Environmental and genetic cues in the evolution of phenotypic polymorphism

Phenotypic polymorphism is a consequence of developmental plasticity, in which the trajectories of developing organisms diverge under the influence of cues. Environmental and genetic phenotype determination are the two main categories of polymorphic development. Even though both may evolve as a response to varied environments, they are traditionally regarded as fundamentally distinct phenomena. They can however be joined into a single framework that emphasizes the parallel roles of environmental and genetic cues in phenotype determination. First, from the point of view of immediate causation, it is common that phenotypic variants can be induced either by environmental or by allelic variation, and this is referred to as gene-environment interchangeability. Second, from the point of view of adaptation, genetic cues in the form of allelic variation at polymorphic loci can play similar roles as environmental cues in providing information to the developmental system about coming selective conditions. Both types of cues can help a developing organism to fit its phenotype to selective circumstances. This perspective of information in environmental and genetic cues can produce testable hypotheses about phenotype determination, and can thus increase our understanding of the evolution of phenotypic polymorphism.     

Adaptive and nonadaptive plasticity in changing environments: Implications for sexual species with different life history strategies

Populations adapt to novel environmental conditions by genetic changes or phenotypic plasticity. Plastic responses are generally faster and can buffer fitness losses under variable conditions. Plasticity is typically modeled as random noise and linear reaction norms that assume simple one‐to‐one genotype–phenotype maps and no limits to the phenotypic response. Most studies on plasticity have focused on its effect on population viability. However, it is not clear, whether the advantage of plasticity depends solely on environmental fluctuations or also on the genetic and demographic properties (life histories) of populations. Here we present an individual‐based model and study the relative importance of adaptive and nonadaptive plasticity for populations of sexual species with different life histories experiencing directional stochastic climate change. Environmental fluctuations were simulated using differentially autocorrelated climatic stochasticity or noise color, and scenarios of directional climate change. Nonadaptive plasticity was simulated as a random environmental effect on trait development, while adaptive plasticity as a linear, saturating, or sinusoidal reaction norm. The last two imposed limits to the plastic response and emphasized flexible interactions of the genotype with the environment. Interestingly, this assumption led to (a) smaller phenotypic than genotypic variance in the population (many‐to‐one genotype–phenotype map) and the coexistence of polymorphisms, and (b) the maintenance of higher genetic variation—compared to linear reaction norms and genetic determinism—even when the population was exposed to a constant environment for several generations. Limits to plasticity led to genetic accommodation, when costs were negligible, and to the appearance of cryptic variation when limits were exceeded. We found that adaptive plasticity promoted population persistence under red environmental noise and was particularly important for life histories with low fecundity. Populations producing more offspring could cope with environmental fluctuations solely by genetic changes or random plasticity, unless environmental change was too fast.     

QUANTITATIVE GENETICS OF BRYOZOAN PHENOTYPIC EVOLUTION. II. ANALYSIS OF SELECTION AND RANDOM CHANGE IN FOSSIL SPECIES USING RECONSTRUCTED GENETIC PARAMETERS

The roles of natural selection and random genetic change in the punctuated phenotypic evolution of eight Miocene-Pliocene tropical American species of the cheilostome bryozoan Metrarabdotos are analyzed by quantitative genetic methods. Trait heritabilities and genetic covariances reconstructed by partitioning within- and among-colony phenotypic variance are similar to those previously obtained for living species of the cheilostome Stylopoma using breeding data. The hypothesis that differences in skeletal morphology between species of Metrarabdotos are entirely due to mutation and genetic drift cannot be rejected for reasonable rates of mutation maintained for periods brief enough to account for the geologically abrupt appearances of these species in the fossil record. Except for one pair of species, separated by the largest morphologic distance, directional selection acting alone would require unrealistically high rates of selective mortality to be maintained for these periods. Thus, directional selection is not strongly implicated in the divergence of Metrarabdotos species. Within species, rates of net phenotypic change are slow enough to require stabilizing selection, but mask large, relatively rapid fluctuations, all of which, however, can be attributed to chance departures from the mean phenotype by mutation and genetic drift, rather than to tracking environmental fluctuation by directional selection. The results are consistent with genetic models involving shifts between multiple adaptive peaks on which phenotypes remain more or less static through long-term stabilizing selection. Regardless of the degree to which directional selection may be involved in peak shifts, phenotypic differentiation is thus related to processes different than the pervasive stabilizing selection acting within species.     

Phenotype Ontologies and Cross-Species Analysis for Translational Research

The use of model organisms as tools for the investigation of human genetic variation has significantly and rapidly advanced our understanding of the aetiologies underlying hereditary traits. However, while equivalences in the DNA sequence of two species may be readily inferred through evolutionary models, the identification of equivalence in the phenotypic consequences resulting from comparable genetic variation is far from straightforward, limiting the value of the modelling paradigm. In this review, we provide an overview of the emerging statistical and computational approaches to objectively identify phenotypic equivalence between human and model organisms with examples from the vertebrate models, mouse and zebrafish. Firstly, we discuss enrichment approaches, which deem the most frequent phenotype among the orthologues of a set of genes associated with a common human phenotype as the orthologous phenotype, or phenolog, in the model species. Secondly, we introduce and discuss computational reasoning approaches to identify phenotypic equivalences made possible through the development of intra- and interspecies ontologies. Finally, we consider the particular challenges involved in modelling neuropsychiatric disorders, which illustrate many of the remaining difficulties in developing comprehensive and unequivocal interspecies phenotype mappings.     

Whole genome comparison of six Crocosphaera watsonii strains with differing phenotypes

Crocosphaera watsonii, a unicellular nitrogen‐fixing cyanobacterium found in oligotrophic oceans, is important in marine carbon and nitrogen cycles. Isolates of C. watsonii can be separated into at least two phenotypes with environmentally important differences, indicating possibly distinct ecological roles and niches. To better understand the evolutionary history and variation in metabolic capabilities among strains and phenotypes, this study compared the genomes of six C. watsonii strains, three from each phenotypic group, which had been isolated over several decades from multiple ocean basins. While a substantial portion of each genome was nearly identical to sequences in the other strains, a few regions were identified as specific to each strain and phenotype, some of which help explain observed phenotypic features. Overall, the small‐cell type strains had smaller genomes and a relative loss of genetic capabilities, while the large‐cell type strains were characterized by larger genomes, some genetic redundancy, and potentially increased adaptations to iron and phosphorus limitation. As such, strains with shared phenotypes were evolutionarily more closely related than those with the opposite phenotype, regardless of isolation location or date. Unexpectedly, the genome of the type‐strain for the species, C. watsonii WH8501, was quite unusual even among strains with a shared phenotype, indicating it may not be an ideal representative of the species. The genome sequences and analyses reported in this study will be important for future investigations of the proposed differences in adaptation of the two phenotypes to nutrient limitation, and to identify phenotype‐specific distributions in natural Crocosphaera populations.     

Decoupled differentiation of gene expression and coding sequence among Drosophila populations

Owing to the relevance to evolutionary theories of genotypic and phenotypic evolution, the correspondence of differentiation among natural populations in complex phenotypic traits and genetic markers has been studied extensively, and generally found to be poor. In contrast, the correspondence of differentiation among natural populations in gene expression, now often considered a genomic era proxy for the phenotype, and genetic markers, remains largely unexplored. Here, an analysis of expression and nucleotide sequence polymorphism of 106 genes in Drosophila melanogaster strains of the Cosmopolitan (M) and Zimbabwe, Africa (Z) mating races showed that differentiation of gene expression and of coding sequences, measured as QST and GST, respectively, were uncorrelated and, generally, QST > GST. However, an exploratory analysis showed that GST of the 5 prime sequences of genes was correlated with QST calculated from expression data, while GST of the coding sequences remained uncorrelated with QST. This scenario is consistent with the population differentiation at cis-regulatory regions that is decoupled from differentiation of the coding regions. However, despite evidence for selection on global levels of gene expression (deduced from QST > GST), 5 prime sequence polymorphisms generally were compatible with selective neutrality, suggesting differentiation in cis-regulated gene expression for these genes has been promoted by drift or selection too weak or too long ago to be detected, or higher organizational levels underlying the genetic architecture of expression are targets of selection. In all, this raises the question how selection on the expression changes (i.e. the phenotype) can be so obvious yet elusive at the level of the nucleotide sequence. Our contrasts between genetic differentiation of populations in expression and sequences revealed that even when genotype and phenotype can be connected the sources of variation that are the target of selection remain to be identified.     

Phenotypic variation along a cline in allozyme and karyotype frequencies, and its relationship with habitat, in the dog-whelk Nucella lapillus, L.

The dog-whelk Nucella lapillus exhibits a number of phenotypic variations and genetic polymorphisms which correlate with habitat-specific environmental pressures, especially those associated with wave action and temperature. This study investigates the relationship between genetic composition (karyotypic and electrophoretic variation) and phenotypic differentiation in N. lapillus sampled at 15 points along an 8 km stretch of coastline. Coincident clinal variation in gene frequencies and shell shape is described; they covary with differences in karyotype and also with growth. Laboratory-reared young show that differences in phenotype (shell shape and growth) are inherited. Experimental evidence is presented that specific shell shapes are adaptive under conditions of thermal stress. Together with the well-established correlations between shell shape and shore exposure, this association provides an argument for a relationship between genetic composition, phenotype and habitat in this species.     

Tests of phenotypic and genetic concordance and their application to the conservation of Panamanian golden frogs (Anura, Bufonidae)

Evolutionarily significant units (ESUs) differ in the extent to which they capture, or even consider, adaptive variation, and most such designations are based solely on neutral genetic differences that may not capture variation relevant to species' adaptabilities to changing environmental conditions. While concordant patterns of divergence among data sets (i.e. neutral and potentially non-neutral characters) can strengthen ESU designations, determining whether such criteria are met for highly variable taxa is especially challenging. This study tests whether previously defined ESUs for endangered Panamanian golden frogs (Atelopus varius and Atelopus zeteki) exhibit concordant variation among multiple phenotypic traits and mitochondrial DNA sequences, and the extent to which such divergence corresponds to environmental differences. Multivariate analyses identify phenotypic and genetic differentiation consistent with proposed ESUs and support the status of A. varius and A. zeteki as separate species. Moreover, the significant association detected between ESU co-membership and genetic similarity, which remained strong after removing the effect of geographic distance, also indicates that genetic differences are not simply due to isolation by distance. Two phenotypic characters (body size and the extent of dorsal black patterning) that differ among ESUs also co-vary with environmental differences, suggesting that to the extent that these phenotypic differences are heritable, variation may be associated with adaptive divergence. Lastly, discriminant function analyses show that the frogs can be correctly assigned to ESUs based on simultaneous analysis of multiple characters. The study confirms the merit of conserving the previously proposed golden frog ESUs as well as demonstrates the utility and feasibility of combined analyses of ecological, morphological and genetic variation in evaluating ESUs, especially for highly variable taxa.     

Habitat range and phenotypic variation in salt marsh plants

Ecologists have long speculated that species with wider environmental ranges would have broader ranges in phenotype; however, most tests of this hypothesis have involved small numbers of species and/or closely related taxa. We related phenotypic variation in twelve salt marsh plant species from six families to variation in four environmental variables using multiple regression. Within species, plant phenotype was predictably related to environmental variation. Salinity was the most common predictor of plant traits, followed by organic content, water content and elevation. Across species, regressions of single plant trait CVs on range (2 × SD) of single environmental variables were not significant and did not support the hypothesis that species occupying broad environmental ranges would have broad ranges in phenotypes. However, regression of a composite phenotypic PCA1 on a composite environmental PCA1 showed a marginally significant (P = 0.054). linear relationship for 10 species. Considering the different patterns of response across species, the lack of a relationship between variation in single phenotypic traits and single environmental variables is likely because the distantly-related taxa employed fundamentally different morphological and physiological strategies to respond to environmental stress gradients. The significant relationship between composite environmental and phenotypic variables reflects the complex nature of species phenotypic response to multivariate environmental gradients. Specifically, in this system, species increase variation in the number of leaves, but decrease variation in leaf size in response to an increase in range of salinity and decrease in range of water and organic content.     

Toxic hydrogen sulfide and dark caves: phenotypic and genetic divergence across two abiotic environmental gradients in Poecilia mexicana

Divergent natural selection drives evolutionary diversification. It creates phenotypic diversity by favoring developmental plasticity within populations or genetic differentiation and local adaptation among populations. We investigated phenotypic and genetic divergence in the livebearing fish Poecilia mexicana along two abiotic environmental gradients. These fish typically inhabit nonsulfidic surface rivers, but also colonized sulfidic and cave habitats. We assessed phenotypic variation among a factorial combination of habitat types using geometric and traditional morphometrics, and genetic divergence using quantitative and molecular genetic analyses. Fish in caves (sulfidic or not) exhibited reduced eyes and slender bodies. Fish from sulfidic habitats (surface or cave) exhibited larger heads and longer gill filaments. Common-garden rearing suggested that these morphological differences are partly heritable. Population genetic analyses using microsatellites as well as cytochrome b gene sequences indicate high population differentiation over small spatial scale and very low rates of gene flow, especially among different habitat types. This suggests that divergent environmental conditions constitute barriers to gene flow. Strong molecular divergence over short distances as well as phenotypic and quantitative genetic divergence across habitats in directions classic to fish ecomorphology suggest that divergent selection is structuring phenotypic variation in this system.     

HOW SIMILAR ARE GENETIC CORRELATION STRUCTURES? DATA FROM MICE AND RATS

An integral assumption of many models of morphometric evolution is the equality of the genetic variance-covariance structure across evolutionary time. To examine this assumption, the quantitative-genetic aspects of morphometric form are examined for eight pelvic traits in laboratory rats (Rattus norvegicus) and random-bred ICR mice (Mus musculus). In both species, all traits are significantly heritable, and there are significant phenotypic and genetic correlations among traits, although environmental correlations among the eight traits are low. The size relations among the pelvic variables are isometric. Three matrix-permutation tests are used to examine similarity of phenotypic, genetic, and environmental covariance and correlation matrices within and between species. Independent patterns of morphometric covariation and correlation arise from genetic and environmental effects within each species and from environmental effects between species. The patterns of phenotypic and genetic covariation and correlation are similar within each species, and the phenotypic and genetic correlations are also similar between these species. However, genetic covariance matrices show no significant statistical association between species. It is suggested that the assumption of equality of genetic variance-covariance structures across divergent taxa should be approached with caution.     

Molecular characterization of relatedness among colour variants of Asian Arowana (Scleropages formosus)

Morphological identification of fish taxa can sometimes prove difficult because phenotypic variation is either being affected by environmental factors, phenotypic characters are highly conserved or marker selection has been inappropriate. DNA based markers especially neutral mitochondrial DNA (mtDNA) have been used widely in recent times to provide better resolution of systematic relationships among vertebrate taxa. The Asian Arowana (Scleropages formosus) is a high value ornamental fish belonging to the family Osteoglossidae with a number of different colour variants distributed geographically across different locations around Southeast Asia. Systematic relationships among colour variants still remain unresolved. Partial sequences of the Cytochrome B (Cyt B) and DNA barcoding gene, Cytochrome C Oxidase I (COI) were used here to assess genetic relationships among colour variants and as a tool for molecular identification for differentiating among colour variants in this species. Results of the study show that in general, colour pattern shows no relationship with extent of COI or Cyt B mtDNA differentiation and so cannot be used to identify taxa. Partial sequences of the mtDNA genes were sufficient however, to identify S. formosus from a closely related species within the order Osteoglossidae.     

Genotypic variation in phenological plasticity: Reciprocal common gardens reveal adaptive responses to warmer springs but not to fall frost

Species faced with rapidly shifting environments must be able to move, adapt, or acclimate in order to survive. One mechanism to meet this challenge is phenotypic plasticity: altering phenotype in response to environmental change. Here, we investigated the magnitude, direction, and consequences of changes in two key phenology traits (fall bud set and spring bud flush) in a widespread riparian tree species, Populus fremontii. Using replicated genotypes from 16 populations from throughout the species’ thermal range, and reciprocal common gardens at hot, warm, and cool sites, we identified four major findings: (a) There are significant genetic (G), environmental (E), and GxE components of variation for both traits across three common gardens; (b) The magnitude of phenotypic plasticity is correlated with provenance climate, where trees from hotter, southern populations exhibited up to four times greater plasticity compared to the northern, frost‐adapted populations; (c) Phenological mismatches are correlated with higher mortality as the transfer distances between provenance and garden increase; and (d) The relationship between plasticity and survival depends not only on the magnitude and direction of environmental transfer, but also on the type of environmental stress (i.e., heat or freezing), and how particular traits have evolved in response to that stress. Trees transferred to warmer climates generally showed small to moderate shifts in an adaptive direction, a hopeful result for climate change. Trees experiencing cooler climates exhibited large, non‐adaptive changes, suggesting smaller transfer distances for assisted migration. This study is especially important as it deconstructs trait responses to environmental cues that are rapidly changing (e.g., temperature and spring onset) and those that are fixed (photoperiod), and that vary across the species’ range. Understanding the magnitude and adaptive nature of phenotypic plasticity of multiple traits responding to multiple environmental cues is key to guiding restoration management decisions as climate continues to change.     

Evolution of the environmental component of the phenotypic variance: stabilizing selection in changing environments and the cost of homogeneity

Quantitative traits show abundant genetic, environmental, and phenotypic variance, yet if they are subject to stabilizing selection for an optimal phenotype, both the genetic and environmental components are expected to decline. The mechanisms that determine the level and maintenance of phenotypic variance are not yet fully understood. While there has been extensive study of mechanisms maintaining genetic variability, it has generally been assumed that environmental variance is not dependent on the genotype and therefore not subject to change. However, accumulating data suggest that the environmental variance is under some degree of genetic control. In this study, it is assumed accordingly that both the genotypic value (i.e., mean phenotypic value) and the variance of phenotypic value given genotypic value depend on the genotype. Two models are investigated as potentially able to explain the protected maintenance of environmental variance of quantitative traits under stabilizing selection. One is varying environment among generations, such that both the optimal phenotype and the strength of the stabilizing selection vary between generations. The other is the cost of homogeneity, which is based on an assumption of an engineering cost of minimizing variability in development. It is shown that a small homogeneity cost is enough to maintain the observed levels of environmental variance, whereas a large amount of temporal variation in the optimal phenotype and the strength of selection would be necessary.     

Genes Confer Similar Robustness to Environmental,Stochastic, and Genetic Perturbations in Yeast

Gene inactivation often has little or no apparent consequence for the phenotype of an organism. This property—enetic (or mutational) robustness—is pervasive, and has important implications for disease and evolution, but is not well understood. Dating back to at least Waddington, it has been suggested that mutational robustness may be related to the requirement to withstand environmental or stochastic perturbations. Here I show that global quantitative data from yeast are largely consistent with this idea. Considering the effects of mutations in all nonessential genes shows that genes that confer robustness to environmental or stochastic change also buffer the effects of genetic change, and with similar efficacy. This means that selection during evolution for environmental or stochastic robustness (also referred to as canalization) may frequently have the side effect of increasing genetic robustness. A dynamic environment may therefore promote the evolution of phenotypic complexity. It also means that “hub” genes in genetic interaction (synthetic lethal) networks are generally genes that confer environmental resilience and phenotypic stability.     

The ecology of an adaptive radiation of three‐spined stickleback from North Uist,Scotland

There has been a large focus on the genetics of traits involved in adaptation, but knowledge of the environmental variables leading to adaptive changes is surprisingly poor. Combined use of environmental data with morphological and genomic data should allow us to understand the extent to which patterns of phenotypic and genetic diversity within a species can be explained by the structure of the environment. Here, we analyse the variation of populations of three‐spined stickleback from 27 freshwater lakes on North Uist, Scotland, that vary greatly in their environment, to understand how environmental and genetic constraints contribute to phenotypic divergence. We collected 35 individuals per population and 30 abiotic and biotic environmental parameters to characterize variation across lakes and analyse phenotype–environment associations. Additionally, we used RAD sequencing to estimate the genetic relationships among a subset of these populations. We found a large amount of phenotypic variation among populations, most prominently in armour and spine traits. Despite large variation in the abiotic environment, namely in ion composition, depth and dissolved organic Carbon, more phenotypic variation was explained by the biotic variables (presence of predators and density of predator and competitors), than by associated abiotic variables. Genetic structure among populations was partly geographic, with closer populations being more similar. Altogether, our results suggest that differences in body shape among stickleback populations are the result of both canalized genetic and plastic responses to environmental factors, which shape fish morphology in a predictable direction regardless of their genetic starting point.     

PHENOTYPIC PLASTICITY AND EPIGENETIC MARKING: AN ASSESSMENT OF EVIDENCE FOR GENETIC ACCOMMODATION

The relationship between genotype (which is inherited) and phenotype (the target of selection) is mediated by environmental inputs on gene expression, trait development, and phenotypic integration. Phenotypic plasticity or epigenetic modification might influence evolution in two general ways: (1) by stimulating evolutionary responses to environmental change via population persistence or by revealing cryptic genetic variation to selection, and (2) through the process of genetic accommodation, whereby natural selection acts to improve the form, regulation, and phenotypic integration of novel phenotypic variants. We provide an overview of models and mechanisms for how such evolutionary influences may be manifested both for plasticity and epigenetic marking. We point to promising avenues of research, identifying systems that can best be used to address the role of plasticity in evolution, as well as the need to apply our expanding knowledge of genetic and epigenetic mechanisms to our understanding of how genetic accommodation occurs in nature. Our review of a wide variety of studies finds widespread evidence for evolution by genetic accommodation.     

Aphid wing dimorphisms: linking environmental and genetic control of trait variation

Both genetic and environmental factors underlie phenotypic variation. While research at the interface of evolutionary and developmental biology has made excellent advances in understanding the contribution of genes to morphology, less well understood is the manner in which environmental cues are incorporated during development to influence the phenotype. Also virtually unexplored is how evolutionary transitions between environmental and genetic control of trait variation are achieved. Here, I review investigations into molecular mechanisms underlying phenotypic plasticity in the aphid wing dimorphism system. Among aphids, some species alternate between environmentally sensitive (polyphenic) and genetic (polymorphic) control of wing morph determination in their life cycle. Therefore, a traditional molecular genetic approach into understanding the genetically controlled polymorphism may provide a unique avenue into not only understanding the molecular basis of polyphenic variation in this group, but also the opportunity to compare and contrast the mechanistic basis of environmental and genetic control of similar dimorphisms.     

Moose body mass variation revisited: disentangling effects of environmental conditions and genetics

Large-scale geographical variation in phenotypic traits within species is often correlated to local environmental conditions and population density. Such phenotypic variation has recently been shown to also be influenced by genetic structuring of populations. In ungulates, large-scale geographical variation in phenotypic traits, such as body mass, has been related to environmental conditions and population density, but little is known about the genetic influences. Research on the genetic structure of moose suggests two distinct genetic lineages in Norway, structured along a north-south gradient. This corresponds with many environmental gradients, thus genetic structuring provides an additional factor affecting geographical phenotypic variation in Norwegian moose. We investigated if genetic structure explained geographical variation in body mass in Norwegian moose while accounting for environmental conditions, age and sex, and if it captured some of the variance in body mass that previously was attributed to environmental factors. Genetic structuring of moose was the most important variable in explaining the geographic variation in body mass within age and sex classes. Several environmental variables also had strong explanatory power, related to habitat diversity, environmental seasonality and winter harshness. The results suggest that environmental conditions, landscape characteristics, and genetic structure should be evaluated together when explaining large-scale patterns in phenotypic characters or life history traits. However, to better understand the role of genetic and environmental effects on phenotypic traits in moose, an extended individual-based study of variation in fitness-related characters is needed, preferably in an area of convergence between different genetic lineages.     

The Evolution of Plasticity and Nonplastic Spatial and Temporal Adaptations in the Presence of Imperfect Environmental Cues

A model for the evolution of plasticity is considered in which the phenotype, undergoing stabilizing selection, is modeled as a linear function of an environmental cue correlated with the phenotypic optimum, with the coefficients z(0) and z(1) evolving according to standard quantitative genetic theory. In contrast to previous theoretical models, as the rate of migration between demes or the rate of cyclic fluctuations in the optimum increases, the amount of plasticity z&d1;1 at equilibrium is shown to increase gradually, in part accounting for the effect of reduced nonplastic adaptation and reaching a maximum equal to the squared correlation between the environmental cue and the phenotypic optimum. Given that information available to the organism is limited, this bias of the expressed phenotype toward the global optimum is still optimal, however, in a certain decision-theoretic sense. When genetic variation in the plastic component of the trait is small so that spatial or temporal differentiation in plasticity is small, the effect of plasticity on nonplastic adaptation is to reduce the effects of variation in the phenotypic optimum by a factor 1-z&d1;1 only. Information acquisition costs and joint evolution of sensory systems are discussed.