Evo-devo Approach Research Articles

Evolution and diversity in avian vocal system: An Evo‐Devo model from the morphological and behavioral perspectives

Birds use various vocalizations to mark their territory and attract mates. Three groups of birds (songbirds, parrots, and hummingbirds) learn their vocalizations through imitation. In the brain of such vocal learners, there is a neural network called the song system specialized for vocal learning and production. In contrast, birds such as chickens and pigeons do not have such a neural network and can only produce innate sounds. Since each avian species shows distinct, genetically inherited vocal learning abilities that are related to its morphology, the avian vocal system is a good model for studying the evolution of functional neural circuits. Nevertheless, studies on avian vocalization from an evolutionary developmental-biological (Evo-Devo) perspective are scant. In the present review, we summarize the results of songbird studies and our recent work that used the Evo-Devo approach to understand the evolution of the avian vocal system.

Hunting for “factor X”: the genetic basis of segmental mismatch

Defending an evo-devo approach to the study of evolution in the pages of this journal may appear to be an unnecessary exercise. However, there are some case studies which, better than others, illustrate the necessity and the potential of considering developmental causes for explaining the evolution of organisms’ body architecture. An example involving the evolution of segmentation in arthropods is the recent study by Janssen et al. (2008). A zoology textbook would typically define a segmented animal as one whose body is composed of a series of modules (segments) that, more or less morphologically differentiated, are aligned along the main body axis. However, there are segmented animals in which such a modular composition is hardly recognizable, because different serial structures along the same axis of the same organism are repeated in discordant arrangement. This condition, termed ‘‘segmental mismatch,’’ characterizes the trunk of many arthropod taxa, in particular myriapods (millipedes, centipedes, and their allies), where the

Evo-Devo and the Evolution of Social Behavior: Brain Gene Expression Analyses in Social Insects

Studies of genes and social behavior, aided by new genomic resources, are coming of age. Here, we show how some of the insights that have emerged from research on the evolution of development (evo-devo) also provide a useful framework for studying the evolution of social behavior at the molecular level. These insights include co-opting old genes for new functions, phenotypic modularity, genetic tool kits, the importance of gene regulation in evolutionary change, and the influences of some genes over multiple timescales. We next outline a few differences between development and behavior that pose challenges for an evo-devo approach to behavior. For the remainder of this chapter, we review several studies that illustrate the relevance of evo-devo insights to our understanding of the evolution of behaviors related to eusociality in the insect societies.

Towards a synthetic view of axis specification mechanisms in vertebrates: insights from the dogfish

The genetic mechanisms, which control axis specification, apparently extensively diverge across vertebrates. In amphibians and teleosts, they are tightly linked to the establishment of an early dorso-ventral polarity. This polarity has no equivalent in amniotes, which unlike the former, retain a considerable plasticity for their site of axis formation until blastula stages and rely on signals secreted by extra-embryonic tissues for the establishment of their early rostro-caudal pattern. In order to better understand the links between these seemingly highly divergent mechanisms, we have used an evo-devo approach, aimed at reconstructing the gnathostome ancestral state and focussed on a chondrichthyan, the dogfish Scyliorhinus canicula. A detailed molecular characterization of the dogfish embryo at blastula and gastrula stages highlights striking similarities with all vertebrate model organisms including amniotes. It suggests the presence in the dogfish of territories homologous to the hypoblast and extra-embryonic ectoderm of the latter, which may therefore reflect the primitive condition of jawed vertebrates. In the ancestral state, these territories are specified at opposite sides of an early axis of bilateral symmetry, homologous to the dorso-ventral axis of amphibians and teleosts, and aligned with the later forming embryonic axis, from head to tail. Amniotes have diverged from this pattern through a posterior expansion of extra-embryonic ectoderm, resulting in an apparently radial symmetry at late blastula stages. These data delineate the broad outlines of the gnathostome ancestral pattern of axis specification and highlight an unexpected unity of mechanisms across jawed vertebrates. They illustrate the complementarity of comparative and genetic approaches for a comprehensive view of developmental mechanisms themselves. To cite this article: M. Coolen et al., C. R. Biologies 332 (2009).

A phylostratigraphy approach to uncover the genomic history of major adaptations in metazoan lineages

Macroevolutionary trends traditionally are studied by fossil analysis, comparative morphology or evo-devo approaches. With the availability of genome sequences and associated data from an increasing diversity of taxa, it is now possible to add an additional level of analysis: genomic phylostratigraphy. As an example of this approach, we use a phylogenetic framework and embryo expression data from Drosophila to show that grouping genes by their phylogenetic origin can uncover footprints of important adaptive events in evolution.

Current opinions in flower development and the evo-devo approach in plant phylogeny

During the last 15 years enormous progress had been made in understanding the genetic and molecular regulation of flower development. The classical A-B-C model, which describes how the activities of three classes of genes coding for transcription factors (A, B, C) alone or coordinately specify the different floral organs, has been expanded by class D genes involved in ovule development and class E genes required for the identities of all floral organs. The molecular quartet model advances the genetic A-B-C-D-E model by describing the presumed interactions between floral MADS-domain proteins. Although the basic developmental program appears to be quite conserved, in non-core eudicots modifications such as ``sliding-boundary'' and ``fading borders'' models had to be established. Since the identity of floral organs is strictly dependent on the activity of the MADS-box genes, duplication and diversification within these genes must have been key processes in flower evolution. Hence, insights into the phylogeny of the floral homeotic genes may help to better understand the evolution of flowers (``evo-devo'').

Comment on “Evo‐Devo and the lungfish: the last gasp of intelligent design”

We have read the editorial entitled “Evo-Devo and the lungfish: the last gasp of intelligent design” (1) with great interest. The mere thought that Intelligent Design could even be put forward in this day and age is mind boggling to most scientists. But with all due respect, merely citing that the transition from water to land was accompanied by the appearance of the aldosterone receptor does not explain how this may have occurred based on natural selection. Without a mechanism for this process, the evolutionists are telling Kipling “Just So Stories” that are no more credible than those of the Intelligent Design proponents, which is why the Intelligent Designers maintain credibility with the lay public. We have published several position papers showing how the lung may have evolved from the swim bladder based on cell–cell signaling mediated by a specific gene regulatory network that functionally integrates the structure and function of the lung from fish to man (2–4), providing a testable mechanism for selection based on stretch-regulation of the surfactant system. We predict that this mechanistic comparative functional genomic evo-devo approach will ultimately elucidate the selection pressure for the aldosterone receptor of the kidney as well.

Can knowledge of developmental processes illuminate the evolution of parental care?

There are two levels of investigation for elucidating the evolution of parental behavior. The macro level focuses on how parental behavior can evolve as an aspect of reproduction. The micro level focuses on how species variations in parental behavior evolve. Recently, modern evolutionary biology has turned to developmental biology as a source for information about how trait variability (the substrate upon which natural selection and other evolutionary mechanisms can operate) can emerge during development (called "evo-devo"). Application of this evo-devo approach to the phenomenon of parental behavior requires identification of those mechanisms that produce variations in developmental pathways leading to parental behavior. It is these variations that provide the phenotypes for the potential evolution of different parental behavior systems. Variations in rodent maternal behavior affect the development of the HPA and HPG axes in their offspring. These mechanisms are examined to reveal how such developmental variations could underlie the evolution of biparental behavior. Knowledge of the developmental mechanisms responsible for species variations in mammalian parental behavior systems may provide insight into those mechanisms that may have been involved in the evolution of parental behavior itself.

Amphioxus: a peaceful anchovy fillet to illuminate Chordate Evolution (I)

The cephalochordate amphioxus occupies a central place in evolutionary thoughts to the origin of Vertebrates. With a prototypical vertebrate-like body plan and a preduplicative genome, the friendly lancelet seems to be in morphological and genetic motionless since its separation from the major branch of evolution that eventually ended up in our corner in the Animal Kingdom. This makes it an ideal model system with which, with the current development of genomic and experimental tools, an Evo-Devo approach to the understanding of the origin of vertebrates looks proper, reliable, and excitingly promising.

Evolutionary origin of the feather epidermis

The formation of scales and feathers in reptiles and birds has fascinated biologists for decades. How might the developmental processes involved in the evolution of the amniote ectoderm be interpreted to shed light on the evolution of integumental appendages? An Evo-Devo approach to this question is proving essential to understand the observation that there is homology between the transient embryonic layers covering the scale epidermis of alligators and birds and the epidermal cell populations of embryonic feather filaments. Whereas the embryonic layers of scutate scales are sloughed off at hatching, that their homologues persist in feathers demonstrates that the predecessors of birds took advantage of the ability of their ectoderm to generate embryonic layers by recruiting them to make the epidermis of the embryonic feather filament. Furthermore, observations on mutant chickens with altered scale and feather development (Abbott and Asmundson [1957] J. Hered. 18:63-70; Abbott [1965] Poult. Sci. 44:1347; Abbott [1967] Methods in developmental biology. New York: Thomas Y. Crowell) suggest that the ectodermal placodes of feathers, which direct the formation of unique dermal condensations and subsequently appendage outgrowth, provided the mechanism by which the developmental processes generating the embryonic layers diverged during evolution to support the morphogenesis of the epidermis of the primitive feather filament with its barb ridges.

Evolution of eyes and photoreceptor cell types.

The evolution of the eye is a matter of debate ever since Darwin's Origin of Species. While morphological comparisons of eye anatomy and photoreceptor cell types led to the view that animal eyes evolved multiple times independently, the molecular conservation of the pax6 eye-specifying cascade has indicated the contrary - that animal eyes evolved from a common, simple precursor, the proto-eye. Morphological and molecular comparative approaches are combined here in a novel Evo-Devo approach, the molecular comparison of cell types ("comparative molecular cell biology"). In the eye, the various types of photoreceptor cells, as well as pigment and lens cells, each require distinct combinations of specifying transcription factors that control their particular differentiation programmes, such as opsin expression in photoreceptors, specific neurotransmitter metabolism, or axonal outgrowth. Comparing the molecular combinatorial codes of cell types of animal extant eyes, their evolutionary histories can be reconstructed. This is exemplified here on the evolution of ciliary and rhabdomeric photoreceptor cells in bilaterian eyes and on the evolution of cell type diversity in the vertebrate retina. I propose that the retinal ganglion, amacrine and horizontal cells are evolutionary sister cell types that evolved from a common rhabdomeric photoreceptor cell precursor.

'De-evolution' of Drosophila toward a more generic mode of axis patterning.

The genetics of the establishment of the primary axes of the early embryo have been worked out in great detail Drosophila. However, evidence has accumulated that Drosophila employs a mode of patterning that is not shared with most insects. In particular, the use of the morphogenic gradient of the Bicoid homeoprotein appears to be a novel addition to the fly developmental toolkit. To better understand the ancestral mode of patterning that is probably more widely used by insects, several groups have used Evo-Devo approaches as well as sophisticated genetic manipulations of Drosophila to achieve some form of 'de-evolution' of this derived insect. Genetic manipulations of the beetle Tribolium and the wasp Nasonia have validated most of these results.

Evolution and development: some insights from evolutionary theory

Developmental biology and evolutionary biology are both mature integrative disciplines which started in the 19th century and then followed parallel and independent scientific pathways. Recently, a genetical component has stepped into both disciplines (developmental genetics and evolutionary genetics) pointing out the need for future convergent maturation. Indeed, the Evo-Devo approach is becoming popular among developmental biologists, based on the facts that distant groups share a common ancestry, that precise phylogenies can be worked out and that homologous genes often play similar roles during the development of very different organisms. In this essay, I try to show that the real future of Evo-Devo thinking is still broader. The evolutionary theory is a set of diverse concepts which can and should be used in any biological field. Evolutionary thinking trains to ask << why >> questions and to provide logical and plausible answers. It can shed some light on a diversity of general problems such as how to distinguish homologies from analogies, the costs and benefits of multicellularity, the origin of novel structures (e.g. the head), or the evolution of sexual reproduction. In the next decade, we may expect a progressive convergence between developmental genetics and quantitative genetics.

Peer Commentaries on Marcy A. Kingsbury and Barbara L. Finlay’s The cortex in multidimensional space: where do cortical areas come from?

Elizabeth Bates, Brain evolution and development: passing through the eye of the needle, p. 143Serena M. Dudek, Multidimensional gene expression in cortical space, p. 145Henry Kennedy and Colette Dehay, Gradients and boundaries: limits of modularity and its influence on the isocortex, p. 147Sarah L. Pallas, Specification of mammalian neocortex: the power of the evo–devo approach in resolving the nature–nurture dichotomy, p. 148Michel Roger, Embryonic stage of commitment of neocortical cells to develop area‐specific connections, p. 151M.W. Spratling and M.H. Johnson, Activity‐dependent processes in regional cortical specialization, p. 153