The relationship between relative solvent accessibility and evolutionary rate in protein evolution

Recent work with Saccharomyces cerevisiae shows a linear relationship between the evolutionary rate of sites and the relative solvent accessibility (RSA) of the corresponding residues in the folded protein. Here, we aim to develop a mathematical model that can reproduce this linear relationship. We first demonstrate that two models that both seem reasonable choices (a simple model in which selection strength correlates with RSA and a more complex model based on RSA-dependent amino acid distributions) fail to reproduce the observed relationship. We then develop a model on the basis of observed site-specific amino acid distributions and show that this model behaves appropriately. We conclude that evolutionary rates are directly linked to the distribution of amino acids at individual sites. Because of this link, any future insight into the biophysical mechanisms that determine amino acid distributions will improve our understanding of evolutionary rates.     

Developmental system drift and flexibility in evolutionary trajectories

SUMMARY The comparative analysis of homologous characters is a staple of evolutionary developmental biology and often involves extrapolating from experimental data in model organisms to infer developmental events in non-model organisms. In order to determine the general importance of data obtained in model organisms, it is critical to know how often and to what degree similar phenotypes expressed in different taxa are formed by divergent developmental processes. Both comparative studies of distantly related species and genetic analysis of closely related species indicate that many characters known to be homologous between taxa have diverged in their morphogenetic or gene regulatory underpinnings. This process, which we call "developmental system drift" (DSD), is apparently ubiquitous and has significant implications for the flexibility of developmental evolution of both conserved and evolving characters. Current data on the population genetics and molecular mechanisms of DSD illustrate how the details of developmental processes are constantly changing within evolutionary lineages, indicating that developmental systems may possess a great deal of plasticity in their responses to natural selection.     

Developmental plasticity associated with early structural integration and evolutionary patterns: Examples of developmental bias and developmental facilitation in the skeletal system

The relation of developmental plasticity to evolutionary diversification is a key component of evolutionary theory involving developmental bias, but the basis of the relationship varies among traits and among taxa. Here I review some scenarios of how structural integration during early organogenesis could influence this relationship. When condensations are highly integrated and dependent on each other during early organogenesis, both plasticity and evolution are restricted, for example size proportions in molar tooth rows and phalanges within a digit. When similar condensations develop and remain separate (in tracheal cartilages and feather buds), they show high levels of variation and diversity in number but not in shape and size, at least at early stages. When non‐similar structures form separately and then integrate while still undergoing patterning, high levels of plasticity (in number, size, shape; in rib uncinate processes) or new dimensions of ecologically‐significant variation (cusp offset, in mammal teeth) are seen. Although each of these structural integration scenarios is unique, the modulation of evolvability is detectable and informative. Parsing the influence of structural integration at these developmental levels, rather than later‐stage structural correlations or only through genetic covariation, may be necessary to advance understanding of evolvability of the phenotype.     

The choice of model organisms in evo-devo

Study of the model organisms of developmental biology was crucial in establishing evo-devo as a new discipline. However, it has been claimed that this limited sample of organisms paints a biased picture of the role of development in evolution. Consequently, judicious choice of new model organisms is necessary to provide a more balanced picture. The challenge is to determine the best criteria for choosing new model organisms, given limited resources.     

Functional evolutionary developmental biology (evo-devo) of morphological novelties in plants

The origin of morphological and ecological novelties is a long-standing problem in evolutionary biology.Understanding these processes requires investigation from both the development and evolution standpoints,which promotes a new research field called evolutionary developmental biology (evo-devo).The fundamental mechanism for the origin of a novel structure may involve heterotopy,heterochrony,ectopic expression,or loss of an existing regulatory factor.Accordingly,the morphological and ecological traits cont...     

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.     

Embryos in evolution: evo-devo at the Naples Zoological Station in 1874

Eighteen seventy-four was a high point in evolutionary embryology. Thanks to Charles Darwin, the theory of evolution by natural selection provided a revolutionary new way of viewing the relationships and origins of organisms on Earth. Thanks to Ernst Haeckel, embryos were the way to study evolution (Haeckel in Generelle morphologie der organismen, vols 1, 2. Verlag Georg Reimer, Berlin, 1866)—it really was embryos in evolution—and recapitulation was in the air. Thanks to Anton Dohrn, a new research facility was on the ground, designed, located and structured to facilitate the study of embryos in evolution. Anton Dohrn devised, designed, financed, supervised the construction and then administered the Naples Zoological Station specifically so that researchers from all nations would have a facility where Darwin’s theory of evolution by natural selection could be tested. The zoologists who took advantage of the brand new facility within weeks of its opening late in 1873 established lines of research into evolutionary embryology, the field we now know as evolutionary developmental biology (evo-devo), the study of embryos in evolution. I examine the approach taken by Ambrosius Hubrecht, the first Dutch embryologist to undertake research at the station, and then evaluate the research of three British zoologists—E. Ray Lankester, Albert Dew-Smith, and Francis Maitland (Frank) Balfour. All four sought insights into origins, especially vertebrate origins that rested on comparative embryology, homology, germ layers, and a Darwinian approach to origins.

Molecular biology of feather morphogenesis: a testable model for evo-devo research

Darwin's theory describes the principles that are responsible for evolutionary change of organisms and their attributes. The actual mechanisms, however, need to be studied for each species and each organ separately. Here we have investigated the mechanisms underlying these principles in the avian feather. Feathers comprise one of the most complex and diverse epidermal organs as demonstrated by their shape, size, patterned arrangement and pigmentation. Variations can occur at several steps along each level of organization, leading to highly diverse forms and functions. Feathers develop gradually during ontogeny through a series of steps that may correspond to the evolutionary steps that were taken during the phylogeny from a reptilian ancestor to birds. These developmental steps include 1) the formation of feather tract fields on the skin surfaces; 2) periodic patterning of the individual feather primordia within the feather tract fields; 3) feather bud morphogenesis establishing anterio-posterior (along the cranio-caudal axis) and proximo-distal axes; 4) branching morphogenesis to create the rachis, barbs and barbules within a feather bud; and 5) gradual modulations of these basic morphological parameters within a single feather or across a feather tract. Thus, possibilities for variation in form and function of feathers occur at every developmental step. In this paper, principles guiding feather tract formation, distributions of individual feathers within the tracts and variations in feather forms are discussed at a cellular and molecular level.     

Cavefish as a model system in evolutionary developmental biology

The Mexican tetra Astyanax mexicanus has many of the favorable attributes that have made the zebrafish a model system in developmental biology. The existence of eyed surface (surface fish) and blind cave (cavefish) dwelling forms in Astyanax also provides an attractive system for studying the evolution of developmental mechanisms. The polarity of evolutionary changes and the environmental conditions leading to the cavefish phenotype are known with certainty, and several different cavefish populations have evolved constructive and regressive changes independently. The constructive changes include enhancement of the feeding apparatus (jaws, taste buds, and teeth) and the mechanosensory system of cranial neuromasts. The homeobox gene Prox 1, which is expressed in the expanded taste buds and cranial neuromasts, is one of the genes involved in the constructive changes in sensory organ development. The regressive changes include loss of pigmentation and eye degeneration. Although adult cavefish lack functional eyes, small eye primordia are formed during embryogenesis, which later arrest in development, degenerate, and sink into the orbit. Apoptosis and lens signaling to other eye parts, such as the cornea, iris, and retina, result in the arrest of eye development and ultimate optic degeneration. Accordingly, an eye with restored cornea, iris, and retinal photoreceptor cells is formed when a surface fish lens is transplanted into a cavefish optic cup, indicating that cavefish optic tissues have conserved the ability to respond to lens signaling. Genetic analysis indicates that multiple genes regulate eye degeneration, and molecular studies suggest that Pax6 may be one of the genes controlling cavefish eye degeneration. Further studies of the Astyanax system will contribute to our understanding of the evolution of developmental mechanisms in vertebrates.     

Emerging model systems in evo-devo: cavefish and microevolution of development

SUMMARY Cavefish and their conspecific surface-dwelling ancestors ( Astyanax mexicanus ) are emerging as a model system to study the microevolution of development. Here we describe attributes that make this system highly promising for such studies. We review how the Astyanax system is being used to understand evolutionary forces underlying loss of eyes and pigmentation in cavefish. Pigment regression is probably explained by neutral mutations, whereas natural selection is a likely mechanism for loss of eyes. Finally, we discuss several research frontiers in which Astyanax is poised to make significant contributions in the future: evolution of constructive traits, the craniofacial skeleton, the central nervous system, and behavior.     

Kowalevsky, comparative evolutionary embryology, and the intellectual lineage of evo-devo

Alexander Kowalevsky was one of the most significant 19th century biologists working at the intersection of evolution and embryology. The reinstatement of the Alexander Kowalevsky Medal by the St. Petersburg Society of Naturalists for outstanding contributions to understanding evolutionary relationships in the animal kingdom, evolutionary developmental biology, and comparative zoology is timely now that Evo-devo has emerged as a major research discipline in contemporary biology. Consideration of the intellectual lineage of comparative evolutionary embryology explicitly forces a reconsideration of some current conceptions of the modern emergence of Evo-devo, which has tended to exist in the shadow of experimental embryology throughout the 20th century, especially with respect to the recent success of developmental biology and developmental genetics. In particular we advocate a sharper distinction between the heritage of problems and the heritage of tools for contemporary Evo-devo. We provide brief overviews of the work of N. J. Berrill and D. T. Anderson to illustrate comparative evolutionary embryology in the 20th century, which provides an appropriate contextualization for a conceptual review of our research on the sea urchin genus Heliocidaris over the past two decades. We conclude that keeping research questions rather than experimental capabilities at the forefront of Evo-devo may be an antidote to any repeat of the stagnation experienced by the first group of evolutionary developmental biologists over one hundred years ago and acknowledges Kowalevsky's legacy in evolutionary embryology.     

Network properties, species abundance and evolution in a model of evolutionary ecology

We study the evolution of the network properties of a populated network embedded in a genotype space characterized by either a low or a high number of potential links, with particular emphasis on the connectivity and clustering. Evolution produces two distinct types of network. When a specific genotype is only able to influence a few other genotypes, the ecosystem consists of separate non-interacting clusters (i.e. isolated compartments) in genotype space. When different types may influence a large number of other sites, the network becomes one large interconnected cluster. The distribution of interaction strengths--but not the number of connections--changes significantly with time. We find that the species abundance is only realistic for a high level of species connectivity. This suggests that real ecosystems form one interconnected whole in which selection leads to stronger interactions between the different types. Analogies with niche and neutral theory and assembly models are also considered.     

An evo-devo view on the origin of the backbone: evolutionary development of the vertebrae

Vertebral columns are a group of diverse axial structures that define the vertebrates and provide supportive, locomotive, protective, and other important functions. The embryonic origin of the first vertebral element in this subphylum, the lamprey arcualia, has remained a puzzle for more than a century although much developmental and genetic progress has been made. The comparative approach is a very powerful tool for studying vertebrate morphological variation and understanding how the novel structures were generated during evolution. Here, I first briefly describe the vertebral structures and their developmental processes in major taxa, and then analyze the most recently published data on the basal vertebrates. Finally, an ontogenetic and phylogenetic origin is proposed. The lamprey may have already evolved a sclerotome, which gave rise to arcualia ontogenetically; whole genome duplications likely promoted the establishment of sclerotomal core genetic program by gene co-options.     

Experimental evolution of viruses: Microviridae as a model system

φX174 was developed as a model system for experimental studies of evolution because of its small genome size and ease of cultivation. It has been used extensively to address statistical questions about the dynamics of adaptive evolution. Molecular changes seen during experimental evolution of φX174 under a variety of conditions were compiled from 10 experiments comprising 58 lineages, where whole genomes were sequenced. A total of 667 substitutions was seen. Parallel evolution was rampant, with over 50 per cent of substitutions occurring at sites with three or more events. Comparisons of experimentally evolved sites to variation seen among wild phage suggest that at least some of the adaptive mechanisms seen in the laboratory are relevant to adaptation in nature. Elucidation of these mechanisms is aided by the availability of capsid and pro-capsid structures for φX174 and builds on years of genetic studies of the phage life history.     

Heavy metal tolerance in plants: A model evolutionary system

Evolved tolerance to toxic concentrations of heavy metals in plants inhabiting spoil heaps of mines is a well known phenomenon that has been the subject of much research in the last two decades. These plants are useful models for studying processes involved in the early stages of the speciation of edaphic endemics. Recent work has revealed the importance of several phenomena in the differentiation of tolerant populations, including natural selection, founder effects and ‘hitch-hiking’, and has demonstrated the early evolution of morphological differentiation and reproductive isolating mechanisms. Further studies of the biochemistry and molecular biology of heavy metal tolerance will help to show why some plant groups, such as Agrostis, are far more prone to evolve tolerance than others.     

Developmental evolution of sexual ornamentation: model and a test of feather growth and pigmentation

A tremendous diversity of avian color displays has stimulatednumerous studies of natural and sexual selection. Yet, the developmentalmechanisms that produce such diversification, and thus the proximatetargets of selection pressures, are rarely addressed and poorlyunderstood. In particular, because feathers are colored duringgrowth, the dynamics of feather growth play a deterministicrole in the variation in ornamentation. No study to date, however,has addressed the contribution of feather growth to the expressionof carotenoid-based ornamentation. Here, we examine the developmentalbasis of variation in ornamental feather shapes in male housefinches (Carpodacus mexicanus)—a species in which carotenoiddisplays are under strong natural and sexual selection. First,we use geometric morphometrics to partition the observed shapevariation in fully grown feathers among populations, ages, degreesof elaboration, ornamental body parts, and individuals. Second,we use a biologically informed mathematical model of feathergrowth to predict variation in shape of ornamental feathersdue to simulated growth rate, angle of helical growth of featherbarbs, initial number of barb ridges, rate of addition of newbarbs, barb diameter, and ramus-expansion angle. We find closeconcordance between among-individual variation in feather shapeand hue of entire ornament, and show that this concordance canbe attributed to a shared mechanism—growth rate of featherbarbs. Predicted differences in feather shape due to rate ofaddition of barbs and helical angle of feather growth explainedobserved variation in ornamental area both among individualsand between populations, whereas differences in helical angleof growth and the number of barbs in the feather follicle explaineddifferences in feather shape between ornamental parts and amongmales of different ages. The findings of a close associationof feather growth dynamics and overall ornamentation identifythe proximate targets of selection for elaboration of sexualdisplays. Moreover, the close association of feather growthand pigmentation not only can reinforce condition-dependencein color displays, but can also enable phenotypic and geneticaccommodation of novel pigments into plumage displays providinga mechanism for the observed concordance of within-populationdevelopmental processes and between-population diversificationof color displays.     

Heterochrony: Developmental mechanisms and evolutionary results

The concept of heterochrony, that the relative timing of ontogenetic events can shift during evolution, has been a major paradigm for understanding the role of developmental processes in evolution. In this paper we consider heterochrony from the perspective of developmental biology. Our objective is to redefine heterochrony more broadly so that the concept becomes readily applicable to the evolution of the full range of ontogenetic processes, from embryogenesis through the adult. Throughout, we stress the importance of considering heterochrony from a hierarchical perspective. Thus, we recognize that a heterochronic change at one level of organization may be the result of non-heterochronic events at an underlying level. As such, heterochrony must be studied using a combination of genetic, molecular, cellular, and morphological approaches.