An end to endless forms: epistasis, phenotype distribution bias, and nonuniform evolution

Studies of the evolution of development characterize the way in which gene regulatory dynamics during ontogeny constructs and channels phenotypic variation. These studies have identified a number of evolutionary regularities: (1) phenotypes occupy only a small subspace of possible phenotypes, (2) the influence of mutation is not uniform and is often canalized, and (3) a great deal of morphological variation evolved early in the history of multicellular life. An important implication of these studies is that diversity is largely the outcome of the evolution of gene regulation rather than the emergence of new, structural genes. Using a simple model that considers a generic property of developmental maps-the interaction between multiple genetic elements and the nonlinearity of gene interaction in shaping phenotypic traits-we are able to recover many of these empirical regularities. We show that visible phenotypes represent only a small fraction of possibilities. Epistasis ensures that phenotypes are highly clustered in morphospace and that the most frequent phenotypes are the most similar. We perform phylogenetic analyses on an evolving, developmental model and find that species become more alike through time, whereas higher-level grades have a tendency to diverge. Ancestral phenotypes, produced by early developmental programs with a low level of gene interaction, are found to span a significantly greater volume of the total phenotypic space than derived taxa. We suggest that early and late evolution have a different character that we classify into micro- and macroevolutionary configurations. These findings complement the view of development as a key component in the production of endless forms and highlight the crucial role of development in constraining biotic diversity and evolutionary trajectories.     

Rates of morphological evolution are correlated with species richness in salamanders

The tempo and mode of species diversification and phenotypic evolution vary widely across the tree of life, yet the relationship between these processes is poorly known. Previous tests of the relationship between rates of phenotypic evolution and rates of species diversification have assumed that species richness increases continuously through time. If this assumption is violated, simple phylogenetic estimates of net diversification rate may bear no relationship to processes that influence the distribution of species richness among clades. Here, we demonstrate that the variation in species richness among plethodontid salamander clades is unlikely to have resulted from simple time-dependent processes, leading to fundamentally different conclusions about the relationship between rates of phenotypic evolution and species diversification. Morphological evolutionary rates of both size and shape evolution are correlated with clade species richness, but are uncorrelated with simple estimators of net diversification that assume constancy of rates through time. This coupling between species diversification and phenotypic evolution is consistent with the hypothesis that clades with high rates of morphological trait evolution may diversify more than clades with low rates. Our results indicate that assumptions about underlying processes of diversity regulation have important consequences for interpreting macroevolutionary patterns.     

Determinants of maturation in animals

Maturation is a critical transition in the life cycle. Recent models have used retrospective analyses of patterns of variation in age and size at maturity in an attempt to understand the mechanisms responsible for generating phenotypic variation in maturation. Empirical work has revealed greater complexity in the biology of maturation than has been incorporated in current models, and has cast doubt on some of the assumptions and conclusions of the models. Recent insights from experimental work, coupled with theoretical advances for the analysis of growth, size and other complex characters, have great potential to elucidate evolution of maturation and how adaptive maturation phenotypes are achieved by real organisms.     

The multiple directions of evolutionary change

The theory of Punctuated Equilibria challenges the neo-Darwinian tenet that evolution is a uniform process. Recently, an article by Hunt has found that directional change during the evolution of a lineage is relatively small (occurring only in 5% of 250 analyzed traits). Of those traits that were shown to follow a trend, size was more likely to show gradual changes, whereas shape changes were more random. Here, we provide a short view of the nature of evolutionary trends, showing that directional change within lineages and among clades provides valuable evolutionary information about the processes involved in their generation.     

Phenotypic plasticity in development and evolution: facts and concepts

This theme issue pursues an exploration of the potential of taking into account the environmental sensitivity of development to explaining the evolution of metazoan life cycles, with special focus on complex life cycles and the role of developmental plasticity. The evolution of switches between alternative phenotypes as a response to different environmental cues and the evolution of the control of the temporal expression of alternative phenotypes within an organism''s life cycle are here treated together as different dimensions of the complex relationships between genotype and phenotype, fostering the emergence of a more general and comprehensive picture of phenotypic evolution through a quite diverse sample of case studies. This introductory article reviews fundamental facts and concepts about phenotypic plasticity, adopting the most authoritative terminology in use in the current literature. The main topics are types and components of phenotypic variation, the evolution of organismal traits through plasticity, the origin and evolution of phenotypic plasticity and its adaptive value.     

Multivariate Phenotypic Divergence Due to the Fixation of Beneficial Mutations in Experimentally Evolved Lineages of a Filamentous Fungus

The potential for evolutionary change is limited by the availability of genetic variation. Mutations are the ultimate source of new alleles, yet there have been few experimental investigations of the role of novel mutations in multivariate phenotypic evolution. Here, we evaluated the degree of multivariate phenotypic divergence observed in a long-term evolution experiment whereby replicate lineages of the filamentous fungus Aspergillus nidulans were derived from a single genotype and allowed to fix novel (beneficial) mutations while maintained at two different population sizes. We asked three fundamental questions regarding phenotypic divergence following approximately 800 generations of adaptation: (1) whether divergence was limited by mutational supply, (2) whether divergence proceeded in relatively many (few) multivariate directions, and (3) to what degree phenotypic divergence scaled with changes in fitness (i.e. adaptation). We found no evidence that mutational supply limited phenotypic divergence. Divergence also occurred in all possible phenotypic directions, implying that pleiotropy was either weak or sufficiently variable among new mutations so as not to constrain the direction of multivariate evolution. The degree of total phenotypic divergence from the common ancestor was positively correlated with the extent of adaptation. These results are discussed in the context of the evolution of complex phenotypes through the input of adaptive mutations.     

Neophenogenesis: a developmental theory of phenotypic evolution

An important task for evolutionary biology is to explain how phenotypes change over evolutionary time. Neo-Darwinian theory explains phenotypic change as the outcome of genetic change brought about by natural selection. In the neo-Darwinian account, genetic change is primary; phenotypic change is a secondary outcome that is often given no explicit consideration at all. In this article, we introduce the concept of neophenogenesis: a persistent, transgenerational change in phenotypes over evolutionary time. A theory of neophenogenesis must encompass all sources of such phenotypic change, not just genetic ones. Both genetic and extra-genetic contributions to neophenogenesis have their effect through the mechanisms of development, and developmental considerations, particularly a rejection of the commonly held distinction between inherited and acquired traits, occupy a central place in neophenogenetic theory. New phenotypes arise because of a change in the patterns of organism-environment interaction that produce development in members of a population. So long as these new patterns of developmental interaction persist, the new phenotype(s) will also persist. Although the developmental mechanisms that produce the novel phenotype may change, as in the process known as "genetic assimilation", such changes are not necessary in order for neophenogenesis to occur, because neophenogenetic theory is a theory of phenotypic, not genetic, change.     

Quantitative genetic variation in static allometry in the threespine stickleback

The common pattern of replicated evolution of a consistent shape-environment relationship might reflect selection acting in similar ways within each environment, but divergently among environments. However, phenotypic evolution depends on the availability of additive genetic variation as well as on the direction of selection, implicating a bias in the distribution of genetic variance as a potential contributor to replicated evolution. Allometry, the relationship between shape and size, is a potential source of genetic bias that is poorly understood. The threespine stickleback, Gasterosteus aculeatus, provides an ideal system for exploring the contribution of genetic variance in body shape allometry to evolutionary patterns. The stickleback system comprises marine populations that exhibit limited phenotypic variation, and young freshwater populations which, following independent colonization events, have often evolved similar phenotypes in similar environments. In particular, stickleback diversification has involved changes in both total body size and relative size of body regions (i.e., shape). In a laboratory-reared cohort derived from an oceanic Alaskan population that is phenotypically and genetically representative of the ancestor of the diverse freshwater populations in this region, we determined the phenotypic static allometry, and estimated the additive genetic variation about these population-level allometric functions. We detected significant allometry, with larger fish having relatively smaller heads, a longer base to their second dorsal fin, and longer, shallower caudal peduncles. There was additive genetic variance in body size and in size-independent body shape (i.e., allometric elevation), but typically not in allometric slopes. These results suggest that the parallel evolution of body shape in threespine stickleback is not likely to have been a correlated response to selection on body size, or vice versa. Although allometry is common in fishes, this study highlights the need for additional data on genetic variation in allometric functions to determine how allometry evolves and how it influences phenotypic evolution.     

Adaptive processes drive ecomorphological convergent evolution in antwrens (Thamnophilidae)

Phylogenetic niche conservatism (PNC) and convergence are contrasting evolutionary patterns that describe phenotypic similarity across independent lineages. Assessing whether and how adaptive processes give origin to these patterns represent a fundamental step toward understanding phenotypic evolution. Phylogenetic model‐based approaches offer the opportunity not only to distinguish between PNC and convergence, but also to determine the extent that adaptive processes explain phenotypic similarity. The Myrmotherula complex in the Neotropical family Thamnophilidae is a polyphyletic group of sexually dimorphic small insectivorous forest birds that are relatively homogeneous in size and shape. Here, we integrate a comprehensive species‐level molecular phylogeny of the Myrmotherula complex with morphometric and ecological data within a comparative framework to test whether phenotypic similarity is described by a pattern of PNC or convergence, and to identify evolutionary mechanisms underlying body size and shape evolution. We show that antwrens in the Myrmotherula complex represent distantly related clades that exhibit adaptive convergent evolution in body size and divergent evolution in body shape. Phenotypic similarity in the group is primarily driven by their tendency to converge toward smaller body sizes. Differences in body size and shape across lineages are associated to ecological and behavioral factors.     

How fast is fast? Eco‐evolutionary dynamics and rates of change in populations and phenotypes

It is increasingly recognized that evolution may occur in ecological time. It is not clear, however, how fast evolution – or phenotypic change more generally – may be in comparison with the associated ecology, or whether systems with fast ecological dynamics generally have relatively fast rates of phenotypic change. We developed a new dataset on standardized rates of change in population size and phenotypic traits for a wide range of species and taxonomic groups. We show that rates of change in phenotypes are generally no more than 2/3, and on average about 1/4, the concurrent rates of change in population size. There was no relationship between rates of population change and rates of phenotypic change across systems. We also found that the variance of both phenotypic and ecological rates increased with the mean across studies following a power law with an exponent of two, while temporal variation in phenotypic rates was lower than in ecological rates. Our results are consistent with the view that ecology and evolution may occur at similar time scales, but clarify that only rarely do populations change as fast in traits as they do in abundance.     

Complex life cycles drive community assembly through immigration and adaptive diversification

Most animals undergo ontogenetic niche shifts during their life. Yet, standard ecological theory builds on models that ignore this complexity. Here, we study how complex life cycles, where juvenile and adult individuals each feed on different sets of resources, affect community richness. Two different modes of community assembly are considered: gradual adaptive evolution and immigration of new species with randomly selected phenotypes. We find that under gradual evolution complex life cycles can lead to both higher and lower species richness when compared to a model of species with simple life cycles that lack an ontogenetic niche shift. Thus, complex life cycles do not per se increase the scope for gradual adaptive diversification. However, complex life cycles can lead to significantly higher species richness when communities are assembled trough immigration, as immigrants can occupy isolated peaks of the dynamic fitness landscape that are not accessible via gradual evolution.     

THE EVOLUTION OF PHENOTYPIC CORRELATIONS AND “DEVELOPMENTAL MEMORY”

Development introduces structured correlations among traits that may constrain or bias the distribution of phenotypes produced. Moreover, when suitable heritable variation exists, natural selection may alter such constraints and correlations, affecting the phenotypic variation available to subsequent selection. However, exactly how the distribution of phenotypes produced by complex developmental systems can be shaped by past selective environments is poorly understood. Here we investigate the evolution of a network of recurrent nonlinear ontogenetic interactions, such as a gene regulation network, in various selective scenarios. We find that evolved networks of this type can exhibit several phenomena that are familiar in cognitive learning systems. These include formation of a distributed associative memory that can “store” and “recall” multiple phenotypes that have been selected in the past, recreate complete adult phenotypic patterns accurately from partial or corrupted embryonic phenotypes, and “generalize” (by exploiting evolved developmental modules) to produce new combinations of phenotypic features. We show that these surprising behaviors follow from an equivalence between the action of natural selection on phenotypic correlations and associative learning, well‐understood in the context of neural networks. This helps to explain how development facilitates the evolution of high‐fitness phenotypes and how this ability changes over evolutionary time.     

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.     

Variations in stress sensitivity and genomic expression in diverse S. cerevisiae isolates

Interactions between an organism and its environment can significantly influence phenotypic evolution. A first step toward understanding this process is to characterize phenotypic diversity within and between populations. We explored the phenotypic variation in stress sensitivity and genomic expression in a large panel of Saccharomyces strains collected from diverse environments. We measured the sensitivity of 52 strains to 14 environmental conditions, compared genomic expression in 18 strains, and identified gene copy-number variations in six of these isolates. Our results demonstrate a large degree of phenotypic variation in stress sensitivity and gene expression. Analysis of these datasets reveals relationships between strains from similar niches, suggests common and unique features of yeast habitats, and implicates genes whose variable expression is linked to stress resistance. Using a simple metric to suggest cases of selection, we found that strains collected from oak exudates are phenotypically more similar than expected based on their genetic diversity, while sake and vineyard isolates display more diverse phenotypes than expected under a neutral model. We also show that the laboratory strain S288c is phenotypically distinct from all of the other strains studied here, in terms of stress sensitivity, gene expression, Ty copy number, mitochondrial content, and gene-dosage control. These results highlight the value of understanding the genetic basis of phenotypic variation and raise caution about using laboratory strains for comparative genomics.     

What is wrong with absolute individual fitness?

One of the most basic facts about evolution is that fitness is a relative concept. It does not matter how well an organism survives and reproduces, only that it does so better than other organisms bearing alternative traits. Nevertheless, many evolutionary arguments are framed in terms of absolute individual fitness. The absolute fitness criterion (AFC) can be justified in terms of relative fitness only given certain assumptions that are frequently violated in nature. In particular, interactions must occur in groups that are randomly formed and phenotypic variation among groups must be tightly coupled to genetic variation. Complicating the genotype-phenotype relationship can cause phenotypic variation among groups to become nonrandom, even when the groups are randomly formed, favoring traits that do not maximize absolute individual fitness. Complex genotype-phenotype relationships and complex population structures require explicit models of evolutionary change based on relative fitness differences within and among groups.     

Evolution of complex dynamics in spatially structured populations

Dynamics of populations depend on demographic parameters which may change during evolution. In simple ecological models given by one-dimensional difference equations, the evolution of demographic parameters generally leads to equilibrium population dynamics. Here we show that this is not true in spatially structured ecological models. Using a multi-patch metapopulation model, we study the evolutionary dynamics of phenotypes that differ both in their response to local crowding, i.e. in their competitive behaviour within a habitat, and in their rate of dispersal between habitats. Our simulation results show that evolution can favour phenotypes that have the intrinsic potential for very complex dynamics provided that the environment is spatially structured and temporally variable. These phenotypes owe their evolutionary persistence to their large dispersal rates. They typically coexist with phenotypes that have low dispersal rates and that exhibit equilibrium dynamics when alone. This coexistence is brought about through the phenomenon of evolutionary branching, during which an initially uniform population splits into the two phenotypic classes.     

MODELING PHENOTYPIC PLASTICITY IN GROWTH TRAJECTORIES: A STATISTICAL FRAMEWORK

Phenotypic plasticity, that is multiple phenotypes produced by a single genotype in response to environmental change, has been thought to play an important role in evolution and speciation. Historically, knowledge about phenotypic plasticity has resulted from the analysis of static traits measured at a single time point. New insight into the adaptive nature of plasticity can be gained by an understanding of how organisms alter their developmental processes in a range of environments. Recent advances in statistical modeling of functional data and developmental genetics allow us to construct a dynamic framework of plastic response in developmental form and pattern. Under this framework, development, genetics, and evolution can be synthesized through statistical bridges to better address how evolution results from phenotypic variation in the process of development via genetic alterations.     

The evolutionary genetics of canalization

Evolutionary genetics has recently made enormous progress in understanding how genetic variation maps into phenotypic variation. However why some traits are phenotypically invariant despite apparent genetic and environmental changes has remained a major puzzle. In the 1940s, Conrad Hal Waddington coined the concept and term "canalization" to describe the robustness of phenotypes to perturbation; a similar concept was proposed by Waddington's contemporary Ivan Ivanovich Schmalhausen. This paper reviews what has been learned about canalization since Waddington. Canalization implies that a genotype's phenotype remains relatively invariant when individuals of a particular genotype are exposed to different environments (environmental canalization) or when individuals of the same single- or multilocus genotype differ in their genetic background (genetic canalization). Consequently, genetic canalization can be viewed as a particular kind of epistasis, and environmental canalization and phenotypic plasticity are two aspects of the same phenomenon. Canalization results in the accumulation of phenotypically cryptic genetic variation, which can be released after a "decanalizing" event. Thus, canalized genotypes maintain a cryptic potential for expressing particular phenotypes, which are only uncovered under particular decanalizing environmental or genetic conditions. Selection may then act on this newly released genetic variation. The accumulation of cryptic genetic variation by canalization may therefore increase evolvability at the population level by leading to phenotypic diversification under decanalizing conditions. On the other hand, under canalizing conditions, a major part of the segregating genetic variation may remain phenotypically cryptic; canalization may therefore, at least temporarily, constrain phenotypic evolution. Mechanistically, canalization can be understood in terms of transmission patterns, such as epistasis, pleiotropy, and genotype by environment interactions, and in terms of genetic redundancy, modularity, and emergent properties of gene networks and biochemical pathways. While different forms of selection can favor canalization, the requirements for its evolution are typically rather restrictive. Although there are several methods to detect canalization, there are still serious problems with unambiguously demonstrating canalization, particularly its adaptive value.     

Synthetic circuits reveal how mechanisms of gene regulatory networks constrain evolution

Phenotypic variation is the raw material of adaptive Darwinian evolution. The phenotypic variation found in organismal development is biased towards certain phenotypes, but the molecular mechanisms behind such biases are still poorly understood. Gene regulatory networks have been proposed as one cause of constrained phenotypic variation. However, most pertinent evidence is theoretical rather than experimental. Here, we study evolutionary biases in two synthetic gene regulatory circuits expressed in Escherichia coli that produce a gene expression stripe—a pivotal pattern in embryonic development. The two parental circuits produce the same phenotype, but create it through different regulatory mechanisms. We show that mutations cause distinct novel phenotypes in the two networks and use a combination of experimental measurements, mathematical modelling and DNA sequencing to understand why mutations bring forth only some but not other novel gene expression phenotypes. Our results reveal that the regulatory mechanisms of networks restrict the possible phenotypic variation upon mutation. Consequently, seemingly equivalent networks can indeed be distinct in how they constrain the outcome of further evolution.