The developmental renaissance in adaptationism

From an adaptation perspective, unoccupied patches of morphological space are inferred to be empty because they are of low fitness and selected against. These inferences hinge on venturesome assumptions, because emptiness is explained by low fitness and low fitness is inferred from emptiness. Moreover, non-adaptive factors, such as developmental constraint, could also plausibly account for empty morphospace. In response, biologists increasingly study ontogeny to test the assumption that unobserved phenotypes could be produced if selection were to favor them; finding that empty space morphologies can be readily produced in development helps reject constraint and lends support to adaptive hypotheses. This developmental approach to adaptation calls on manifold techniques, including embryology, artificial selection and comparative methods. Belying their diversity, all of these methods examine the causes of empty morphospace and mark a return of development, long excluded from traditional evolutionary biology, to adaptationist practice.     

Integrating ecology and developmental biology to explain the timing of frog metamorphosis

Amphibian metamorphosis has long intrigued ecologists and developmental biologists, yet the two research programs have progressed separately and toward different goals. Plasticity in metamorphic timing has profound effects on fitness, which has prompted ecologists to develop and test models for predicting how environmental factors affect the size and age of metamorphosis. These models rely upon untested assumptions about the mechanisms for regulating growth and development. Whereas developmental biologists explicitly investigate these mechanisms at the hormonal and genetic levels, they largely ignore the role of environmental input. Recent developments in our understanding of the molecular biology of frog metamorphosis are revealing how these two research programs could be integrated. Here, I review these developments to test ecologists' assumptions about frog metamorphosis, and to present strategies for both research fields to investigate the mechanistic basis of metamorphic plasticity.     

Costing reproduction

The placing of animal behaviour in an evolutionary context is one of the great achievements of biologists in the last century. Life history theory has been a powerful tool in explaining both adaptation and constraint in phenotypic evolution, but rarely addresses the mechanistic bases of the traits it discusses. Recent advances in molecular biology have begun to uncover these mechanisms, and provide a challenge to the traditional view that life history trade-offs are the result of the differential allocation of limiting resources. In particular, costs of reproduction in Caenorhabditis elegans appear to arise from molecular signals, which have been claimed to be arbitrary with respect to fitness. We review the evidence that costs of reproduction in C. elegans are not resource based, and find that this is not necessarily the case. However, we welcome the challenge to traditional thinking, and suggest that integrating an understanding of mechanisms into life history theory will be one of the most exciting tasks facing evolutionary biologists in the 21st century. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Developmental capacitance, genetic accommodation, and adaptive evolution

The concept of genetic accommodation remains controversial, in part because it remains unclear whether evolution by genetic accommodation forces a revolution, or merely a shift in emphasis, in our understanding of how evolution produces adaptive new traits. Here I outline a perspective that largely favors the latter view. I argue that evolution by genetic accommodation can easily be integrated into traditional evolutionary concepts. At the same time, evolution by genetic accommodation invites novel empirical and theoretical approaches that may allow biologists to push the boundaries of our current understanding of the process of evolution and to solve some long-standing controversies. Specifically, I discuss the role of developmental mechanisms as natural, and likely ubiquitous, capacitors of cryptic genetic variation, and the role of environmental perturbations as mechanisms by which such variation can become visible to selection on an individual to population-wide scale. I argue that in combination, developmental capacitance and large-scale environmental perturbations have the potential to facilitate rapid evolution including the origin of novel adaptive features while circumventing otherwise powerful genetic and population-biological constraints on adaptive evolution. I end by highlighting several promising avenues for future empirical research to explore the mechanisms and significance of evolution by genetic accommodation.     

The Evolution of Language: A Comparative Review

For many years the evolution of language has been seen as a disreputable topic, mired in fanciful “just so stories” about language origins. However, in the last decade a new synthesis of modern linguistics, cognitive neuroscience and neo-Darwinian evolutionary theory has begun to make important contributions to our understanding of the biology and evolution of language. I review some of this recent progress, focusing on the value of the comparative method, which uses data from animal species to draw inferences about language evolution. Discussing speech first, I show how data concerning a wide variety of species, from monkeys to birds, can increase our understanding of the anatomical and neural mechanisms underlying human spoken language, and how bird and whale song provide insights into the ultimate evolutionary function of language. I discuss the “descended larynx” of humans, a peculiar adaptation for speech that has received much attention in the past, which despite earlier claims is not uniquely human. Then I will turn to the neural mechanisms underlying spoken language, pointing out the difficulties animals apparently experience in perceiving hierarchical structure in sounds, and stressing the importance of vocal imitation in the evolution of a spoken language. Turning to ultimate function, I suggest that communication among kin (especially between parents and offspring) played a crucial but neglected role in driving language evolution. Finally, I briefly discuss phylogeny, discussing hypotheses that offer plausible routes to human language from a non-linguistic chimp-like ancestor. I conclude that comparative data from living animals will be key to developing a richer, more interdisciplinary understanding of our most distinctively human trait: language.     

Convergence, adaptation, and constraint

Convergent evolution of similar phenotypic features in similar environmental contexts has long been taken as evidence of adaptation. Nonetheless, recent conceptual and empirical developments in many fields have led to a proliferation of ideas about the relationship between convergence and adaptation. Despite criticism from some systematically minded biologists, I reaffirm that convergence in taxa occupying similar selective environments often is the result of natural selection. However, convergent evolution of a trait in a particular environment can occur for reasons other than selection on that trait in that environment, and species can respond to similar selective pressures by evolving nonconvergent adaptations. For these reasons, studies of convergence should be coupled with other methods-such as direct measurements of selection or investigations of the functional correlates of trait evolution-to test hypotheses of adaptation. The independent acquisition of similar phenotypes by the same genetic or developmental pathway has been suggested as evidence of constraints on adaptation, a view widely repeated as genomic studies have documented phenotypic convergence resulting from change in the same genes, sometimes even by the same mutation. Contrary to some claims, convergence by changes in the same genes is not necessarily evidence of constraint, but rather suggests hypotheses that can test the relative roles of constraint and selection in directing phenotypic evolution.     

Exploring the correlations between sequence evolution rate and phenotypic divergence across the Mammalian tree provides insights into adaptive evolution

Sequence evolution behaves in a relatively consistent manner, leading to one of the fundamental paradigms in biology, the existence of a ??molecular clock??. The molecular clock can be distilled to the concept of accumulation of substitutions, through time yielding a stable rate from which we can estimate lineage divergence. Over the last 50?years, evolutionary biologists have obtained an in-depth understanding of this clock??s nuances. It has been fine-tuned by taking into account the vast heterogeneity in rates across lineages and genes, leading to ??relaxed?? molecular clock methods for timetree reconstruction. Sequence rate varies with life history traits including body size, generation time and metabolic rate, and we review recent studies on this topic. However, few studies have explicitly examined correlates between molecular evolution and morphological evolution. The patterns observed across diverse lineages suggest that rates of molecular and morphological evolution are largely decoupled. We discuss how identifying the molecular mechanisms behind rapid functional radiations are central to understanding evolution. The vast functional divergence within mammalian lineages that have relatively ??slow?? sequence evolution refutes the hypotheses that pulses in diversification yielding major phenotypic change are the result of steady accumulation of substitutions. Patterns rather suggest phenotypic divergence is likely caused by regulatory alterations mediated through mechanisms such as insertions/deletions in functional regions. These can rapidly arise and sweep to fixation faster than predicted from a lineage??s sequence neutral substitution rate, enabling species to leapfrog between phenotypic ??islands??. We suggest research directions that could illuminate mechanisms behind the functional diversity we see today.     

The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes

The question of how genetic variation translates into organismal diversity has puzzled biologists for decades. Despite recent advances in evolutionary and developmental genetics, the mechanisms that underlie adaptation, diversification and evolutionary innovation remain largely unknown. The exceptionally diverse species flocks of cichlid fishes are textbook examples of adaptive radiation and explosive speciation and emerge as powerful model systems to study the genetic basis of animal diversification. East Africa's hundreds of endemic cichlid species are akin to a natural mutagenesis screen and differ greatly not only in ecologically relevant (hence naturally selected) characters such as mouth morphology and body shape, but also in sexually selected traits such as coloration. One of the most fascinating aspects of cichlid evolution is the frequent occurrence of evolutionary parallelisms, which has led to the question whether selection alone is sufficient to produce these parallel morphologies, or whether a developmental or genetic bias has influenced the direction of diversification. Here, I review fitness-relevant traits that could be responsible for the cichlids' evolutionary success and assess whether these were shaped by sexual or natural selection. I then focus on the interaction and the relative importance of sexual vs. natural selection in cichlid evolution. Finally, I discuss what is currently known about the genes underlying the morphogenesis of adaptively relevant traits and highlight the importance of the forthcoming cichlid genomes in the quest of the genetic basis of diversification in this group.     

Changing Museum Visitors’ Conceptions of Evolution

We examined whether a single visit to an evolution exhibition contributed to conceptual change in adult (n?=?30), youth, and child (n?=?34) museum visitors?? reasoning about evolution. The exhibition included seven current research projects in evolutionary science, each focused on a different organism. To frame this study, we integrated a developmental model of visitors?? understanding of evolution, which incorporates visitors?? intuitive beliefs, with a model of free-choice learning that includes personal, sociocultural, and contextual variables. Using pre- and post-measures, we assessed how visitors?? causal explanations about biological change, drawn from three reasoning patterns (evolutionary, intuitive, and creationist), were modified as a result of visiting the exhibition. Whatever their age, background beliefs, or prior intuitive reasoning patterns, visitors significantly increased their use of explanations from the evolutionary reasoning pattern across all measures and extended this reasoning across diverse organisms. Visitors also increased their use of one intuitive reasoning pattern, need-based (goal-directed) explanations, which, we argue, may be a step toward evolutionary reasoning. Nonetheless, visitors continued to use mixed reasoning (endorsing all three reasoning patterns) in explaining biological change. The personal, socio-cultural, and contextual variables were found to be related to these reasoning patterns in predictable ways. These findings are used to examine the structure of visitors?? reasoning patterns and those aspects of the exhibition that may have contributed to the gains in museum visitors?? understanding of evolution.     

The derived FOXP2 variant of modern humans was shared with Neandertals

Although many animals communicate vocally, no extant creature rivals modern humans in language ability. Therefore, knowing when and under what evolutionary pressures our capacity for language evolved is of great interest. Here, we find that our closest extinct relatives, the Neandertals, share with modern humans two evolutionary changes in FOXP2, a gene that has been implicated in the development of speech and language. We furthermore find that in Neandertals, these changes lie on the common modern human haplotype, which previously was shown to have been subject to a selective sweep. These results suggest that these genetic changes and the selective sweep predate the common ancestor (which existed about 300,000-400,000 years ago) of modern human and Neandertal populations. This is in contrast to more recent age estimates of the selective sweep based on extant human diversity data. Thus, these results illustrate the usefulness of retrieving direct genetic information from ancient remains for understanding recent human evolution.     

Membranes,trafficking, and signaling during animal development

Molecular genetics has been key in allowing developmental biologists to uncover many of the molecules that participate in pattern formation. Cell biology is now beginning to help developmental biologists in their quest to understand how these molecules interact within cells to direct tissue behavior. This is particularly true in the areas of membrane trafficking and cell motility. Recent work has shown that various trafficking events such as secretion, endocytosis, segregation in membrane microdomains, intracellular transport, and targeting to lysosomes regulate various signaling pathways. It is likely that within the context of an embryo, these trafficking events are integrated such that secreted factors reliably orchestrate many developmental decisions.     

Life history evolution and comparative developmental biology of echinoderms

Evolutionary biologists studying life history variation have used echinoderms in experimental, laboratory, and field studies of life history evolution. This focus on echinoderms grew originally from the tradition of comparative embryology, in which echinoderms were central. The tools for obtaining and manipulating echinoderm gametes and larvae were taken directly from comparative embryological research. In addition, the comparative embryologists employed a diverse array of echinoderms, not a few model species, and this diversity has led to a broad understanding of the development, function, and evolution of echinoderm larvae. As a result, this branch of life history evolution has deep roots in comparative developmental biology of echinoderms. Here two main aspects of this relationship are reviewed. The first is a broad range of studies of fertilization biology, dispersal, population genetics, functional morphology, and asexual reproduction in which developmental biologists might take a keen interest because of the historical origins of this research in echinoderm comparative embryology. The second is a similarly broad variety of topics in life history research in which evolutionary biologists require techniques or data from developmental biology in order to make progress on understanding patterns of life history variation among echinoderm species and higher taxa. Both sets of topics provide opportunities for interaction and collaboration.     

Source-sink dynamics of virulence evolution

To understand the evolution of genetic diversity within species--bacterial and others--we must dissect the first steps of genetic adaptation to novel habitats, particularly habitats that are suboptimal for sustained growth where there is strong selection for adaptive changes. Here, we present the view that bacterial human pathogens represent an excellent model for understanding the molecular mechanisms of the adaptation of a species to alternative habitats. In particular, bacterial pathogens allow us to develop analytical methods to detect genetic adaptation using an evolutionary 'source-sink' model, with which the evolution of bacterial pathogens can be seen from the angle of continuous switching between permanent (source) and transient (sink) habitats. The source-sink model provides a conceptual framework for understanding the population dynamics and molecular mechanisms of virulence evolution.     

Evolutionary physiology at 30+: Has the promise been fulfilled?

Three decades ago, interactions between evolutionary biology and physiology gave rise to evolutionary physiology. This caused comparative physiologists to improve their research methods by incorporating evolutionary thinking. Simultaneously, evolutionary biologists began focusing more on physiological mechanisms that may help to explain constraints on and trade-offs during microevolutionary processes, as well as macroevolutionary patterns in physiological diversity. Here we argue that evolutionary physiology has yet to reach its full potential, and propose new avenues that may lead to unexpected advances. Viewing physiological adaptations in wild animals as potential solutions to human diseases offers enormous possibilities for biomedicine. New evidence of epigenetic modifications as mechanisms of phenotypic plasticity that regulate physiological traits may also arise in coming years, which may also represent an overlooked enhancer of adaptation via natural selection to explain physiological evolution. Synergistic interactions at these intersections and other areas will lead to a novel understanding of organismal biology.     

L’espèce en paléontologie : de l’utilisation du binôme linnéen chez les rongeurs fossiles (Mammalia,Rodentia)

Many species concepts have been proposed, but biologists and palaeontologists can use the same concept to interpret present and past biodiversity as well as evolution at the species level. But the present development of many disciplines creates the opportunity of reciprocal enlightenment of the pictures obtained of species according to different criteria: morphology, hybridization, and affiliation. Observations of long (geological) and short (biological, ecological) time intervals can consequently be more easily integrated. The increase in number of developmental studies is also an important event for understanding morphological evolution. In this context, the present work aims to comment on a few studies done on rodents (Rodentia, Mammalia), which successively deal with species recognition, estimation of past biodiversity, and the pictures given by fossils of morphological evolution.     

Size and shape: the developmental regulation of static allometry in insects

Among all organisms, the size of each body part or organ scales with overall body size, a phenomenon called allometry. The study of shape and form has attracted enormous interest from biologists, but the genetic, developmental and physiological mechanisms that control allometry and the proportional growth of parts have remained elusive. Recent progress in our understanding of body-size regulation provides a new synthetic framework for thinking about the mechanisms and the evolution of allometric scaling. In particular, insulin/IGF signaling, which plays major roles in longevity, diabetes and the regulation of cell, organ and body size, might also be centrally involved in regulating organismal shape. Here we review recent advances in the fields of growth regulation and endocrinology and use them to construct a developmental model of static allometry expression in insects. This model serves as the foundation for a research program that will result in a deeper understanding of the relationship between growth and form, a question that has fascinated biologists for centuries.     

Current advances in the phylogenetic reconstruction of metazoan evolution. A new paradigm for the Cambrian explosion?

The study of metazoan evolution has fascinated biologists for centuries, and it will certainly keep doing so. Recent interest on the origin of metazoan body plans, early metazoan evolution, genetic mechanisms generating disparity and diversity, molecular clock information, paleontology, and biogeochemistry is contributing to a better understanding of the current phyletic diversity. Unfortunately, the pattern of the metazoan tree of life still shows some important gaps in knowledge. It is the aim of this article to review some of the most important issues related to the inference of the metazoan tree, and point towards possible ways of solving certain obscure aspects in the history of animal evolution. A new hypothesis of the metazoan diversification during the Cambrian explosion is proposed by synthesizing ideas from phylogenetics, molecular evolution, paleontology, and developmental biology.     

Neural mirroring mechanisms and imitation in human infants

Studying human infants will increase our understanding of the nature, origins and function of neural mirroring mechanisms. Human infants are prolific imitators. Infant imitation indicates observation–execution linkages in the brain prior to language and protracted learning. Investigations of neural aspects of these linkages in human infants have focused on the sensorimotor mu rhythm in the electroencephalogram, which occurs in the alpha frequency range over central electrode sites. Recent results show that the infant mu rhythm is desynchronized during action execution as well as action observation. Current work is elucidating properties of the infant mu rhythm and how it may relate to prelinguistic action processing and social understanding. Here, we consider this neuroscience research in relation to developmental psychological theory, particularly the ‘Like-Me’ framework, which holds that one of the chief cognitive tasks of the human infant is to map the similarity between self and other. We elucidate the value of integrating neuroscience findings with behavioural studies of infant imitation, and the reciprocal benefit of examining mirroring mechanisms from an ontogenetic perspective.     

Developmental perspective on size change and allometry in evolution

The evolution of changes in body size is one of the most important patterns in the history of life. Its importance arises from both the frequency of the pattern and the biological implications of size change itself, which affects myriad aspects of an organism's structure and function through well-known scaling relationships. Yet relatively little attention has been focused on the underlying genetic and developmental controls of size change or their implications with regard to other morphological changes. Here, I review the endocrine growth axis and show that variation in several key growth-control substances, particularly growth hormone (GH) and insulin-like growth factor I (IGF I), is clearly linked to intraspecific differences in postnatal growth rates and terminal body size. I intentionally review a considerable amount of literature on nonprimate mammals because this research is vital to an understanding of the general topic. Research on human pygmies, giant transgenic mice, and other models of growth disturbances indicates that shifts in GH and/or IGF I levels not only yield the expected changes in terminal body size, but also result in simple truncations or extensions of underlying allometric patterns. These data provide a possible developmental basis for the common finding of ontogenetic scaling and coordinated transformations in series of closely related fossil or living species that differ in body size. At present, however, this must be viewed as a hypothesis that requires testing through interspecific analyses. A consideration of previous interpretations of the morphological distinctions of human pygmies and some other organisms demonstrates the novel information that a developmental perspective brings to morphological comparisons. Clearly, knowledge of the genetic and developmental controls of morphogenesis will greatly enhance our understanding of a multitude of evolutionary patterns, processes and mechanisms, for it is perturbations in these these controls that ultimately produce the raw material for evolutionary transformations.