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(1) Shubin, N. (2009). Your inner fish: A journey into the 3.5-Billion-Year History of the Human Body. Vintage.
(2) V. Makarenkov, D. Kevorkov, P. Legendre. Phylogenetic network construction approaches. Applied Mycology and Biotechnology, 6 (2006), pp. 61-97, 10.1016/S1874-5334(06)80006-7
(3) Graham A. Developmental homoplasy: convergence in cellular differentiation. J Anat. 2010 Jun;216(6):651-5. doi: 10.1111/j.1469-7580.2010.01232.x. Epub 2010 Mar 30. PMID: 20374410; PMCID: PMC2952378.
(4) Homologous Structures https://bio.libretexts.org/@go/page/13468 (accessed Apr 6, 2023).
(5) Aqua. (2019). Hoatzin Birds: the Strangest Bird in the Amazon. https://www.aquaexpeditions.com/blog/amazon/hoatzin-bird-amazon
(6) Warren W, et al. Genome analysis of the platypus reveals unique signatures of evolution. Nature 453, 175–183 (2008). https://doi.org/10.1038/nature06936
(7) Tiwari A, Gautam D, Kulkarni PP, et al. Noncanonical Sonic Hedgehog signaling amplifies platelet reactivity and thrombogenicity. Blood Adv. 2022;6(17):5024-5040. doi:10.1182/bloodadvances.2021006560
(8) Zimmer, C. (2012). Turning Fins Into Hands. Nat Geo.
https://www.nationalgeographic.com/science/article/turning-fins-into-hands
(9) Klump, L. R. (2003). The Geochemistry of Mass Extinction. Treatise on Geochemistry, Volume 7. Editor: Fred T. Mackenzie. Executive Editors: Heinrich D. Holland and Karl K. Turekian. pp. 407. ISBN 0-08-043751-6. Elsevier, 2003., p.351-367. doi:10.1016/B0-08-043751-6/07101-2
(10) Howell, C. (2011). Archaeopteryx - the missing link between dinosaurs and birds? Wales Museum. https://museum.wales/articles/1011/Archaeopteryx---the-missing-link-between-dinosaurs-and-birds/#:~:text=Archaeopteryx%20is%20an%20iconic%20fossil,and%20their%20links%20with%20dinosaurs
(11) Guardian News and Media. (2022, December 31). Out of Africa: My lifelong mission to trace the origins of humanity. The Guardian. https://www.theguardian.com/focus/2022/dec/31/chris-stringer-origins-of-man-lifelong-mission
(12) Oldest bilaterian fossil found in Australia | paleontology | sci-news.com. (n.d.). Retrieved April 6, 2023, from https://www.sci.news/paleontology/ikaria-wariootia-08254.html

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Homologous structures are features in organisms that share common ancestors that are similar in physical structures but do not share similar functionality. A clear example of this is limbs in humans, canines, crustaceans, and bats. (4)

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Homoplasy is the development of organs or other bodily structures within different species that tend to resemble one another and have similar functions, but do not have common origins through ancestry. (2)
Supplementary Information:
https://www.sciencedirect.com/topics/biochemistry-genetics-and-molecular-biology/homoplasy#:~:text=Homoplasy%20is%20the%20development%20of,not%20homologous%20to%20each%20other.

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Palaeontology is an essential practice to fully understand the history of humans. This is due to the resulting discovery of fossils that is facilitated by this practice, showing animals never seen before, and providing the only direct, physical evidence towards the history of evolution to go along with genome sequencing.

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Image of the possible impact of the asteroid received from Britannica, The Editors of Encyclopaedia. "K–T extinction". Encyclopedia Britannica, 5 Sep. 2022.

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Extinction, although generally frowned upon is the fate of all species, occurring at normal rates, or by 'mass extinction' events.
Paleontology was essential in understanding how the KT mass extinction event may have happened.
The KT extinction, according to the leading theory, was due to a large asteroid hitting the earth, this is supported by many different findings including:
a) iridium abundance near the KT boundary
b) Shocked quartz abundant at the boundary
c)Microkektites also being abundant at the boundary.
These are paleontological findings that help us to understand what causes mass extinctions. (9)
More Information:
https://ui.adsabs.harvard.edu/abs/2003TrGeo...7..351K/abstract

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Introducing the Concept of One’s “Inner Fish”

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Introducing the Concept of One’s “Inner Fish”

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(1) Shubin writes “How can a walk through the zoo help us predict where we should look in the rocks to find important fossils? A zoo offers a great variety of creatures that are all distinct in many ways. But let's not focus on what makes them distinct; to pull off our prediction, we need to focus on what different creatures share. We can then use the features common to all species to identify groups of creatures with similar traits.”

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“The theory of evolution is quite rightly called the greatest unifying theory in biology.”
-Ernst Mayr
This is a quote that still rings true today, evolution seems to have been the missing piece that allowed an understanding of many fields of biology. This is important as the book 'Your Inner Fish' integrates evolution and biology with paleontology, displaying the importance of the field on science overall.

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Fossils found within limestone from USA Government (Public Domain)

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Using palaeontology it is possible to pinpoint locations that would likely hold fossils of the organism that is an specific area of interest for study. Using the same ideas, palaeontologists can also conclude what types of rocks and sedimentary materials would be likely to contain fossils. Shubin writes that he specifically searches for “sedimentary rocks: limestones, sandstones, silt-stones, and shales” (17). These fossils can and do help support the ideas of common ancestors, as we can see similarities between these fossilized organisms and multiple modern organisms. (1)

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Why is Homoplasy Important When Describing Evolution?

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Why is Homoplasy Important When Describing Evolution?

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Acknowledgement of homoplasy helps to explain potential inconsistencies with the taxonomy of some species. Additionally, it helps to support the idea of adaptations by showing two different lineages that produce the same or similar structures seperately.

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Archaeopteryx specimen - Museum für Naturkunde, Berlin, Germany

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A Historic Context: Proof of Evolution VIA Paleobiology

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A Historic Context: Proof of Evolution VIA Paleobiology

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The concept of evolution was refuted for a long time due to words from the Holy Bible. Many people argued things such as “if species adapted how come we have never seen a transition state”. This argument was rendered moot in 1861 when Hermann von Meyer discovered the first Archaeopteryx fossil in limestone, proving a transitional state between birds and reptiles, as well as solidifying evolution into modern science. (10)
More information:
https://museum.wales/articles/1011/Archaeopteryx---the-missing-link-between-dinosaurs-and-birds/#:~:text=Archaeopteryx%20is%20an%20iconic%20fossil,and%20their%20links%20with%20dinosaurs.

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(1) Shubin writes “Like a concerto composed on individual notes played by many instruments, our bodies are a composition of individual genes turning on and off inside each cell during our development” (Pg. 46), this is a beautiful simile that paints a picture in our heads that shows how intricate our bodies development is. Painting DNA as the composers it shows how  important it is that every cell has the right instructions.

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Hoatzins are a very important specimen for the understanding of evolution as they act as a transitional species between reptiles and birds, whilst leaning more towards modern birds as opposed to archaeopteryx. Their young have claws like reptiles and archaeopteryx but as they age they lose their reptile-like feature and become even more bird-like. (5)
More information on hoatzins:
https://www.aquaexpeditions.com/blog/amazon/hoatzin-bird-amazon/

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Figure 1: Emergence of traits along the mammalian lineage. From Warren et al. "Genome analysis of the platypus reveals unique signatures of evolution".

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A Link Between Reptiles and Mammals: the Platypus

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A Link Between Reptiles and Mammals: the Platypus

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The Duck-Billed Platypus (Ornithorhynchus anatinus) is one of the few 'transitional species' that is able to be observed in the modern world. The platypus, like reptiles, lays eggs and has webbed feet as well as a characteristic toxic spur, which is very uncharacteristic of mammals. However, the platypus also possesses hair and mammary glands, which are essential in the identification of mammals. These features, as well as genetic features, suggest that reptiles evolved into mammals at one point in the past. (6)
More information on Platypuses:
https://www.nature.com/articles/nature06936

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Amniotes split into the sauropsids (leading to birds and reptiles) and synapsids (leading to mammal-like reptiles). These small early mammals developed hair, homeothermy and lactation (red lines). Monotremes diverged from the therian mammal lineage ∼166 Myr ago and developed a unique suite of characters (dark-red text). Therian mammals with common characters split into marsupials and eutherians around 148 Myr ago (dark-red text). Geological eras and periods with relative times (Myr ago) are indicated on the left. Mammal lineages are in red; diapsid reptiles, shown as archosaurs (birds, crocodilians and dinosaurs), are in blue; and lepidosaurs (snakes, lizards and relatives) are in green.

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Figure 1: Emergence of traits along the mammalian lineage.

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Amniotes split into the sauropsids (leading to birds and reptiles) and synapsids (leading to mammal-like reptiles). These small early mammals developed hair, homeothermy and lactation (red lines). Monotremes diverged from the therian mammal lineage ∼166 Myr ago and developed a unique suite of characters (dark-red text).

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From Hall, T.M., Porter, J.A., Beachy, P.A., Leahy, D.J. A potential catalytic site revealed by the 1.7-A crystal structure of the amino-terminal signalling domain of hedgehog protein.

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Through research on flies scientists Andy Macmahon, Phil Ingham, and Tabin discovered the ‘hedgehog’ gene that codes one side of the fly to be different than the other. Knowing the makeup and look of this gene they were able to identify similar genes in chickens they called a ‘Sonic hedgehog’. Being able to experiment, they located a Sonic hedgehog gene and concluded that every limbed animal has one. This is strong evidence of animals being related as it is responsible for the CNS, limbs, digits and many other parts of the body development in all animals. (7)
More information on the hedgehog gene:
https://pubmed.ncbi.nlm.nih.gov/35704688/

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From Zimmer and Emlen, Evolution: Making Sense of Life (Robert Publishing)

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Looking at the physiological comparisons of human and the transitional animals from water to land like Tiktaalik roseae, we can see that they also have structures in their limbs similar to ours like humerus, radius, and ulna. As the progression went on you can see the development of these bones progressing, which would eventually progress into limbs as we see them today. (8)
More information:
https://www.nationalgeographic.com/science/article/turning-fins-into-hands

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Rendition of the transitional-animal Tiktaalik roeae

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The Discovery of the Tiktaalik roseae Fossil

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The Discovery of the Tiktaalik roseae Fossil

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With the unearthing and discovery of Tiktaalik roseae, a transitional-fossil that shows the change from aquatic to land-roaming animals we are able to support the idea of evolution. Evolution as a process is done in step-by-step processes such as that of natural selection. Tiktaalik roseae is a golden example of an animal that displays the change over time definitive of evolution, such that is on the way to being land-roaming but is still aquatic. (1)

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On December 31st 2022, Chris Stringer made news headlines with his work on finding the origins of human life. He reported that he had data that supports the spreading out from Africa, and therefore the evolution of the human race originating in one singular spot. This is substantial as it backs the theory of evolution, and therefore helps us to further understand our “inner fish”. (11)
Linked Here: https://www.theguardian.com/focus/2022/dec/31/chris-stringer-origins-of-man-lifelong-mission

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For Supplemental Instruction on Homologous Structures

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For Supplemental Instruction on Homologous Structures

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(4) https://bio.libretexts.org/Bookshelves/Introductory_and_General_Biology/Book%3A_General_Biology_(Boundless)/18%3A_Evolution_and_the_Origin_of_Species/18.05%3A_Evidence_of_Evolution/18.5F%3A_Homologous_Structures

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Homologous structures are similar structures that evolved from a common ancestor.

Learning Objectives

Describe the connection between evolution and the appearance of homologous structures

Key Points

Homology is a relationship defined between structures or DNA derived from a common ancestor and illustrates descent from a common ancestor.

Analogous structures are physically (but not genetically) similar structures that were not present the last common ancestor.

Homology can also be partial; new structures can evolve through the combination or parts of developmental pathways.

Analogy may also be referred to as homoplasy, which is further divided into parallelism, reversal, and convergence.

Key Terms

homology: A correspondence of structures in two life forms with a common evolutionary origin, such as flippers and hands.

analogy: The relationship between characteristics that are apparently similar but did not develop from the same structure

homoplasy: A correspondence between the parts or organs of different species acquired as the result of parallel evolution or convergence.

Homologous Structures

Homology is the relationship between structures or DNA derived from the most recent common ancestor. A common example of homologous structures in evolutionary biology are the wings of bats and the arms of primates. Although these two structures do not look similar or have the same function, genetically, they come from the same structure of the last common ancestor. Homologous traits of organisms are therefore explained by descent from a common ancestor.

It's important to note that defining two structures as homologous depends on what ancestor is being described as the common ancestor. If we go all the way back to the beginning of life, all structures are homologous!

Figure \(\PageIndex{1}\): Homology in the forelimbs of vertebrates: The principle of homology illustrated by the adaptive radiation of the forelimb of mammals. All conform to the basic pentadactyl pattern but are modified for different usages. The third metacarpal is shaded throughout; the shoulder is crossed-hatched.

In genetics, homology is measured by comparing protein or DNA sequences. Homologous gene sequences share a high similarity, supporting the hypothesis that they share a common ancestor.

Homology can also be partial: new structures can evolve through the combination of developmental pathways or parts of them. As a result, hybrid or mosaic structures can evolve that exhibit partial homologies. For example, certain compound leaves of flowering plants are partially homologous both to leaves and shoots because they combine some traits of leaves and some of shoots.

Paralogous Structures

Homologous sequences are considered paralogous if they were separated by a gene duplication event; if a gene in an organism is duplicated to occupy two different positions in the same genome, then the two copies are paralogous.

A set of sequences that are paralogous are called paralogs of each other. Paralogs typically have the same or similar function, but sometimes do not. It is considered that due to lack of the original selective pressure upon one copy of the duplicated gene, this copy is free to mutate and acquire new functions.

Figure \(\PageIndex{1}\): Homology vs. analogy: The wings of pterosaurs (1), bats (2), and birds (3) are analogous as wings, but homologous as forelimbs. This is because they are similar characteristically and even functionally, but evolved from different ancestral roots.

Paralogous genes often belong to the same species, but not always. For example, the hemoglobin gene of humans and the myoglobin gene of chimpanzees are considered paralogs. This is a common problem in bioinformatics; when genomes of different species have been sequenced and homologous genes have been found, one can not immediately conclude that these genes have the same or similar function, as they could be paralogs whose function has diverged.

Analogous Structures

The opposite of homologous structures are analogous structures, which are physically similar structures between two taxa that evolved separately (rather than being present in the last common ancestor). Bat wings and bird wings evolved independently and are considered analogous structures. Genetically, a bat wing and a bird wing have very little in common; the last common ancestor of bats and birds did not have wings like either bats or birds. Wings evolved independently in each lineage after diverging from ancestors with forelimbs that were not used as wings (terrestrial mammals and theropod dinosaurs, respectively).

It is important to distinguish between different hierarchical levels of homology in order to make informative biological comparisons. In the above example, the bird and bat wings are analogous as wings, but homologous as forelimbs because the organ served as a forearm (not a wing) in the last common ancestor of tetrapods.

Analogy is different than homology. Although analogous characteristics are superficially similar, they are not homologous because they are phylogenetically independent. The wings of a maple seed and the wings of an albatross are analogous but not homologous (they both allow the organism to travel on the wind, but they didn't both develop from the same structure). Analogy is commonly also referred to as homoplasy.

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Homologous structures are similar structures that evolved from a common ancestor. Learning Objectives Describe the connection between evolution and the appearance of homologous structures Homology is a relationship defined between structures or DNA derived from a common ancestor and illustrates descent from a common ancestor.

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The wings of birds and bats respectively received from Vladimir Makarenkov et al. "Applied Mycology and Biotechnology".

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Flight is a very clear example of homoplasy in biology. The wings of bats and the wings of birds evolved independently, birds from archosaurs, and bats from eutherian mammals. They both use flight very similarly and yet according to the fossil record they come from radically different lineages. (2)

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A rendition of what Ikaria wariootia might have looked like

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Oldest Bilaterian Fossil Found in Australia 

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Oldest Bilaterian Fossil Found in Australia 

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In March of 2020, the University of California’s Scott Evans led a research team that discovered a fossil for Ikaria wariootia, a worm-like organism that lived in the area that is now Australia more than 555 mya. This is the earliest known bilateral animal. This is interesting as evolutionary biologists speculated holes in this area were likely made by some ancient ancestor of worms as we know them today, but this discovery conformed this. One researcher, Professor Droser was even quoted to say “It’s really exciting that what we have found lines up so neatly with their prediction”
This shows that other bilateral animals likely evolved from this species or ones similar. (12)
Article can be found here: https://www.sci.news/paleontology/ikaria-wariootia-08254.html

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For Supplemental Instruction on Homoplasy

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For Supplemental Instruction on Homoplasy

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(3) https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2952378/#:~:text=The%20existence%20of%20the%20phenomenon,disease%20state%20and%20disease%20repair.

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Abstract

There is an accumulating body of evidence that highlights the fact that one can identify convergence in programmes of cellular differentiation. That is, that a particular differentiated cell/tissue type can be generated via non-identical paths. Convergence is also seen in evolution and here it is termed homoplasy, thus one could term convergence in cellular differentiation, developmental homoplasy. It is important to appreciate its existence as it can confound our understanding of cellular differentiation. In particular, it highlights the point that the analysis of cellular differentiation in one region of the body may not generate an understanding that is generally applicable. The existence of the phenomenon of developmental homoplasy may lie in the evolutionary history of developmental processes, which are assembled over phylogenetic time. Such convergence in cellular differentiation may also have significance for understanding disease state and disease repair.

Keywords: cellular differentiation, convergence, dermis, evolution, muscle, sensory neurons, skeleton, smooth muscle

Introduction

Homoplasy describes the emergence of similarities that arise as a result of convergence during evolution ( Lankester, 1870). A classic example of homoplasy would be the wings of birds and the wings of bats ( Fig. 1A ). Although both these groups of animals possess wings that allow them to fly, their wings have evolved independently. The most recent common ancestor of birds and bats did not possess wings. Thus the modification to the development of the forelimbs that gave rise to the wings of birds occurred independently from that which generated bat wings. A number of lines of evidence would seem to suggest that homoplasy can also be detected in programmes of cellular differentiation. Thus, there is an increasing body of work on a number of diverse tissues that suggests there is convergence in processes of cellular differentiation. It has been shown that many of the differentiated cell types that are found in vertebrates do not emerge from a single precursor population but that they can have dual or multiple origins ( Fig. 1B ). Furthermore, it is also becoming apparent that molecular details of the paths of differentiation can also vary between different regions of the body.

Skeletogenesis

Skeletal tissues provide the body with its framework and underpin its morphology. It has been apparent, however, that there are differences in the routes through which bone and cartilage are generated. In the trunk, the skeleton has a mesodermal origin. The axial skeleton emerges from the somites and the appendicular skeleton from the lateral plate mesoderm, and most bones are formed by endochondral ossification via a cartilaginous template. Contrastingly, in the head, much of the skeletal tissue derives from neural crest cells ( Le Douarin & Kalcheim, 1999). These are a transient multipotent embryonic progenitor population that migrates from the neural tube early in development. It is also important to note that in the head, whereas some bones are formed by endochondral ossification, others, the dermal bones, arise by direct differentiation of the neural crest cells into osteoblasts. Thus the chondrocytes and osteocytes of the trunk and head have very different developmental histories and bone can be formed via distinct paths. Yet, even when the neural crest and mesodermal precursor populations differentiate to form the same skeletal tissue, endochondral bone, differences are also apparent. Mice with a targeted mutation in Indian Hedgehog (IHH) have severely reduced endochondrally derived trunk bones, yet endochondrally derived cranial bones, such as the basioccipital and basisphenoid, are largely unaffected in these animals ( Abzhanov et al., 2007). This would seem to suggest that the endochondral bones of the head have a differential requirement for IHH from those in the trunk.

Sensory neuronal differentiation

Another very clear example of convergence in cellular differentiation can be found in the generation of sensory neurons. The neurons of the dorsal root ganglia (DRGs) of the trunk and of the trigeminal ganglion of the head perform similar functions; both are concerned with relaying general somatosensory information from the periphery to the central nervous system, but they have distinct developmental histories. All of the neurons of the DRGs are neural crest-derived. The neural crest cells emerge from the dorsal neural tube and then migrate into the anterior half of each somite, wherein they subsequently differentiate as post-mitotic neurons. This developmental programme involves an increasingly well-defined cascade of transcription factors ( Marmigere & Ernfors, 2007). The development of the trigeminal ganglion is somewhat more complex ( Fig. 2 ). The first neurons to contribute to the trigeminal ganglion are not neural crest-derived but arise from focal thickening of the ectoderm, termed neurogenic placodes. There are two trigeminal placodes, the ophthalmic and the maxillomandibular, which lie alongside the midbrain hindbrain junction and are dependent on inductive signals from this region of the CNS for their formation ( Canning et al., 2008). The formation of the placodes does not require the transcription factors that drive neural crest formation and the delamination of cells from the placodes is quite distinct from neural crest delamination ( Graham et al., 2007). The trigeminal placodes also differ from each other both in terms of the transcription factors that they express and in the cellular behaviour of the neuronal cells they release. In the ophthalmic placode, post-mitotic neurons differentiate and express sensory neuronal transcription factors within the ectoderm prior to their migration to the site of ganglion formation ( Begbie et al., 2002). Contrastingly, the maxillomandibular placodes release mitotically active neuroblasts that migrate from the ectoderm to the site of ganglion formation before differentiating. Thus there are significant differences in the ways in which the progenitors for the sensory neurons of the DRGs and the trigeminal ganglion are generated and most probably in the cues that direct their terminal differentiation.

There are, however, similarities in the signalling pathways used in the generation of neurons in the DRGs and the trigeminal ganglion. Proprioceptive neurons relay information about the movement and position of body parts. The proprioceptive neurons that innervate the limbs reside in the DRGs and these cells have been shown to require the transcription factor Runx3 and NT3/TrkC signalling ( Marmigere & Ernfors, 2007). Runx3 expression has been detected in the neurons of the trigeminal ganglion, and in Runx3 mutants it has been reported that there is a loss of TrkC expressing neurons here, suggesting similarities in the developmental path leading to the formation proprioceptive sensory neurons in DRGs and trigeminal ganglion sensory neurons ( Levanon et al., 2002). Yet, there are no proprioceptive sensory neurons in the trigeminal ganglion; they are somatosensory. The proprioceptive neurons that contribute to the trigeminal nerve reside in the CNS; these are the cells of the mesencephalic trigeminal nucleus, and these are not exclusively dependent upon TrkC signalling for their formation ( Fan et al., 2000) ( Fig. 2 ). Thus the pathway that promotes the differentiation of proprioceptive sensory neurons in the trunk affects the development of a different class of sensory neurons in the trigeminal ganglion.

Skeletal muscle development

A more recent example of developmental homoplasy has emerged from studies of skeletal muscle development. It has been shown that trunk and cranial muscles derive from separate genetic lineages ( Harel et al., 2009). In the trunk, skeletal muscle cells arise from the somites and they can be genetically labelled through their expression of Pax3. The cranial musculature does not derive from somites but from the unsegmented cranial paraxial mesoderm and the precursors of the cranial skeletal muscles do not express Pax3. They can, however, be genetically labelled via their expression of a different transcription factor, Mesp1. It has also been shown that aspects of the myogenic programme differ between head and trunk muscle. In the trunk, it is known that Pax3 acts in a pathway parallel to Myf5 and Mrf4 and will rescue MyoD-mediated myogenesis in the absence of these two transcription factors ( Tajbakhsh et al., 1997). Yet, in the head, myogenesis will ensue in Pax3: Myf5(Mrf4) mutants. Instead, Tbx1 function is required for myogenesis in pharyngeal arch muscles in the absence of Myf5, which again highlights to existence of convergence in developmental processes ( Sambasivan et al., 2009). The neurons that innervate the pharyngeal muscle reside in the hindbrain, and it is important to recognize that these motor neurons can be uniquely defined through their expression of the transcription factors Phox2b and Tbx20, and are thus distinct from spinal motor neurons ( Dufour et al., 2006).

Dermis formation

Although these previous examples have focussed on differences between the head and trunk, examples of developmental homoplasy can be found exclusively within the trunk. In particular, it has been shown that the dorsal and ventral dermis of the trunk arises from distinct progenitor populations ( Mauger, 1972). Thus, while the dorsal dermis originates from the somites, the ventral dermis is generated by the lateral plate mesoderm. The dorsal and ventral dermis also differ in their requirement for wnt signalling during development. In both dorsal and ventral dermis, β-catenin is required for cell fate selection, but in the ventral dermis, β-catenin is additionally required for progenitor cell survival ( Ohtola et al., 2008).

Vascular smooth muscle differentiation

Perhaps one of the most striking examples of convergence in cellular differentiation is that associated with the generation of vascular smooth muscle cells. These cells originate from an incredibly broad range of embryonic tissues, including, the neural crest, the secondary heart field, the somites, the splanchnic mesoderm and the mesothelium ( Majesky, 2007). Significantly, it has been found that different blood vessels, and indeed different segments of the same vessel, such as the aorta, are composed of smooth muscle cells generated by distinct progenitors. The complexities in the origins of the vascular smooth muscle cells are reflected in aspects of their differentiation. Thus, although it has been shown that all smooth muscle cells express the smooth muscle myosin heavy chain (SM-MHC) gene, dissection of the regulatory apparatus of this gene has revealed the existence of distinct elements that are required for the expression of this gene in different smooth muscle cell populations ( Manabe & Owens, 2001).

The evolutionary origin of developmental homoplasy

Having established that there are a number of examples of developmental homoplasy associated with multiple tissue types, it is crucial to consider why they are present. The answer to this most probably lies in the complexity of the evolutionary history of development. Alterations to the developmental programme are vital for evolutionary change and these can include the emergence of novel features or a loss of components. Thus, it is important to appreciate that development is modular and that the developmental programme of particular modules can be altered without affecting the whole developmental process. With respect to formation of skeletal components, analysis of the fossil record has suggested that the splanchnocranial skeleton, those elements associated with the pharyngeal arches and which are likely to be neural crest derived, are ancient, whereas the appendicular skeleton, by comparison, is recent ( Donoghue & Sansom, 2002). Thus, the developmental programme underpinning neural crest-derived skeletogenesis is likely to be relatively ancient. The fact that somatosensory neurons are generated from two distinct embryonic populations, neural crest cells and neurogenic placodes, also probably lies in evolutionary history. Neurogenic placodes are a region of the embryonic ectoderm in which neuronal cells are generated, and this is a widespread feature of the metazoa. In numerous animals, from flies to echinoderms, that is how neurons are generated; they are derived from the embryonic skin. However, the neural crest is a vertebrate-specific embryonic cell type. Thus, the ability to generate sensory neurons from the embryonic ectoderm is likely to have preceded the generation of sensory neurons by neural crest cells. Finally, it has been shown that homologues of the Phox2/Tbx20 motor neurons that innervate pharyngeal musculature have been identified in ascidians ( Dufour et al., 2006). In Ciona, CiPhox2 expressing neurons lies in a region of the developing nervous system that abuts the domain of expression of CiOtx rostrally and overlaps with the expression of CiHox1 at its posterior end. These expression profiles define this region as being equivalent to the vertebrate hindbrain. In the post-metamorphic animals, these cells are found in the cerebral ganglion and they express CiTbx20. They also project to the muscle of the pharyngeal basket. One can therefore conclude that it is likely that the pharyngeal musculature and its associated motor neurons evolved prior to the emergence of the vertebrates, well before, for example, the spinal motor that innervates the limb musculature. Thus developmental homoplasy will have arisen as the consequence of the sequential modification of developmental processes over phylogenetic time.

Developmental homoplasy - implications for disease and repair

The fact that developmental homoplasy exists, may have ramifications for our understanding of the differential presentation of some diseases and for the correction of defects through stem cell treatment. For example, it has been noted that muscular dystrophies can affect distinct muscle groups ( Emery, 2002) and this could be underlain by the fact that different muscle groups develop via distinct pathways. The lineage diversity of smooth muscle cells may also relate to vascular disease. There are differences in atherosclerotic lesion formation between thoracic and abdominal aorta, with thoracic segments being more resistant than abdominal, and this was thought to be due to differences in haemodynamic flow patterns. However, transplantation studies have shown that thoracic segments transplanted into atherosclerosis-susceptible abdominal aorta remained resistant after 1 year on an atherogenic diet, suggesting that their developmental origins may be an important factor in this behaviour ( Majesky, 2007). It has also been shown recently that there is a marked difference in the ability of stem cells derived from neural crest to contribute to bone regeneration vs. those derived from mesoderm ( Leucht et al., 2008). Skeletal stem cells derived from the mandible, which has a neural crest origin, can contribute to the regeneration of mandibular fractures and also to the regeneration of fractures of the mesodermally derived tibia. However, stem cells from the tibia can only help repair tibial fractures and will not contribute osteocytes to mandibular defects. Thus in some instances it may be critical to consider the fact that differentiated cell types can be generated through convergent paths and that the developmental history of the stems cells being used to repair a deficit may affect their efficacy. Finally, this of course would also apply to the generation of differentiated cell types from stem cells in vitro. It may not be enough to generate a motor neuron or a smooth muscle cell; the particular features of these cells must be considered as well.

Conclusions

As work progresses, it is probable that instances of developmental homoplasy will become more apparent in many systems, and, in particular, in areas of the body with complex developmental and evolutionary histories, such as the central nervous system and the immune system. With regards to the immune system, studies would seem to suggest that lymph nodes in different sites in the mouse, such as those associated with the nasal tissue vs. Peyer's patch in the gut, employ different mechanisms to realize similar objectives ( Kiyono & Fukuyama, 2004). However, determining the extent to which this represents an example of developmental homoplasy awaits the uncovering of the precise details of the developmental origins of these structures.

Acknowledgments

The author would like to thank Adrian Hayday, Andrew Lumsden, Paul Martin, Ivor Mason, Jo Richardson and Moya Smith for helpful discussions. Work in the author's laboratory is supported by the Wellcome Trust and the Leverhulme Trust.

References

Lankester ER. On the use of the term homology in modern zoology and the distinction between homogenetic and homoplastic agreements. Ann Mag Nat Hist Zool Bot Geol. 1870;6:34-43. [Google Scholar]

Le Douarin NM, Kalcheim C. The Neural Crest. Cambridge: Cambridge University Press; 1999. [Google Scholar]

Articles from Journal of Anatomy are provided here courtesy of Anatomical Society of Great Britain and Ireland

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There is an accumulating body of evidence that highlights the fact that one can identify convergence in programmes of cellular differentiation. That is, that a particular differentiated cell/tissue type can be generated via non-identical paths. Convergence is also seen in evolution and here it is termed homoplasy, thus one could term convergence in cellular differentiation, developmental homoplasy.