lick each other, and a female may even position herself in front of her partner to tell him she's ready.

7. Great-horned owls
Male great-horned owls begin searching for a mate early in the year by calling, swelling their chests and bowing to females. An attracted female will respond by returning bowing and hooting, and then a mated pair may stay together for years or even the rest of their lives.

8. A female bobcat will let males know she is ready to breed by rubbing her body on trees and spreading urine. She may even call loudly so that males can find her. (9 adorable Iowa mammals)
Once a male approaches an agreeable female, she will begin vocalizing, will arch her back and circle around the male, and then they will wrestle and chase each other. This behavior and breeding may continue for more than two weeks, and then the male leaves and the female raises the young.

9. Northern leopard frogs
Northern leopard frogs emerge from hibernation early and begin breeding rituals right away. A male will find a breeding location, far from other males, and will begin making long, snore-like sounds to call in a female. She will swim in the water, and the male with hang onto her back for two-three days. When she releases eggs, he will fertilize them in the water.

10. Snapping turtles have a long mating season, actively breeding April-November. A pair will begin courtship by facing each other and moving their heads from side to side.
A female doesn't have to mate every year. She can store sperm in her body to fertilize eggs even in years when she doesn't mate.

(Download free, printable Valentine's Day cards)

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Prairie voles Prairie voles are almost the epitome of a happy, healthy animal relationship. The creatures, about the size of a hamster, only live one-two years, but they are monogamous during that time. Once they meet a member of the opposite sex, pheromones help them to ready for mating.

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These courtship processes often depict couples bowing at one another prior to a dance.

Their life mate selections are normally around 2 to 4 years old.

During this courtship time, the two swans will sing, blow in the water, swim, and head bob.