Starting from fins: parallelism in the evolution of limbs and genitalia. The fin-to-limb transition

The March/April 2002 issue of Evolution and Development focused on three presentations made at the Starting from Fins: Parallelism in the Evolution of Limbs and Genitalia symposium held as part of the 2001 Chicago meeting of the Society of Integrative and Comparative Biology. The intention of the symposium and the publication of the presentations was to extend discussion of the potential and the limits of using serial homologues to understand developmental aspects of morphological evolution. The March/April 2002 issue concentrated on unpaired fin to genitalia transitions. This issue focuses on paired fins to limbs and highlights the need for developmental data to be integrated with data from fossil materal, phylogenetic analysis, and explicitly comparative studies. Coates et al. use phylogenetic methods to explore the limb/fin characters of taxa, but their analysis departs somewhat from the usual in that the reference group for organisms includes sister group taxa not usually considered true tetrapods. They state that including finned taxa from the stem group permits an attempt to distinguish the primitive condition of the characteristics demonstrated by the crown group, that is, "limbed tetrapods." In focusing on limb characters specifically and including aspects of the appendicular girdles, Coates et al. highlight morphological details and trends within a given phylogeny. They also demonstrate the degree of relevance of limb characters during the establishment of lineages and their branching patterns by using only limb characters to generate a tree and use a direct comparison of serial versus special homologies to explore the degree of evolutionary parallelism between fore-and hindlimbs. The preliminary conclusions indicate a high level of independence between the serially homologous fore-and hindlimb. Innes et al. present outcomes from the use of cutting edge molecular genetic approaches to understand developmental aspects of limb morphology. In a manner conceptually similar to Coates et al.'s use of fossil characters, Innes et al. use the serial analysis of gene expression to sort differences from similarities in the gene expression profiles of fore-and hindlimbs of the same embryos. Although these gene expression pattems are likely to reflect the serial homology of the paired limbs, they are silent in terms of our understanding both the profound and subtle differences between fore- and hindlimbs in any given species. Innes et al. point out the volume of data generated by SAGE far exceeds our ability to interpret its biological meaning. The studies presented here and in the March/April issue are excellent examples of the need to interpret complex data in light of collective knowledge of evolutionary history. We hope the insights gained from the symposium and papers contribute to a dialogue on how to integrate different approaches and assist in moving forward the field of Evolution and 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.     

The dynamics of developmental system drift in the gene network underlying wing polyphenism in ants: a mathematical model

SUMMARY Understanding the complex interaction between genotype and phenotype is a major challenge of Evolutionary Developmental Biology. One important facet of this complex interaction has been called "Developmental System Drift" (DSD). DSD occurs when a similar phenotype, which is homologous across a group of related species, is produced by different genes or gene expression patterns in each of these related species. We constructed a mathematical model to explore the developmental and evolutionary dynamics of DSD in the gene network underlying wing polyphenism in ants. Wing polyphenism in ants is the ability of an embryo to develop into a winged queen or a wingless worker in response to an environmental cue. Although wing polyphenism is homologous across all ants, the gene network that underlies wing polyphenism has evolved. In winged ant castes, our simulations reproduced the conserved gene expression patterns observed in the network that controls wing development in holometabolous insects. In wingless ant castes, we simulated the suppression of wings by interrupting (up- or downregulating) the expression of genes in the network. Our simulations uncovered the existence of four groups of genes that have similar effects on target gene expression and growth. Although each group is comprised of genes occupying different positions in the network, their interruption produces vestigial discs that are similar in size and shape. The implications of our results for understanding the origin, evolution, and dissociation of the gene network underlying wing polyphenism in ants are discussed.     

Conservation and co-option in developmental programmes: the importance of homology relationships

One of the surprising insights gained from research in evolutionary developmental biology (evo-devo) is that increasing diversity in body plans and morphology in organisms across animal phyla are not reflected in similarly dramatic changes at the level of gene composition of their genomes. For instance, simplicity at the tissue level of organization often contrasts with a high degree of genetic complexity. Also intriguing is the observation that the coding regions of several genes of invertebrates show high sequence similarity to those in humans. This lack of change (conservation) indicates that evolutionary novelties may arise more frequently through combinatorial processes, such as changes in gene regulation and the recruitment of novel genes into existing regulatory gene networks (co-option), and less often through adaptive evolutionary processes in the coding portions of a gene. As a consequence, it is of great interest to examine whether the widespread conservation of the genetic machinery implies the same developmental function in a last common ancestor, or whether homologous genes acquired new developmental roles in structures of independent phylogenetic origin. To distinguish between these two possibilities one must refer to current concepts of phylogeny reconstruction and carefully investigate homology relationships. Particularly problematic in terms of homology decisions is the use of gene expression patterns of a given structure. In the future, research on more organisms other than the typical model systems will be required since these can provide insights that are not easily obtained from comparisons among only a few distantly related model species.     

Conserved developmental processes and the formation of evolutionary novelties: examples from butterfly wings

The origin and diversification of evolutionary novelties-lineage-specific traits of new adaptive value-is one of the key issues in evolutionary developmental biology. However, comparative analysis of the genetic and developmental bases of such traits can be difficult when they have no obvious homologue in model organisms. The finding that the evolution of morphological novelties often involves the recruitment of pre-existing genes and/or gene networks offers the potential to overcome this challenge. Knowledge about shared developmental processes obtained from extensive studies in model organisms can then be used to understand the origin and diversification of lineage-specific structures. Here, we illustrate this approach in relation to eyespots on the wings of Bicyclus anynana butterflies. A number of spontaneous mutations isolated in the laboratory affect eyespots, lepidopteran-specific features, and also processes that are shared by most insects. We discuss how eyespot mutants with disturbed embryonic development may help elucidate the genetic pathways involved in eyespot formation, and how venation mutants with altered eyespot patterns might shed light on mechanisms of eyespot development.     

Evolution and development — the nematode vulva as a case study

To understand how morphological characters change during evolution, we need insight into the evolution of developmental processes. Comparative developmental approaches that make use of our fundamental understanding of development in certain model organisms have been initiated for different animal systems and flowering plants. Nematodes provide a useful experimental system with which to investigate the genetic and molecular alterations underlying evolutionary changes of cell fate specification in development, by comparing different species to the genetic model system Caenorhabditis elegans. In this review, I will first discuss the different types of evolutionary alterations seen at the cellular level by focusing mainly on the analysis of vulva development in different species. The observed alterations involve changes in cell lineage, cell migration and cell death, as well as induction and cell competence. I then describe a genetic approach in the nematode Pristionchus pacificus that might identify those genetic and molecular processes that cause evolutionary changes of cell fate specification.     

Distinguishing heat from light in debate over controversial fossils

Fossil organisms offer our only direct insight into how the distinctive body plans of extant organisms were assembled. However, realizing the potential evolutionary significance of fossils can be hampered by controversy over their interpretation. Here, as a guide to evaluating palaeontological debates, we outline the process and pitfalls of fossil interpretation. The physical remains of controversial fossils should be reconstructed before interpreting homologies, and choice of interpretative model should be explicit and justified. Extinct taxa lack characters diagnostic of extant clades because the characters had not yet evolved, because of secondary loss, or because they have rotted away. The latter, if not taken into account, will lead to the spurious assignment of fossils to basally branching clades. Conflicting interpretations of fossils can often be resolved by considering all the steps in the process of anatomical analysis and phylogenetic placement, although we must accept that some fossil organisms are simply too incompletely preserved for their evolutionary significance to be realized.     

The place of phylogeny and cladistics in Evo-Devo research

Here we review the various uses to which phylogenetic trees may be put when analysing the evolution of organisms and of the genotypic and phenotypic characteristics of these organisms. We briefly discuss the cladistic method and its application in the inference of phylogenetictrees. Next we consider the uses to which phylogenetic trees can be put: in particular for determining the homology or otherwise of characters distributed on those trees and for estimating the likely characteristics of ancestral taxa. Finally we show the application of this information for deepening our understanding of the processes of evolution. All of these forms of inference are fundamental for comparative biology and of immediate importance to the practice of evolutionary developmental biology.     

A hitchhikers guide to the Galápagos: co-phylogeography of Galápagos mockingbirds and their parasites

Background

Parasites are evolutionary hitchhikers whose phylogenies often track the evolutionary history of their hosts. Incongruence in the evolutionary history of closely associated lineages can be explained through a variety of possible events including host switching and host independent speciation. However, in recently diverged lineages stochastic population processes, such as retention of ancestral polymorphism or secondary contact, can also explain discordant genealogies, even in fully co-speciating taxa. The relatively simple biogeographic arrangement of the Galápagos archipelago, compared with mainland biomes, provides a framework to identify stochastic and evolutionary informative components of genealogic data in these recently diverged organisms.

Results

Mitochondrial DNA sequences were obtained for four species of Galápagos mockingbirds and three sympatric species of ectoparasites - two louse and one mite species. These data were complemented with nuclear EF1α sequences in selected samples of parasites and with information from microsatellite loci in the mockingbirds. Mitochondrial sequence data revealed differences in population genetic diversity between all taxa and varying degrees of topological congruence between host and parasite lineages. A very low level of genetic variability and lack of congruence was found in one of the louse parasites, which was excluded from subsequent joint analysis of mitochondrial data. The reconciled multi-species tree obtained from the analysis is congruent with both the nuclear data and the geological history of the islands.

Conclusions

The gene genealogies of Galápagos mockingbirds and two of their ectoparasites show strong phylogeographic correlations, with instances of incongruence mostly explained by ancestral genetic polymorphism. A third parasite genealogy shows low levels of genetic diversity and little evidence of co-phylogeny with their hosts. These differences can mostly be explained by variation in life-history characteristics, primarily host specificity and dispersal capabilities. We show that pooling genetic data from organisms living in close ecological association reveals a more accurate phylogeographic history for these taxa. Our results have implications for the conservation and taxonomy of Galápagos mockingbirds and their parasites.     

Evolutionary change in the functional specificity of genes.

Species throughout the animal kingdom share not only housekeeping but also many key regulatory genes. Nonetheless, species differ from one another developmentally and thus, also morphologically. One of the general aims of comparative developmental genetics is to understand how similar molecules can generate the known diversity of biological form. Here, we argue that gene function can change in different ways during the evolution of developmental processes. Genes can be recruited to serve completely new functions in a new regulatory linkage (co-option), they can change their molecular specificity while remaining in the original (homologous) developmental program and can, at the same time, retain other functions. We describe evidence for such evolutionary patterns based on the comparison of loss-of-function mutations of homologous genes of the two free-living nematodes Caenorhabditis elegans and Pristionchus pacificus. Ultimately, it is the interplay of conservation and change of the specificity of genes and genetic networks that generates developmental novelty over evolutionary time.     

Multigene families and the evolution of complexity

Summary Higher organisms are complex, and their developmental processes are controlled by the sequential expression of genes that often form multigene families. Facts are surveyed on how functional diversity of genes is related to duplication of genes or segments of genes, by emphasizing that diversity is often enhanced by alternate splicing and proteolytic cleavage involving duplicated genes or gene segments. Analyses of a population genetics model for the origin of gene families suggest that positive Darwinian selection is needed for acquiring gene families with desirable functions. Based on these considerations, examples that show acceleration of amino acid substitution relative to synonymous change during evolutionary processes are surveyed. Some of such examples strongly suggest that positive selection has worked. In other cases it is difficult to judge whether or not acceleration is caused by positive Darwinian selection. As a general pattern, acceleration of amino acid substitution is often found to be related to gene duplication. It is thought that complexity and diversity of gene function have been advantageous in the long evolutionary course of higher organisms.     

Developmental variations among Panagrolaimid nematodes indicate developmental system drift within a small taxonomic unit

Comparative studies of nematode embryogenesis among different clades revealed considerable variations. However, to what extent developmental differences exist between closely related species has mostly remained nebulous. Here, we explore the correlation between phylogenetic neighborhood and developmental variation in a restricted and morphologically particularly uniform taxonomic group (Panagrolaimidae) to determine to what extent (1) morphological and developmental characters go along with molecular data and thus can serve as diagnostic tools for the definition of kinship and (2) developmental system drift (DSD; modifications of developmental patterns without corresponding morphological changes) can be found within a small taxonomic unit. Our molecular approaches firmly support subdivision of Panagrolaimid nematodes into two monophyletic groups. These can be discriminated by distinct peculiarities in early embryonic cell lineages and a mirror-image expression pattern of the gene skn-1. This suggests major changes in the logic of cell specification and the action of DSD in the studied representatives of the two neighboring nematode taxa.     

Speciation and diversification of parasite lineages: an analysis of congeneric parasite species in vertebrates

The evolutionary diversification of living organisms is a central research theme in evolutionary ecology, and yet it remains difficult to infer the action of evolutionary processes from patterns in the distribution of rates of diversification among related taxa. Using data from helminth parasite communities in 76 species of birds and 114 species of mammals, the influence of four factors that may either be associated with or modulate rates of parasite speciation were examined in a comparative analysis. Two measures of the relative number of congeneric parasite species per host species were used as indices of parasite diversification, and related to host body mass, host density, latitude, and whether the host is aquatic or terrestrial. The occurrence of congeneric parasites was not distributed randomly with respect to these factors. Aquatic bird species tended to harbour more congeneric parasites than terrestrial birds. Large-bodied mammal species, or those living at low latitudes, harboured more congeneric parasites than small-bodied mammals, or than those from higher latitudes. Host density had no apparent association with either measures of parasite diversification. These patterns, however, reflect only the present-day distribution of parasite diversification among host taxa, and not the evolutionary processes responsible for diversification, because the apparent effects of the factors investigated disappeared once corrections were made for host phylogeny. This indicates that features other than host body size, host density, latitude, and whether the habitat is terrestrial or aquatic, have been the key driving forces in the diversification of parasitic helminth lineages. This revised version was published online in July 2006 with corrections to the Cover Date.     

Comparative methods for examining adaptation depend on evolutionary models

Comparisons among taxa provide a powerful means for helping to understand why primate species differ from each other in morphology, behaviour and life history. Comparative tests can also mislead when not applied correctly, and correct application means taking into account the phylogenetic relationships among the species being compared. Adaptation is defined as a comparative concept. The reasons for phenotypic similarity among closely related taxa are summarized. Different models of evolutionary change dictate different methods for reconstructing ancestral character states and for performing comparative analyses on categorical and continuously varying character. All comparative methods rely either implicitly of explicitly on some model of how evolution proceeds. The choice of a particular method of analysis is, therefore, an implicit choice of a model of evolution.     

Recent findings in evolution and function of insect innexins

The past decade has seen significant advances in the field of innexin biology, particularly in the model invertebrate organisms, the nematode Caenorhabditis elegans and the fly Drosophila melanogaster. However, advances in genomics and functional techniques during this same period are ushering in a period of comparative innexin biology. Insects are the most diverse metazoan taxa in terms of species number, as well as in developmental, physiological, and morphological processes. Combined with genomics data, the study of innexins should rapidly advance. In this review, we consider the current state of knowledge regarding innexins in insects, focusing on innexin diversity, both evolutionary and functional. We also consider an unusual set of innexins, known as vinnexins, that have been isolated from mutualistic viruses of some parasitoid wasps. We conclude with a call to study insect innexins from a broader, evolutionary perspective. Knowledge derived from such comparative studies will offer significant insight into developmental and evolutionary physiology, as well as specific functional processes in a taxon that has huge biomedical and ecological impact on humans.     

Modularity, comparative embryology and evo-devo: Developmental dissection of evolving body plans

Modules can be defined as quasi-autonomous units that are connected loosely with each other within a system. A need for the concept of modularity has emerged as we deal with evolving organisms in evolutionary developmental research, especially because it is unknown how genes are associated with anatomical patterns. One of the strategies to link genotypes with phenotypes could be to relate developmental modules with morphological ones. To do this, it is fundamental to grasp the context in which certain anatomical units and developmental processes are associated with each other specifically. By identifying morphological modularities as units recognized by some categories of general homology as established by comparative anatomy, it becomes possible to identify developmental modules whose genetic components exhibit coextensive expressions. This permits us to distinguish the evolutionary modification in which the identical morphological module simply alters its shape for adaptation, without being decoupled from the functioning gene network (‘coupled modularities’), from the evolution of novelty that involves a heterotopic shift between the anatomical and developmental modules. Using this formulation, it becomes possible, within the realm of Geoffroy's homologous networks, to reduce morphological homologies to developmental mechanistic terms by dissociating certain classes of modules that are often associated with actual shapes and functions.     

Evolution of male sexual characters in the oriental Drosophila melanogaster species group

Understanding the genetic and molecular mechanisms of morphological evolution is one of the greatest challenges in evolutionary biology. Sexually dimorphic traits, which often evolve at a high rate due to their involvement in mate choice and sexual selection, present unique opportunities for investigating changes in development over short evolutionary distances. Phylogenetic analysis is essential to provide a historical framework for comparative studies of development by establishing the order and polarity of morphological changes. In this report, we apply a new molecular phylogeny to reconstruct the evolution of male sexual characters in a group of species closely related to the model species Drosophila melanogaster. These highly variable traits include wing melanin patterns, the sex comb, and the structure of external genitalia and analia. We show that sexually dimorphic characters can diverge very rapidly among closely related species. More surprisingly, we also find a pervasive pattern of independent origin and secondary loss of male sexual traits in different evolutionary lineages.     

Mouse models and the evolutionary developmental biology of the skull

Understanding development is relevant to understanding evolutionbecause developmental processes structure the expression ofphenotypic variation upon which natural selection acts. Advancesin developmental biology are fueling a new synthesis of developmentaland evolutionary biology, but it remains unclear how to usedevelopmental information that largely derives from a few modelorganisms to test hypotheses about the evolutionary developmentalbiology of taxa such as humans and other primates that havenot been or are not amenable to direct study through experimentaldevelopmental biology. In this article, we discuss how and whenmodel organisms like mice are useful for studying the evolutionarydevelopmental biology of even rather distantly related and morphologicallydifferent groups like primates. A productive approach is tofocus on processes that are likely to play key roles in producingevolutionarily significant phenotypic variation across a largephylogenetic range. We illustrate this approach by applyingthe analysis of craniofacial variation in mouse mutant modelsto primate and human evolution.