Evolvability and Robustness in Color Displays: Bridging the Gap between Theory and Data

Evolution of diet-derived sexual ornaments—some of the most spectacular and diverse traits in the living world—highlights the gap between modern evolutionary theory and empirical data on the origin and inheritance of complex environment-dependent traits. Specifically, current theory offers little insight into how strong environmental contingency of diet-dependent color biosynthesis and environmental variability in precursor supply can be reconciled with extensive evolutionary elaboration, diversification, and convergence of diet-dependent displays among animal taxa. Moreover, biosynthetic pathways of diet-derived displays combine seemingly irreconcilable robustness, lability, and modularity to facilitate elaboration under variable environmental conditions. Here I show that an ontogenetic decrease in the predictability of an association between organismal and environmental components of color biosynthesis and the corresponding evolutionary transition from short-term epigenetic inheritance of peripheral biosynthetic components to genetic inheritance of the most reliable upstream components link the causes of developmental variation with the causes of inheritance in diet-derived displays. Using carotenoid-based colors as an empirical model, I outline general principles of a testable evolutionary framework of diversification and functional robustness of diet-derived displays, and suggest that such a framework provides insight into the foundational question of evolutionary biology—how to connect causes of within-generation developmental variation with causes of among-generation and among-taxa variation and thus with causes of evolution?     

Evolutionary models of extended phenotypes

A variety of theoretical models incorporate phenotypes expressed in the external environment, but a core question is whether such traits generate dynamics that alter evolution. This has proven to be a challenging and controversial proposition. However, several recent modelling frameworks provide insight: indirect genetic effect (IGE) models, niche construction models, and evolutionary feedback models. These distinct approaches converge upon the observation that gene action at a distance generates feedback that expands the range of trait values and evolutionary rates that we should expect to observe in empirical studies. Such conceptual replication provides solid evidence that traits with extended effects have important evolutionary consequences, but more empirical work is needed to evaluate the predictive power of different modelling approaches.     

The place of development in mathematical evolutionary theory

Development plays a critical role in structuring the joint offspring-parent phenotype distribution. It thus must be part of any truly general evolutionary theory. Historically, the offspring-parent distribution has often been treated in such a way as to bury the contribution of development, by distilling from it a single term, either heritability or additive genetic variance, and then working only with this term. I discuss two reasons why this approach is no longer satisfactory. First, the regression of expected offspring phenotype on parent phenotype can easily be nonlinear, and this nonlinearity can have a pronounced impact on the response to selection. Second, even when the offspring-parent regression is linear, it is nearly always a function of the environment, and the precise way that heritability covaries with the environment can have a substantial effect on adaptive evolution. Understanding these complexities of the offspring-parent distribution will require understanding of the developmental processes underlying the traits of interest. I briefly discuss how we can incorporate such complexity into formal evolutionary theory, and why it is likely to be important even for traits that are not traditionally the focus of evo-devo research. Finally, I briefly discuss a topic that is widely seen as being squarely in the domain of evo-devo: novelty. I argue that the same conceptual and mathematical framework that allows us to incorporate developmental complexity into simple models of trait evolution also yields insight into the evolution of novel traits.     

Developmental plasticity and evolution—quo vadis?

The role of developmental (phenotypic) plasticity in ecology and evolution is receiving a growing appreciation among the biologists, and many plasticity-specific concepts have become well established as part of the mainstream evolutionary biological thinking. In this essay, I posit that despite this progress several key perspectives in developmental plasticity remain remarkably traditional, and that it may be time to re-evaluate their continued usefulness in the face of the available evidence as the field looks to its future. Specifically, I discuss the utility of viewing plastic development as ultimately rooted in genes and genomes, and investigate the common notion that the environment—albeit a critical source of information—nevertheless remains passive, external to and separable from the organism responding to it. I end by highlighting conceptual and empirical opportunities that may permit developmental plasticity research to transcend its current boundaries and to continue its contributions toward a holistic and realistic understanding of organismal development and evolution.     

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.     

集合生态系统研究15年回顾与展望

集合生态系统(meta-ecosystem)由法国的Loreau教授等于2003年提出,是指"由跨生态系统边界的物质流、能量流和生物体流所连接起来的一系列生态系统的集合",是对只关注生物体(organism)迁移交换的集合种群(meta-population)和集合群落(meta-community)概念的外推,也是为了给生态系统空间异质性研究提供一个重要的分析路径,对研究和理解生态系统的结构、过程、功能和异质性具有重要意义。通过对相关文献的梳理分析,简述了集合生态系统研究的基本状况,分析了对集合生态系统概念的狭义和广义两种理解,指出了探讨集合生态系统结构的两个方向,构建了分析集合生态系统研究的六维整体框架,综述了研究集合生态系统的两类方法,探讨了经验化的集合生态系统(empirical meta-ecosystem)的3种空间结构和两种构建路径。将集合生态系统概念和理论引入流域复合生态系统(integrated watershed ecosystem)的分析,为流域生态学研究提供新的概念框架。     

Multivariate morphometrics,quantitative genetics,and neutral theory: Developing a “modern synthesis” for primate evolutionary morphology

Anthropologists are increasingly turning to explicit model‐bound evolutionary approaches for understanding the morphological diversification of humans and other primate lineages. Such evolutionary morphological analyses rely on three interconnected conceptual frameworks; multivariate morphometrics for quantifying similarity and differences among taxa, quantitative genetics for modeling the inheritance and evolution of morphology, and neutral theory for assessing the likelihood that taxon diversification is due to stochastic processes such as genetic drift. Importantly, neutral theory provides a framework for testing more parsimonious explanations for observed morphological differences before considering more complex adaptive scenarios. However, the consistency with which these concepts are applied varies considerably, which mirrors some of the theoretical obstacles faced during the “modern synthesis” of classical population genetics in the early 20th century. Here, each framework is reviewed and some potential stumbling blocks to the full conceptual integration of multivariate morphometrics, quantitative genetics, and neutral theory are considered.     

Beyond Arabidopsis. Translational biology meets evolutionary developmental biology

Developmental processes shape plant morphologies, which constitute important adaptive traits selected for during evolution. Identifying the genes that act in developmental pathways and determining how they are modified during evolution is the focus of the field of evolutionary developmental biology, or evo-devo. Knowledge of genetic pathways in the plant model Arabidopsis serves as the starting point for investigating how the toolkit of developmental pathways has been used and reused to form different plant body plans. One productive approach is to identify genes in other species that are orthologous to genes known to control developmental pathways in Arabidopsis and then determine what changes have occurred in the protein coding sequence or in the gene's expression to produce an altered morphology. A second approach relies on natural variation among wild populations or crop plants. Natural variation can be exploited to identify quantitative trait loci that underlie important developmental traits and, thus, define those genes that are responsible for adaptive changes. The possibility of applying comparative genomics approaches to Arabidopsis and related species promises profound new insights into the interplay of evolution and development.     

Phenotypic integration: studying the ecology and evolution of complex phenotypes

Phenotypic integration refers to the study of complex patterns of covariation among functionally related traits in a given organism. It has been investigated throughout the 20th century, but has only recently risen to the forefront of evolutionary ecological research. In this essay, I identify the reasons for this late flourishing of studies on integration, and discuss some of the major areas of current endeavour: the interplay of adaptation and constraints, the genetic and molecular bases of integration, the role of phenotypic plasticity, macroevolutionary studies of integration, and statistical and conceptual issues in the study of the evolution of complex phenotypes. I then conclude with a brief discussion of what I see as the major future directions of research on phenotypic integration and how they relate to our more general quest for the understanding of phenotypic evolution within the neo‐Darwinian framework. I suggest that studying integration provides a particularly stimulating and truly interdisciplinary convergence of researchers from fields as disparate as molecular genetics, developmental biology, evolutionary ecology, palaeontology and even philosophy of science.     

Sequence heterochrony and the evolution of development

One of the most persistent questions in comparative developmental biology concerns whether there are general rules by which ontogeny and phylogeny are related. Answering this question requires conceptual and analytic approaches that allow biologists to examine a wide range of developmental events in well-structured phylogenetic contexts. For evolutionary biologists, one of the most dominant approaches to comparative developmental biology has centered around the concept of heterochrony. However, in recent years the focus of studies of heterochrony largely has been limited to one aspect, changes in size and shape. I argue that this focus has restricted the kinds of questions that have been asked about the patterns of developmental change in phylogeny, which has narrowed our ability to address some of the most fundamental questions about development and evolution. Here I contrast the approaches of growth heterochrony with a broader view of heterochrony that concentrates on changes in developmental sequence. I discuss a general approach to sequence heterochrony and summarize newly emerging methods to analyze a variety of kinds of developmental change in explicit phylogenetic contexts. Finally, I summarize a series of studies on the evolution of development in mammals that use these new approaches.     

Do human ‘life history strategies’ exist?

Interest in incorporating life history research from evolutionary biology into the human sciences has grown rapidly in recent years. Two core features of this research have the potential to prove valuable in strengthening theoretical frameworks in the health and social sciences: the idea that there is a fundamental trade-off between reproduction and health; and that environmental influences are important in determining how life histories develop. However, the literature on human life histories has increasingly travelled away from its origins in biology, and become conceptually diverse. For example, there are differences of opinion between evolutionary researchers about the extent to which behavioural traits associate with life history traits to form ‘life history strategies’. Here, I review the different approaches to human life histories from evolutionary anthropologists, developmental psychologists and personality psychologists, in order to assess the evidence for human ‘life history strategies’. While there is precedent in biology for the argument that some behavioural traits, notably risk-taking behaviour, may be linked in predictable ways with life history traits, there is little theoretical or empirical justification for including a very wide range of behavioural traits in a ‘life history strategy’. Given the potential of life history approaches to provide a powerful theoretical framework for understanding human health and behaviour, I then recommend productive ways forward for the field: 1) greater focus on the life history trade-offs which underlie proposed strategies; 2) greater precision when using the language of life history theory and life history strategies; 3) collecting more empirical data, from a diverse range of populations, on linkages between life history traits, behavioural traits and the environment, including the underlying mechanisms which generate these linkages; and 4) greater integration with the social and health sciences.     

Stability of the G-matrix in a population experiencing pleiotropic mutation, stabilizing selection, and genetic drift

Abstract. Quantitative genetics theory provides a framework that predicts the effects of selection on a phenotype consisting of a suite of complex traits. However, the ability of existing theory to reconstruct the history of selection or to predict the future trajectory of evolution depends upon the evolutionary dynamics of the genetic variance-covariance matrix (G-matrix). Thus, the central focus of the emerging field of comparative quantitative genetics is the evolution of the G-matrix. Existing analytical theory reveals little about the dynamics of G, because the problem is too complex to be mathematically tractable. As a first step toward a predictive theory of G-matrix evolution, our goal was to use stochastic computer models to investigate factors that might contribute to the stability of G over evolutionary time. We were concerned with the relatively simple case of two quantitative traits in a population experiencing stabilizing selection, pleiotropic mutation, and random genetic drift. Our results show that G-matrix stability is enhanced by strong correlational selection and large effective population size. In addition, the nature of mutations at pleiotropic loci can dramatically influence stability of G. In particular, when a mutation at a single locus simultaneously changes the value of the two traits (due to pleiotropy) and these effects are correlated, mutation can generate extreme stability of G. Thus, the central message of our study is that the empirical question regarding G-matrix stability is not necessarily a general question of whether G is stable across various taxonomic levels. Rather, we should expect the G-matrix to be extremely stable for some suites of characters and unstable for others over similar spans of evolutionary time.     

The role of behavior in evolution: a search for mechanism

Behavior has been viewed as a pacemaker of evolutionary change because changes in behavior are thought to expose organisms to novel selection pressures and result in rapid evolution of morphological, life history and physiological traits. However, the idea that behavior primarily drives evolutionary change has been challenged by an alternative view of behavior as an inhibitor of evolution. According to this view, a high level of behavioral plasticity shields organisms from strong directional selection by allowing individuals to exploit new resources or move to a less stressful environment. Here, I suggest that absence of clear mechanisms underlying these hypotheses impedes empirical evaluation of behavior’s role in evolution in two ways. First, both hypotheses focus on behavioral shifts as a key step in the evolutionary process but ignore the developmental mechanisms underlying these shifts and this has fostered unwarranted assumptions about the specific types of behavioral shifts that are important for evolutionary change. Second, neither hypothesis provides a means of connecting within-individual changes in behavior to population-level processes that lead to evolutionary diversification or stasis. To resolve these issues, I incorporate developmental and evolutionary mechanisms into a conceptual framework that generates predictions about the types of behavior and types of behavioral shifts that should affect both micro and macroevolutionary processes.     

Historical and philosophical perspectives on the study of developmental bias

Throughout the recent history of research at the intersection of evolution and development, notions such as developmental constraint, evolutionary novelty, and evolvability have been prominent, but the term “developmental bias” has scarcely been used. And one may even doubt whether a unique and principled definition of bias is possible. I argue that the concept of developmental bias can still play a vital scientific role by means of setting an explanatory agenda that motivates investigation and guides the formulation of integrative explanatory frameworks. Less crucial is a definition that would classify patterns of phenotypic variation and unify variational patterns involving different traits and taxa as all being “bias.” Instead, what we should want is a concept that generates intellectual identity across various researchers, and that unites the diverse fields and approaches relevant to the study of developmental bias, from paleontology to behavioral biology. I point to some advantages of conducting research specifically under the label of “developmental bias,” compared with employing other, more common terms such as “evolvability.”     

A generalised approach to the study and understanding of adaptive evolution

Evolutionary theory has made large impacts on our understanding and management of the world, in part because it has been able to incorporate new data and new insights successfully. Nonetheless, there is currently a tension between certain biological phenomena and mainstream evolutionary theory. For example, how does the inheritance of molecular epigenetic changes fit into mainstream evolutionary theory? Is niche construction an evolutionary process? Is local adaptation via habitat choice also adaptive evolution? These examples suggest there is scope (and perhaps even a need) to broaden our views on evolution. We identify three aspects whose incorporation into a single framework would enable a more generalised approach to the understanding and study of adaptive evolution: (i) a broadened view of extended phenotypes; (ii) that traits can respond to each other; and (iii) that inheritance can be non-genetic. We use causal modelling to integrate these three aspects with established views on the variables and mechanisms that drive and allow for adaptive evolution. Our causal model identifies natural selection and non-genetic inheritance of adaptive parental responses as two complementary yet distinct and independent drivers of adaptive evolution. Both drivers are compatible with the Price equation; specifically, non-genetic inheritance of parental responses is captured by an often-neglected component of the Price equation. Our causal model is general and simplified, but can be adjusted flexibly in terms of variables and causal connections, depending on the research question and/or biological system. By revisiting the three examples given above, we show how to use it as a heuristic tool to clarify conceptual issues and to help design empirical research. In contrast to a gene-centric view defining evolution only in terms of genetic change, our generalised approach allows us to see evolution as a change in the whole causal structure, consisting not just of genetic but also of phenotypic and environmental variables.     

Developmental constraints vs. variational properties: How pattern formation can help to understand evolution and development

This article suggests that apparent disagreements between the concept of developmental constraints and neo-Darwinian views on morphological evolution can disappear by using a different conceptualization of the interplay between development and selection. A theoretical framework based on current evolutionary and developmental biology and the concepts of variational properties, developmental patterns and developmental mechanisms is presented. In contrast with existing paradigms, the approach in this article is specifically developed to compare developmental mechanisms by the morphological variation they produce and the way in which their functioning can change due to genetic variation. A developmental mechanism is a gene network, which is able to produce patterns in space though the regulation of some cell behaviour (like signalling, mitosis, apoptosis, adhesion, etc.). The variational properties of a developmental mechanism are all the pattern transformations produced under different initial and environmental conditions or IS-mutations. IS-mutations are DNA changes that affect how two genes in a network interact, while T-mutations are mutations that affect the topology of the network itself. This article explains how this new framework allows predictions not only about how pattern formation affects variation, and thus phenotypic evolution, but also about how development evolves by replacement between pattern formation mechanisms. This article presents testable inferences about the evolution of the structure of development and the phenotype under different selective pressures. That is what kind of pattern formation mechanisms, in which relative temporal order, and which kind of phenotypic changes, are expected to be found in development.     

Reduce, reuse, and recycle: developmental evolution of trait diversification

A major focus of evolutionary developmental (evo-devo) studies is to determine the genetic basis of variation in organismal form and function, both of which are fundamental to biological diversification. Pioneering work on metazoan and flowering plant systems has revealed conserved sets of genes that underlie the bauplan of organisms derived from a common ancestor. However, the extent to which variation in the developmental genetic toolkit mirrors variation at the phenotypic level is an active area of research. Here we explore evidence from the angiosperm evo-devo literature supporting the frugal use of genes and genetic pathways in the evolution of developmental patterning. In particular, these examples highlight the importance of genetic pleiotropy in different developmental modules, thus reducing the number of genes required in growth and development, and the reuse of particular genes in the parallel evolution of ecologically important traits.     

Challenges in linking trait patterns to niche differentiation

Among approaches to establish the importance of niche differentiation for species coexistence, the use of functional traits is attractive for its potential to suggest specific coexistence mechanisms. Recent studies have looked for trait patterns reflective of niche differentiation, building on a line of research with a deep but somewhat neglected history. We review the field from its foundation in limiting similarity theory in the 1960s to its resurgence in 2000s, and find the theory of trait patterning still in a stage of development. Elements still to be accounted for include environmental fluctuations, multidimensional niche space, transient dynamics, immigration, intraspecific variation, evolution and spatial scales. Recent empirical methods are better than early approaches, but still focus on patterning arising in simplistic models, and should rigorously link niche space with trait space, use informative null models, and adopt new metrics of pattern as theory develops. Because tests based on overly simplistic expectations of trait pattern are of little value, we argue that progress in the field requires theory development, which should entail exploring patterns across a set of conceptual and system‐specific models of competition along trait axes. Synthesis Traits relate to ecological performance and are easy to measure. Trait patterns can thus be a practical tool for inferring community assembly processes, and have been extensively used for this purpose. Classical trait patterning theory dates back to the 1960s, and despite heavy criticism still persists in empirical studies. Here we highlight steps needed for traits to realize their potential. These include firmly linking them to niche axes, and updating pattern expectations to consider recent results from models of niche dynamics, such as the emergence of species clusters. Further theory development should reveal whether there is a common traits‐based signature across different niche mechanisms.     

Partitioning of resources: the evolutionary genetics of sexual conflict over resource acquisition and allocation

Fitness depends on both the resources that individuals acquire and the allocation of those resources to traits that influence survival and reproduction. Optimal resource allocation differs between females and males as a consequence of their fundamentally different reproductive strategies. However, because most traits have a common genetic basis between the sexes, conflicting selection between the sexes over resource allocation can constrain the evolution of optimal allocation within each sex, and generate trade‐offs for fitness between them (i.e. ‘sexual antagonism’ or ‘intralocus sexual conflict’). The theory of resource acquisition and allocation provides an influential framework for linking genetic variation in acquisition and allocation to empirical evidence of trade‐offs between distinct life‐history traits. However, these models have not considered the emergence of trade‐offs within the context of sexual dimorphism, where they are expected to be particularly common. Here, we extend acquisition–allocation theory and develop a quantitative genetic framework for predicting genetically based trade‐offs between life‐history traits within sexes and between female and male fitness. Our models demonstrate that empirically measurable evidence of sexually antagonistic fitness variation should depend upon three interacting factors that may vary between populations: (1) the genetic variances and between‐sex covariances for resource acquisition and allocation traits, (2) condition‐dependent expression of resource allocation traits and (3) sex differences in selection on the allocation of resource to different fitness components.     

Genetics, development and evolution of adaptive pigmentation in vertebrates

The study of pigmentation has played an important role in the intersection of evolution, genetics, and developmental biology. Pigmentation's utility as a visible phenotypic marker has resulted in over 100 years of intense study of coat color mutations in laboratory mice, thereby creating an impressive list of candidate genes and an understanding of the developmental mechanisms responsible for the phenotypic effects. Variation in color and pigment patterning has also served as the focus of many classic studies of naturally occurring phenotypic variation in a wide variety of vertebrates, providing some of the most compelling cases for parallel and convergent evolution. Thus, the pigmentation model system holds much promise for understanding the nature of adaptation by linking genetic changes to variation in fitness-related traits. Here, I first discuss the historical role of pigmentation in genetics, development and evolutionary biology. I then discuss recent empirically based studies in vertebrates, which rely on these historical foundations to make connections between genotype and phenotype for ecologically important pigmentation traits. These studies provide insight into the evolutionary process by uncovering the genetic basis of adaptive traits and addressing such long-standing questions in evolutionary biology as (1) are adaptive changes predominantly caused by mutations in regulatory regions or coding regions? (2) is adaptation driven by the fixation of dominant mutations? and (3) to what extent are parallel phenotypic changes caused by similar genetic changes? It is clear that coloration has much to teach us about the molecular basis of organismal diversity, adaptation and the evolutionary process.