Neutral theory, phylogenies, and the relationship between phenotypic change and evolutionary rates

The neutral theory of molecular evolution predicts that rates of phenotypic change are largely independent from genotypic change. A recent study by Bromham et al. (2002) confirmed this expectation, finding no evidence for correlated phenotypic and molecular evolutionary rates in animals. We reevaluate this hypothesis, sampling at different taxonomic levels in plants and animals, using Bayesian inference to reconstruct phylogenetic trees and estimate rates of molecular evolution. We use independent contrasts in branch lengths to maximize the information extracted from each of the trees and nodal posterior probabilities to assess the influence of phylogenetic error. Our results indicate that in vascular plants between 2% and 11% of the variation in phenotypic rates of change can be explained by the rate of genotypic change. These results may be explained by the idea that processes that affect general evolutionary rates, such as body size, may also be expected to influence rates of morphological change.     

Global analysis of genes involved in freshwater adaptation in threespine sticklebacks (Gasterosteus aculeatus)

Examples of parallel evolution of phenotypic traits have been repeatedly demonstrated in threespine sticklebacks (Gasterosteus aculeatus) across their global distribution. Using these as a model, we performed a targeted genome scan--focusing on physiologically important genes potentially related to freshwater adaptation--to identify genetic signatures of parallel physiological evolution on a global scale. To this end, 50 microsatellite loci, including 26 loci within or close to (<6 kb) physiologically important genes, were screened in paired marine and freshwater populations from six locations across the Northern Hemisphere. Signatures of directional selection were detected in 24 loci, including 17 physiologically important genes, in at least one location. Although no loci showed consistent signatures of selection in all divergent population pairs, several outliers were common in multiple locations. In particular, seven physiologically important genes, as well as reference ectodysplasin gene (EDA), showed signatures of selection in three or more locations. Hence, although these results give some evidence for consistent parallel molecular evolution in response to freshwater colonization, they suggest that different evolutionary pathways may underlie physiological adaptation to freshwater habitats within the global distribution of the threespine stickleback.     

Rapid genome‐wide evolution in Brassica rapa populations following drought revealed by sequencing of ancestral and descendant gene pools

There is increasing evidence that evolution can occur rapidly in response to selection. Recent advances in sequencing suggest the possibility of documenting genetic changes as they occur in populations, thus uncovering the genetic basis of evolution, particularly if samples are available from both before and after selection. Here, we had a unique opportunity to directly assess genetic changes in natural populations following an evolutionary response to a fluctuation in climate. We analysed genome‐wide differences between ancestors and descendants of natural populations of Brassica rapa plants from two locations that rapidly evolved changes in multiple phenotypic traits, including flowering time, following a multiyear late‐season drought in California. These ancestor‐descendant comparisons revealed evolutionary shifts in allele frequencies in many genes. Some genes showing evolutionary shifts have functions related to drought stress and flowering time, consistent with an adaptive response to selection. Loci differentiated between ancestors and descendants (F_ST outliers) were generally different from those showing signatures of selection based on site frequency spectrum analysis (Tajima's D), indicating that the loci that evolved in response to the recent drought and those under historical selection were generally distinct. Very few genes showed similar evolutionary responses between two geographically distinct populations, suggesting independent genetic trajectories of evolution yielding parallel phenotypic changes. The results show that selection can result in rapid genome‐wide evolutionary shifts in allele frequencies in natural populations, and highlight the usefulness of combining resurrection experiments in natural populations with genomics for studying the genetic basis of adaptive evolution.     

EXPERIMENTAL EVIDENCE FOR THE EVOLUTION OF INDIRECT GENETIC EFFECTS: CHANGES IN THE INTERACTION EFFECT COEFFICIENT,PSI (Ψ), DUE TO SEXUAL SELECTION

Indirect genetics effects (IGEs)—when the genotype of one individual affects the phenotypic expression of a trait in another—may alter evolutionary trajectories beyond that predicted by standard quantitative genetic theory as a consequence of genotypic evolution of the social environment. For IGEs to occur, the trait of interest must respond to one or more indicator traits in interacting conspecifics. In quantitative genetic models of IGEs, these responses (reaction norms) are termed interaction effect coefficients and are represented by the parameter psi (Ψ). The extent to which Ψ exhibits genetic variation within a population, and may therefore itself evolve, is unknown. Using an experimental evolution approach, we provide evidence for a genetic basis to the phenotypic response caused by IGEs on sexual display traits in Drosophila serrata. We show that evolution of the response is affected by sexual but not natural selection when flies adapt to a novel environment. Our results indicate a further mechanism by which IGEs can alter evolutionary trajectories—the evolution of interaction effects themselves.     

PERSPECTIVE: FROM MUTANTS TO MECHANISMS? ASSESSING THE CANDIDATE GENE PARADIGM IN EVOLUTIONARY BIOLOGY

The generation of mutants in model organisms by geneticists and developmental biologists over the last century has occasionally produced phenotypes that are startlingly reminiscent of those seen in other species. Such extreme mutations have generally been dismissed by evolutionary geneticists since the "modern synthesis" as irrelevant to adaptation and speciation. But only in recent years has information on the molecular bases of mutant phenotypes become widely available, and thus work on testing the relevance of such extreme mutations to the generation of phylogenetic diversity has just begun. Here we evaluate whether evolutionary mimics are, in fact, useful for pinpointing the genetic differences that distinguish morphological variants generated during evolution. Examples come from both plants and animals, and range from intraspecific to interordinal taxonomic ranges. The use of mutationally defined candidate genes to predict evolutionary mechanisms has so far been most fruitful in explaining intraspecific variants, where it has been effective in both plants and animals. In several cases these efforts were facilitated or supported by parallel results from quantitative trait loci studies, in which natural alleles controlling continuous variation in developmental model organisms were mapped to mutationally defined genes. However, despite these successes the approach's utility seems to rapidly decay as a function of phylogenetic distance. This suggests that the divergence of developmental genetic systems is great even in closely related organisms and may become intractable at larger distances. We discuss this result in the context of what it teaches us about development, the future prospects of the candidate gene approach, and the historical debate over process in micro- and macroevolution.     

Adaptation in the age of ecological genomics: insights from parallelism and convergence

Parallel phenotypic diversification in closely related species is a rigorous framework for testing the role of natural selection in evolution. Do parallel phenotypes always diversify by parallel genetic bases or does selection pave many alternative genomic routes to the same phenotypic ends? In this review, we show that the advent of next-generation sequencing technologies and the growing use of genomic approaches make it increasingly feasible to answer these fundamental questions using ecological and evolutionary 'non-model' populations of vertebrates in nature. While it is generally expected, and often observed, that closely related populations or species have parallel genetic bases to parallel phenotypes, exceptions are not rare and show that alternative genetic routes can result in similar phenotypes. Ultimately, this framework may illuminate the ecological conditions, evolutionary histories and genetic architectures that result in recurrent phenotypes and rapid adaptation.     

Assessing rapid evolution in a changing environment

Climate change poses a serious threat to species persistence. Effective modelling of evolutionary responses to rapid climate change is therefore essential. In this review we examine recent advances in phylogenetic comparative methods, techniques normally used to study adaptation over long periods, which allow them to be applied to the study of adaptation over shorter time scales. This increased applicability is largely due to the emergence of more flexible models of character evolution and the parallel development of molecular technologies that can be used to assess adaptive variation at loci scattered across the genome. The merging of phylogenetic and population genetic approaches to the study of adaptation has significant potential to advance our understanding of rapid responses to environmental change.     

The probability of parallel genetic evolution from standing genetic variation

Parallel evolution is often assumed to result from repeated adaptation to novel, yet ecologically similar, environments. Here, we develop and analyse a mathematical model that predicts the probability of parallel genetic evolution from standing genetic variation as a function of the strength of phenotypic selection and constraints imposed by genetic architecture. Our results show that the probability of parallel genetic evolution increases with the strength of natural selection and effective population size and is particularly likely to occur for genes with large phenotypic effects. Building on these results, we develop a Bayesian framework for estimating the strength of parallel phenotypic selection from genetic data. Using extensive individual‐based simulations, we show that our estimator is robust across a wide range of genetic and evolutionary scenarios and provides a useful tool for rigorously testing the hypothesis that parallel genetic evolution is the result of adaptive evolution. An important result that emerges from our analyses is that existing studies of parallel genetic evolution frequently rely on data that is insufficient for distinguishing between adaptive evolution and neutral evolution driven by random genetic drift. Overcoming this challenge will require sampling more populations and the inclusion of larger numbers of loci.     

Diversification on an ecologically constrained adaptive landscape

We used phylogenetic analysis of body-size ecomorphs in a crustacean species complex to gain insight into how spatial complexity of ecological processes generates and maintains biological diversity. Studies of geographically widespread species of Hyalella amphipods show that phenotypic evolution is tightly constrained in a manner consistent with adaptive responses to alternative predation regimes. A molecular phylogeny indicates that evolution of Hyalella ecomorphs is characterized by parallel evolution and by phenotypic stasis despite substantial levels of underlying molecular change. The phylogeny suggests that species diversification sometimes occurs by niche shifts, and sometimes occurs without a change in niche. Moreover, diversification in the Hyalella ecomorphs has involved the repeated evolution of similar phenotypic forms that exist in similar ecological settings, a hallmark of adaptive evolution. The evolutionary stasis observed in clades separated by substantial genetic divergence, but existing in similar habitats, is also suggestive of stabilizing natural selection acting to constrain phenotypic evolution within narrow bounds. We interpret the observed decoupling of genetic and phenotypic diversification in terms of adaptive radiation on an ecologically constrained adaptive landscape, and suggest that ecological constraints, perhaps acting together with genetic and functional constraints, may explain the parallel evolution and evolutionary stasis inferred by the phylogeny.     

When taxonomy meets genomics: lessons from a common songbird

Taxonomy is being increasingly informed by genomics. Traditionally, taxonomy has relied extensively on phenotypic traits for the identification and delimitation of species, though with a growing influence from molecular phylogenetics in recent decades. Now, genomics opens up new and more powerful tools for analysing the evolutionary history and relatedness among species, as well as understanding the genetic basis for phenotypic traits and their role in reproductive isolation. New insights gained from genomics will therefore have major effects on taxonomic classifications and species delimitation. How a genomics approach can inform a flawed taxonomy is nicely exemplified by Mason & Taylor ( 2015 ) in this issue of Molecular Ecology. They studied redpolls, which comprise a genus (Acanthis) of fringillid finches with a wide distribution in the Holarctic region, and whose species taxonomy has been a matter of much controversy for decades (Fig.  1 ). Current authoritative checklists classify them into one, two or three species, and five or six subspecies, based largely on geographical differences in phenotypic traits. Previous studies, including a recent one of the subspecies on Iceland (Amouret et al. 2015 ), have found no evidence of differentiation between these taxa in conventional molecular markers. The lack of genetic structure has been interpreted as incomplete lineage sorting among rapidly evolving lineages. Now Mason & Taylor ( 2015 ), using a large data set of genomewide SNPs, verify that they all belong to a single gene pool with a common evolutionary history, and with little or no geographical structuring. They also show that phenotypic traits used in taxonomic classifications (plumage and bill morphology) are closely associated with polygenic patterns of gene expression, presumably driven by ecological selection on a few regulatory genes. Several lessons can be learned from this study. Perhaps the most important one for taxonomy is the risk of taxonomic inflation resulting from overemphasizing phenotypic traits under local adaptation and ignoring a lack of phylogenetic signal in molecular markers.     

Correlated patterns of genetic diversity and differentiation across an avian family

Comparative studies of closely related taxa can provide insights into the evolutionary forces that shape genome evolution and the prevalence of convergent molecular evolution. We investigated patterns of genetic diversity and differentiation in stonechats (genus Saxicola), a widely distributed avian species complex with phenotypic variation in plumage, morphology and migratory behaviour, to ask whether similar genomic regions have become differentiated in independent, but closely related, taxa. We used whole‐genome pooled sequencing of 262 individuals from five taxa and found that levels of genetic diversity and divergence are strongly correlated among different stonechat taxa. We then asked whether these patterns remain correlated at deeper evolutionary scales and found that homologous genomic regions have become differentiated in stonechats and the closely related Ficedula flycatchers. Such correlation across a range of evolutionary divergence and among phylogenetically independent comparisons suggests that similar processes may be driving the differentiation of these independently evolving lineages, which in turn may be the result of intrinsic properties of particular genomic regions (e.g. areas of low recombination). Consequently, studies employing genome scans to search for areas important for reproductive isolation or adaptation should account for corresponding regions of differentiation, as these regions may not necessarily represent speciation islands or evidence of local adaptation.     

Testing the molecular and evolutionary causes of a 'leapfrog' pattern of geographical variation in coloration

Understanding the mechanisms accounting for the evolution of phenotypic diversity is central to evolutionary biology. We use molecular and phenotypic data to test hypotheses for 'leapfrog' patterns of geographical variation, in which phenotypically similar, disjunct populations are separated by distinct populations of the same species. Phylogenetic reconstructions revealed independent evolution of melanic plumage characters in different populations in the Neotropical avian genus Arremon. Thus, phenotypic similarities between distant populations cannot be explained by close phylogenetic affinity. Nor can they be attributed to recurring mutations in the MC1R gene, a locus involved in melanic pigmentation. A coalescent analysis indicates that plumage traits have become fixed at a faster rate than expected under genetic drift, suggesting that selection underlies their repeated evolution. In contrast to views that genetic drift drives phenotypic differentiation in Neotropical montane birds, our results imply that geographical variation preceding speciation may reflect the action of deterministic selective processes.     

Integration of Random Forest with population‐based outlier analyses provides insight on the genomic basis and evolution of run timing in Chinook salmon (Oncorhynchus tshawytscha)

Anadromous Chinook salmon populations vary in the period of river entry at the initiation of adult freshwater migration, facilitating optimal arrival at natal spawning. Run timing is a polygenic trait that shows evidence of rapid parallel evolution in some lineages, signifying a key role for this phenotype in the ecological divergence between populations. Studying the genetic basis of local adaptation in quantitative traits is often impractical in wild populations. Therefore, we used a novel approach, Random Forest, to detect markers linked to run timing across 14 populations from contrasting environments in the Columbia River and Puget Sound, USA. The approach permits detection of loci of small effect on the phenotype. Divergence between populations at these loci was then examined using both principle component analysis and F_ST outlier analyses, to determine whether shared genetic changes resulted in similar phenotypes across different lineages. Sequencing of 9107 RAD markers in 414 individuals identified 33 predictor loci explaining 79.2% of trait variance. Discriminant analysis of principal components of the predictors revealed both shared and unique evolutionary pathways in the trait across different lineages, characterized by minor allele frequency changes. However, genome mapping of predictor loci also identified positional overlap with two genomic outlier regions, consistent with selection on loci of large effect. Therefore, the results suggest selective sweeps on few loci and minor changes in loci that were detected by this study. Use of a polygenic framework has provided initial insight into how divergence in a trait has occurred in the wild.     

Repeated and predictable patterns of ecotypic differentiation during a biological invasion: lake–stream divergence in parapatric Swiss stickleback

The relative importance of ecological selection and geographical isolation in promoting and constraining genetic and phenotypic differentiation among populations is not always obvious. Interacting with divergent selection, restricted opportunity for gene flow may in some cases be as much a cause as a consequence of adaptation, with the latter being a hallmark of ecological speciation. Ecological speciation is well studied in parts of the native range of the three‐spined stickleback. Here, we study this process in a recently invaded part of its range. Switzerland was colonized within the past 140 years from at least three different colonization events involving different stickleback lineages. They now occupy diverse habitats, ranging from small streams to the pelagic zone of large lakes. We use replicated systems of parapatric lake and stream populations, some of which trace their origins to different invasive lineages, to ask (i) whether phenotypic divergence occurred among populations inhabiting distinct habitats, (ii) whether trajectories of phenotypic divergence follow predictable parallel patterns and (iii) whether gene flow constrains divergent adaptation or vice versa. We find consistent phenotypic divergence between populations occupying distinct habitats. This involves parallel evolution in several traits with known ecological relevance in independent evolutionary lineages. Adaptive divergence supersedes homogenizing gene flow even at a small spatial scale. We find evidence that adaptive phenotypic divergence places constraints on gene flow over and above that imposed by geographical distance, signalling the early onset of ecological speciation.     

Rapid,nonparallel genomic evolution of Brassica rapa (field mustard) under experimental drought

While we know that climate change can potentially cause rapid phenotypic evolution, our understanding of the genetic basis and degree of genetic parallelism of rapid evolutionary responses to climate change is limited. In this study, we combined the resurrection approach with an evolve-and-resequence design to examine genome-wide evolutionary changes following drought. We exposed genetically similar replicate populations of the annual plant Brassica rapa derived from a field population in southern California to four generations of experimental drought or watered conditions in a greenhouse. Genome-wide sequencing of ancestral and descendant population pools identified hundreds of SNPs that showed evidence of rapidly evolving in response to drought. Several of these were in stress response genes, and two were identified in a prior study of drought response in this species. However, almost all genetic changes were unique among experimental populations, indicating that the evolutionary changes were largely nonparallel, despite the fact that genetically similar replicates of the same founder population had experienced controlled and consistent selection regimes. This nonparallelism of evolution at the genetic level is potentially because of polygenetic adaptation allowing for multiple different genetic routes to similar phenotypic outcomes. Our findings help to elucidate the relationship between rapid phenotypic and genomic evolution and shed light on the degree of parallelism and predictability of genomic evolution to environmental change.     

Evolution of adaptive phenotypic traits without positive Darwinian selection

Recent evidence suggests the frequent occurrence of a simple non-Darwinian (but non-Lamarckian) model for the evolution of adaptive phenotypic traits, here entitled the plasticity-relaxation-mutation (PRM) mechanism. This mechanism involves ancestral phenotypic plasticity followed by specialization in one alternative environment and thus the permanent expression of one alternative phenotype. Once this specialization occurs, purifying selection on the molecular basis of other phenotypes is relaxed. Finally, mutations that permanently eliminate the pathways leading to alternative phenotypes can be fixed by genetic drift. Although the generality of the PRM mechanism is at present unknown, I discuss evidence for its widespread occurrence, including the prevalence of exaptations in evolution, evidence that phenotypic plasticity has preceded adaptation in a number of taxa and evidence that adaptive traits have resulted from loss of alternative developmental pathways. The PRM mechanism can easily explain cases of explosive adaptive radiation, as well as recently reported cases of apparent adaptive evolution over ecological time.     

Genetic and developmental basis for parallel evolution and its significance for hominoid evolution

Greater understanding of ape comparative anatomy and evolutionary history has brought a general appreciation that the hominoid radiation is characterized by substantial homoplasy.^1–4 However, little consensus has been reached regarding which features result from repeated evolution. This has important implications for reconstructing ancestral states throughout hominoid evolution, including the nature of the Pan‐Homo last common ancestor (LCA). Advances from evolutionary developmental biology (evo‐devo) have expanded the diversity of model organisms available for uncovering the morphogenetic mechanisms underlying instances of repeated phenotypic change. Of particular relevance to hominoids are data from adaptive radiations of birds, fish, and even flies demonstrating that parallel phenotypic changes often use similar genetic and developmental mechanisms. The frequent reuse of a limited set of genes and pathways underlying phenotypic homoplasy suggests that the conserved nature of the genetic and developmental architecture of animals can influence evolutionary outcomes. Such biases are particularly likely to be shared by closely related taxa that reside in similar ecological niches and face common selective pressures. Consideration of these developmental and ecological factors provides a strong theoretical justification for the substantial homoplasy observed in the evolution of complex characters and the remarkable parallel similarities that can occur in closely related taxa. Thus, as in other branches of the hominoid radiation, repeated phenotypic evolution within African apes is also a distinct possibility. If so, the availability of complete genomes for each of the hominoid genera makes them another model to explore the genetic basis of repeated evolution.     

History, chance and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection

Introduced species often exhibit changes in genetic variation, population structure, selection regime and phenotypic traits as they colonize and expand into new ranges. For these reasons, species invasions are increasingly recognized as promising systems for studying adaptive evolution over contemporary time scales. However, changes in phenotypic traits during invasion occur under non-equilibrium demographic conditions and may reflect the influences of prior evolutionary history and chance events, as well as selection. We briefly review the evidence for phenotypic evolution and the role of selection during invasion. While there is ample evidence for evolutionary change, it is less clear if selection is the primary mechanism. We then discuss the likelihood that stochastic events shift phenotypic distributions during invasion, and argue that hypotheses of adaptation should be tested against appropriate null models. We suggest two experimental frameworks for separating stochastic evolution from adaptation: statistically accounting for phenotypic variation among putative invasion sources identified by using phylogenetic or assignment methods and by comparing estimates of differentiation within and among ranges for both traits and neutral markers ( Q _ST vs. F _ST). Designs that incorporate a null expectation can reveal the role of history and chance in the evolutionary process, and provide greater insights into evolution during species invasions.     

Genetic and morphological divergence between Littorina fabalis ecotypes in Northern Europe

Low dispersal marine intertidal species facing strong divergent selective pressures associated with steep environmental gradients have a great potential to inform us about local adaptation and reproductive isolation. Among these, gastropods of the genus Littorina offer a unique system to study parallel phenotypic divergence resulting from adaptation to different habitats related with wave exposure. In this study, we focused on two Littorina fabalis ecotypes from Northern European shores and compared patterns of habitat‐related phenotypic and genetic divergence across three different geographic levels (local, regional and global). Geometric morphometric analyses revealed that individuals from habitats moderately exposed to waves usually present a larger shell size with a wider aperture than those from sheltered habitats. The phenotypic clustering of L. fabalis by habitat across most locations (mainly in terms of shell size) support an important role of ecology in morphological divergence. A genome scan based on amplified fragment length polymorphisms (AFLPs) revealed a heterogeneous pattern of differentiation across the genome between populations from the two different habitats, suggesting ecotype divergence in the presence of gene flow. The contrasting patterns of genetic structure between nonoutlier and outlier loci, and the decreased sharing of outlier loci with geographic distance among locations are compatible with parallel evolution of phenotypic divergence, with an important contribution of gene flow and/or ancestral variation. In the future, model‐based inference studies based on sequence data across the entire genome will help unravelling these evolutionary hypotheses, improving our knowledge about adaptation and its influence on diversification within the marine realm.     

TRANSLATING BETWEEN MICROEVOLUTIONARY PROCESS AND MACROEVOLUTIONARY PATTERNS: THE CORRELATION STRUCTURE OF INTERSPECIFIC DATA

As species evolve along a phylogenetic tree, we expect closely related species to retain some phenotypic similarities due to their shared evolutionary histories. The amount of expected similarity depends both on the hierarchical phylogenetic structure, and on the specific magnitude and types of evolutionary changes that accumulate during each generation. In this study, we show how models of microevolutionary change can be translated into the resulting macroevolutionary patterns. We illustrate how the structure of phenotypic covariances expected in interspecific measurements can be derived, and how this structure depends on the microevolutionary forces guiding phenotypic change at each generation. We then explore the covariance structure expected from several simple microevolutionary models of phenotypic evolution, including various combinations of random genetic drift, directional selection, stabilizing selection, and environmental change, as well as models of punctuated or burst-like evolution. We find that stabilizing selection leads to patterns of exponential decrease of between species covariance with phylogenetic distance. This is different from the usual linear patterns of decrease assumed in most comparative and systematic methods. Nevertheless, linear patterns of decrease can result from many processes in addition to random genetic drift, such as directional and fluctuating selection as well as modes of punctuated change. Our framework can be used to develop methods for (1) phylogenetic reconstruction; (2) inference of the evolutionary process from comparative data; and (3) conducting or evaluating statistical analyses of comparative data while taking phylogenetic history into account.