Introduction to ‘Homology and convergence in nervous system evolution’

The origin of brains and central nervous systems (CNSs) is thought to have occurred before the Palaeozoic era 540 Ma. Yet in the absence of tangible evidence, there has been continued debate whether today''s brains and nervous systems derive from one ancestral origin or whether similarities among them are due to convergent evolution. With the advent of molecular developmental genetics and genomics, it has become clear that homology is a concept that applies not only to morphologies, but also to genes, developmental processes, as well as to behaviours. Comparative studies in phyla ranging from annelids and arthropods to mammals are providing evidence that corresponding developmental genetic mechanisms act not only in dorso–ventral and anterior–posterior axis specification but also in segmentation, neurogenesis, axogenesis and eye/photoreceptor cell formation that appear to be conserved throughout the animal kingdom. These data are supported by recent studies which identified Mid-Cambrian fossils with preserved soft body parts that present segmental arrangements in brains typical of modern arthropods, and similarly organized brain centres and circuits across phyla that may reflect genealogical correspondence and control similar behavioural manifestations. Moreover, congruence between genetic and geological fossil records support the notion that by the ‘Cambrian explosion’ arthropods and chordates shared similarities in brain and nervous system organization. However, these similarities are strikingly absent in several sister- and outgroups of arthropods and chordates which raises several questions, foremost among them: what kind of natural laws and mechanisms underlie the convergent evolution of such similarities? And, vice versa: what are the selection pressures and genetic mechanisms underlying the possible loss or reduction of brains and CNSs in multiple lineages during the course of evolution? These questions were addressed at a Royal Society meeting to discuss homology and convergence in nervous system evolution. By integrating knowledge ranging from evolutionary theory and palaeontology to comparative developmental genetics and phylogenomics, the meeting covered disparities in nervous system origins as well as correspondences of neural circuit organization and behaviours, all of which allow evidence-based debates for and against the proposition that the nervous systems and brains of animals might derive from a common ancestor.     

Gene expression patterns in seed plant shoot meristems and leaves: homoplasy or homology?

The fossil record reveals that seed plant leaves evolved from ancestral lateral branch systems. Over time, the lateral branch systems evolved to become determinate, planar and eventually laminar. Considering their evolutionary histories, it is instructive to compare the developmental genetics of shoot apical meristems (SAMs) and leaves in extant seed plants. Genetic experiments in model angiosperm species have assigned functions of meristem maintenance, specification of stem cell identity, boundary formation, polarity establishment and primordium initiation to specific genes. Investigation of roles of the same or homologous genes during leaf development has revealed strikingly similar functions in leaves compared to SAMs. Specifically, the marginal blastozone that characterizes many angiosperm leaves appears to function in a manner mechanistically similar to the SAM. We argue here that the similarities may be homologous due to descent from ancestral roles in an ancestral shoot system. Molecular aspects of SAM and leaf development in gymnosperms is largely neglected and could provide insight into seed plant leaf evolution.     

Eye evolution at high resolution: The neuron as a unit of homology

Based on differences in morphology, photoreceptor-type usage and lens composition it has been proposed that complex eyes have evolved independently many times. The remarkable observation that different eye types rely on a conserved network of genes (including Pax6/eyeless) for their formation has led to the revised proposal that disparate complex eye types have evolved from a shared and simpler prototype. Did this ancestral eye already contain the neural circuitry required for image processing? And what were the evolutionary events that led to the formation of complex visual systems, such as those found in vertebrates and insects? The recent identification of unexpected cell-type homologies between neurons in the vertebrate and Drosophila visual systems has led to two proposed models for the evolution of complex visual systems from a simple prototype. The first, as an extension of the finding that the neurons of the vertebrate retina share homologies with both insect (rhabdomeric) and vertebrate (ciliary) photoreceptor cell types, suggests that the vertebrate retina is a composite structure, made up of neurons that have evolved from two spatially separate ancestral photoreceptor populations. The second model, based largely on the conserved role for the Vsx homeobox genes in photoreceptor-target neuron development, suggests that the last common ancestor of vertebrates and flies already possessed a relatively sophisticated visual system that contained a mixture of rhabdomeric and ciliary photoreceptors as well as their first- and second-order target neurons. The vertebrate retina and fly visual system would have subsequently evolved by elaborating on this ancestral neural circuit. Here we present evidence for these two cell-type homology-based models and discuss their implications.     

Single locus affects embryonic segment polarity and multiple aspects of an adult evolutionary novelty

Background  

The characterization of the molecular changes that underlie the origin and diversification of morphological novelties is a key challenge in evolutionary developmental biology. The evolution of such traits is thought to rely largely on co-option of a toolkit of conserved developmental genes that typically perform multiple functions. Mutations that affect both a universal developmental process and the formation of a novelty might shed light onto the genetics of traits not represented in model systems. Here we describe three pleiotropic mutations with large effects on a novel trait, butterfly eyespots, and on a conserved stage of embryogenesis, segment polarity.     

Evolving eyes

Despite the incredible diversity among extant eyes, laws of physics constrain how light can be collected resulting in only eight known optical systems in animal eyes. Surprisingly, all animal eyes share a common molecular strategy using opsin for catching photons, but there are a diverse collection of mechanisms with proteins unrelated to each other used to focus light for vision. However, opsin is expressed in either one of two types of photoreceptor that differ fundamentally in their structure and tissue of origin. Taken together, this collection of observations strongly suggests that eyes have had multiple origins with remarkable convergence due to physics and molecular conservation of the opsin protein. Yet recent work has shown that a family of conserved genes are involved in eye formation despite substantial differences in their structure and origin, leading to a controversy over whether eyes evolved once or repeatedly. A likely resolution of this discussion is that particular genes and genetic programs have become associated with specific features needed for eyes and such suites of genes have been recruited as new eyes evolve. Since specific genes and their products are used repeatedly, it is somewhat difficult to conceptualize their causal relationships relative to evolutionary processes. However, detailed comparison of developmental programs may offer clues about multiple origins.     

Arboreallty and morphological evolution in ground beetles (Carabidae: Harpalinae): testing the taxon pulse model

Abstract.— One-third to two-thirds of all tropical carabids, or ground beetles, are arboreal, and evolution of arboreality has been proposed to be a dead end in this group. Many arboreal carabids have unusual morphological features that have been proposed to be adaptations for life on vegetation, including large, hemispheric eyes; an elongated prothorax; long elytra; long legs; bilobed fourth tarsomeres; adhesive setae on tarsi; and pectinate claws. However, correlations between these features and arboreality have not been rigorously tested previously. I examined the evolution of arboreality and morphological features often associated with this habitat in a phylogenetic context. The number and rates of origins and losses of arboreality in carabids in the subfamily Harpalinae were inferred with parsimony and maximum-likelihood on a variety of phylogenetic hypotheses. Correlated evolution in arboreality and morphological characters was tested with concentrated changes tests, maximum-likelihood, and independent contrasts on optimal phylogenies. There is strong evidence that both arboreality and the morphological features examined originated multiple times and can be reversed, and in no case could the hypothesis of equal rates of gains and losses be rejected. Several features are associated with arboreality: adhesive setae on the tarsi, bilobed tarsomeres, and possibly pectinate claws and an elongated prothorax. Bulgy eyes, long legs, and long elytra were not correlated with arboreality and are probably not arboreal adaptations. The evolution of arboreal carabids has not been unidirectional. These beetles have experienced multiple gains and losses of arboreality and the morphological characters commonly associated with the arboreal habitat. The evolutionary process of unidirectional character change may not be as widespread as previously thought and reversal from specialized lifestyles or habitats may be common.     

Evidence for evolutionary changes in ontogeny: Paleontological, comparative-morphological, and molecular aspects

It has been noted that the integration of modern data of paleontology, comparative morphology, developmental biology, and molecular genetics forms the basis for understanding the mechanisms of evolutionary transformations of ontogeny. Paleontological and morphological evidence of the evolutionary changes in ontogeny are considered based on the data of cell and molecular biology and developmental genetics. It is shown that reorganizations of gene regulatory cascades (mainly Hox genes) play a key role in the evolution of the axial organization of animals and modifications of the limb structure of metazoans, whereas the formation of new types of structures was apparently determined by the emergence of new populations of stem cells in embryogenesis (for example, neural crest cells in the evolution of vertebrates).     

Origins of the other metazoan body plans: the evolution of larval forms

Bilaterian animal body plan origins are not solely about adult forms. Most animals have larvae with body plans, ontogenies and ecologies distinct from adults. There are two primary hypotheses for larval origins. The first hypothesis suggests that the first animals were small pelagic forms similar to modern larvae, with adult bilaterian body plans evolved subsequently. The second hypothesis suggests that adult bilaterian body plans evolved first and that larval body plans arose by interpolation of features into direct-developing ontogenies. The two hypotheses have different consequences for understanding parsimony in evolution of larvae and of developmental genetic mechanisms. If primitive metazoans were like modern larvae and distinct adult forms evolved independently, there should be little commonality of patterning genes among adult body plans. However, sharing of patterning genes is observed. If larvae arose by co-option of adult bilaterian-expressed genes into independently evolved larval forms, larvae may show morphological convergence, but with distinct patterning genes, and this is observed. Thus, comparative studies of gene expression support independent origins of larval features. Precambrian and Cambrian embryonic fossils are also consistent with direct development of the adult as being primitive, with planktonic larvae arising during the Cambrian. Larvae have continued to co-opt genes and evolve new features, allowing study of developmental evolution.     

Evolutionary basis of parallelism in North American scincid lizards

This study uses a phylogenetic framework to explore the causes of parallelism in two North American scincid lizard assemblages: the skiltonianus and fasciatus species groups of the genus Plestiodon. Each group consists of several closely related species with conserved neonate morphology; features that distinguish species become accentuated during ontogeny, and these differences often resemble different endpoints along a developmental continuum. This continuum is believed to be an expression of the ancestral ontogeny, and has led to the hypothesis that evolutionary change in development has generated much of the observed morphological diversity. However, progress on understanding these mechanisms is limited by a lack of well-supported phylogenetic data for the fasciatus group, and for Plestiodon in general. Recent phylogenetic studies on the skiltonianus group have revealed previously undetected cases of parallelism, and raise the possibility that similar cases have yet to be discovered in the fasciatus group. Here, I estimate a phylogeny to test the monophyly of the fasciatus group and infer its relationship with other North American Plestiodon using 2537 bp from six mtDNA genes. I use the phylogeny to reconstruct the mode (graduated vs. punctuated) and direction of body size evolution, to map the evolution of two predominant color morphs, and to test whether size and color pattern evolve concertedly. The results show that the morphotypes of the traditional fasciatus group constitute good species, but that the species group is rendered paraphyletic by several geographically overlapping species that deviate from the fasciatus-like ontogeny. Body size evolution has occurred gradually and bi-directionally, and shifts to large body size have been consistently associated with the loss of the striped color pattern during ontogeny. I show that parallelism, a lack of rigorous phylogenetic analysis, and a reliance on shared ontogenetic features for predicting phylogenetic relatedness, has misled the traditional systematics of these lizards, but that general ideas concerning the role of development in their morphological evolution remain supported. I close by proposing that the processes influencing repeated phyletic patterns in the skiltonianus and fasciatus groups represent adherence to an ancestral ground state, and discuss the importance of using phylogenies for the initial characterization of evolutionary changes in development.     

Genetic and developmental basis for parallel evolution and its significance for hominoid evolution

Greater understanding of ape comparative anatomy and evolutionary history has brought a general appreciation that the hominoid radiation is characterized by substantial homoplasy.^1–4 However, little consensus has been reached regarding which features result from repeated evolution. This has important implications for reconstructing ancestral states throughout hominoid evolution, including the nature of the Pan‐Homo last common ancestor (LCA). Advances from evolutionary developmental biology (evo‐devo) have expanded the diversity of model organisms available for uncovering the morphogenetic mechanisms underlying instances of repeated phenotypic change. Of particular relevance to hominoids are data from adaptive radiations of birds, fish, and even flies demonstrating that parallel phenotypic changes often use similar genetic and developmental mechanisms. The frequent reuse of a limited set of genes and pathways underlying phenotypic homoplasy suggests that the conserved nature of the genetic and developmental architecture of animals can influence evolutionary outcomes. Such biases are particularly likely to be shared by closely related taxa that reside in similar ecological niches and face common selective pressures. Consideration of these developmental and ecological factors provides a strong theoretical justification for the substantial homoplasy observed in the evolution of complex characters and the remarkable parallel similarities that can occur in closely related taxa. Thus, as in other branches of the hominoid radiation, repeated phenotypic evolution within African apes is also a distinct possibility. If so, the availability of complete genomes for each of the hominoid genera makes them another model to explore the genetic basis of repeated evolution.     

Historical perspective on the development and evolution of eyes and photoreceptors

The development and evolution of eyes is an "old problem" in biology, which required a special treatment in Charles Darwin's "Origin of the species" (1882) under the heading of "Difficulties of the theory". Darwin postulated a simple and imperfect eye, as a prototype, which can vary and evolve under natural selection into more complex and perfect eyes. Based upon morphological criteria and the different modes of development of the different kinds of eyes, neodarwinists have postulated that the various eye-types are polyphyletic in origin and that the eyes have evolved independently in the various animal phyla. Recent developmental genetic experiments and molecular phylogenetic analyses cast serious doubts on this interpretation and argue strongly for a monophyletic origin of the eyes from a Darwinian prototype and subsequent divergent, parallel and convergent evolution leading to the various eye-types.     

Something for nothing? Reconstruction of ancestral character states in asterinid sea star development

SUMMARY Traits from early development mapped onto phylogenetic trees can potentially offer insight into the evolutionary history of development by inferring the states of those characters among ancestors at nodes in the phylogeny. A key and often-overlooked aspect of such mapping is the underlying model of character evolution. Without a well-supported and realistic model ("nothing"), character mapping of ancestral traits onto phylogenetic trees might often return results ("something") that lack a sound basis. Here we reconsider a challenging case study in this area of evolutionary developmental biology: the inference of ancestral states for ecological and morphological characters in the reproduction and larval development of asterinid sea stars. We apply improved analytical methods to an expanded set of asterinid phylogenetic data and developmental character states. This analysis shows that the new methods might generally offer some independent insight into choice of a model of character evolution, but that in the specific case of asterinid sea stars the quantitative features of the model (especially the relative probabilities of different directions of change) have an important effect on the results. We suggest caution in applying ancestral state reconstructions in the absence of an independently corroborated model of character evolution, and highlight the need for such modeling in evolutionary developmental biology.     

Hypothesis testing in evolutionary developmental biology: a case study from insect wings

Developmental data have the potential to give novel insights into morphological evolution. Because developmental data are time-consuming to obtain, support for hypotheses often rests on data from only a few distantly related species. Similarities between these distantly related species are parsimoniously inferred to represent ancestral aspects of development. However, with limited taxon sampling, ancestral similarities in developmental patterning can be difficult to distinguish from similarities that result from convergent co-option of developmental networks, which appears to be common in developmental evolution. Using a case study from insect wings, we discuss how these competing explanations for similarity can be evaluated. Two kinds of developmental data have recently been used to support the hypothesis that insect wings evolved by modification of limb branches that were present in ancestral arthropods. This support rests on the assumption that aspects of wing development in Drosophila, including similarities to crustacean epipod patterning, are ancestral for winged insects. Testing this assumption requires comparisons of wing development in Drosophila and other winged insects. Here we review data that bear on this assumption, including new data on the functions of wingless and decapentaplegic during appendage allocation in the red flour beetle Tribolium castaneum.     

Primitive versus derived traits in the developmental program of the vertebrate head: views from cyclostome developmental studies

Evolution can be viewed as a series of changes in the developmental program along the phylogenetic tree. To better understand the early evolution of the vertebrate skull, we can use the embryos of the cyclostome species as models. By comparing the cyclostome developmental patterns with those of gnathostomes, it becomes possible to distinguish the primitive and derived parts of the developmental program as taxon-specific traits. These traits are often recognizable as developmental constraints that define taxa by biasing the developmental trajectories within a certain limited range, resulting in morphological homologies in adults. These developmental constraints are distributed on the phylogenetic tree like the morphological character states of adult animals and are associated with specific regions of the tree. From this perspective, we emphasize the importance of considering gene expression and embryonic anatomy as the mechanistic bases that can result in homologous or nonhomologous morphological patterns at later developmental stages. Taking the acquisition of the jaw and trabecula cranii as examples, we demonstrate that a set of embryonic features can be coupled or decoupled during evolution and development. When they are coupled, they exert an ancestral developmental constraint that results in homologous morphological patterns, and when they are decoupled, the ancestral constraints tend to be abandoned, generating a new body plan. The heterotopy behind the specification of the oral domain is an example of decoupling, based on shifted tissue interactions. We also stress the importance of "developmental burden" in determining the sequential order of changes through evolution.     

Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution

Biologists have long sought to understand which genes and what kinds of changes in their sequences are responsible for the evolution of morphological diversity. Here, I outline eight principles derived from molecular and evolutionary developmental biology and review recent studies of species divergence that have led to a genetic theory of morphological evolution, which states that (1) form evolves largely by altering the expression of functionally conserved proteins, and (2) such changes largely occur through mutations in the cis-regulatory sequences of pleiotropic developmental regulatory loci and of the target genes within the vast networks they control.