Rugged adaptive landscapes shape a complex,sympatric radiation

Strong disruptive ecological selection can initiate speciation, even in the absence of physical isolation of diverging populations. Species evolving under disruptive ecological selection are expected to be ecologically distinct but, at least initially, genetically weakly differentiated. Strong selection and the associated fitness advantages of narrowly adapted individuals, coupled with assortative mating, are predicted to overcome the homogenizing effects of gene flow. Theoretical plausibility is, however, contrasted by limited evidence for the existence of rugged adaptive landscapes in nature. We found evidence for multiple, disruptive ecological selection regimes that have promoted divergence in the sympatric, incipient radiation of ‘sharpfin’ sailfin silverside fishes in ancient Lake Matano (Sulawesi, Indonesia). Various modes of ecological specialization have led to adaptive morphological differences between the species, and differently adapted morphs display significant but incomplete reproductive isolation. Individual fitness and variation in morphological key characters show that disruptive selection shapes a rugged adaptive landscape in this small but complex incipient lake fish radiation.     

Natural selection and the genetics of adaptation in threespine stickleback

Growing knowledge of the molecular basis of adaptation in wild populations is expanding the study of natural selection. We summarize ongoing efforts to infer three aspects of natural selection—mechanism, form and history—from the genetics of adaptive evolution in threespine stickleback that colonized freshwater after the last ice age. We tested a mechanism of selection for reduced bony armour in freshwater by tracking genotype and allele frequency changes at an underlying major locus (Ectodysplasin) in transplanted stickleback populations. We inferred disruptive selection on genotypes at the same locus in a population polymorphic for bony armour. Finally, we compared the distribution of phenotypic effect sizes of genes underlying changes in body shape with that predicted by models of adaptive peak shifts following colonization of freshwater. Studies of the effects of selection on genes complement efforts to identify the molecular basis of adaptive differences, and improve our understanding of phenotypic evolution.     

High evolutionary constraints limited adaptive responses to past climate changes in toad skulls

Interactions among traits that build a complex structure may be represented as genetic covariation and correlation. Genetic correlations may act as constraints, deflecting the evolutionary response from the direction of natural selection. We investigated the relative importance of drift, selection, and constraints in driving skull divergence in a group of related toad species. The distributional range of these species encompasses very distinct habitats with important climatic differences and the species are primarily distinguished by differences in their skulls. Some parts of the toad skull, such as the snout, may have functional relevance in reproductive ecology, detecting water cues. Thus, we hypothesized that the species skull divergence was driven by natural selection associated with climatic variation. However, given that all species present high correlations among skull traits, our second prediction was of high constraints deflecting the response to selection. We first extracted the main morphological direction that is expected to be subjected to selection by using within- and between-species covariance matrices. We then used evolutionary regressions to investigate whether divergence along this direction is explained by climatic variation between species. We also used quantitative genetics models to test for a role of random drift versus natural selection in skull divergence and to reconstruct selection gradients along species phylogeny. Climatic variables explained high proportions of between-species variation in the most selected axis. However, most evolutionary responses were not in the direction of selection, but aligned with the direction of allometric size, the dimension of highest phenotypic variance in the ancestral population. We conclude that toad species have responded to selection related to climate in their skulls, yet high evolutionary constraints dominated species divergence and may limit species responses to future climate change.     

Genetic component of flammability variation in a Mediterranean shrub

Recurrent fires impose a strong selection pressure in many ecosystems worldwide. In such ecosystems, plant flammability is of paramount importance because it enhances population persistence, particularly in non‐resprouting species. Indeed, there is evidence of phenotypic divergence of flammability under different fire regimes. Our general hypothesis is that flammability‐enhancing traits are adaptive; here, we test whether they have a genetic component. To test this hypothesis, we used the postfire obligate seeder Ulex parviflorus from sites historically exposed to different fire recurrence. We associated molecular variation in potentially adaptive loci detected with a genomic scan (using AFLP markers) with individual phenotypic variability in flammability across fire regimes. We found that at least 42% of the phenotypic variation in flammability was explained by the genetic divergence in a subset of AFLP loci. In spite of generalized gene flow, the genetic variability was structured by differences in fire recurrence. Our results provide the first field evidence supporting that traits enhancing plant flammability have a genetic component and thus can be responding to natural selection driven by fire. These results highlight the importance of flammability as an adaptive trait in fire‐prone ecosystems.     

Genetic variation in social influence on mate preferences

Patterns of phenotypic variation arise in part from plasticity owing to social interactions, and these patterns contribute, in turn, to the form of selection that shapes the variation we observe in natural populations. This proximate–ultimate dynamic brings genetic variation in social environments to the forefront of evolutionary theory. However, the extent of this variation remains largely unknown. Here, we use a member of the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae) to assess how mate preferences are influenced by genetic variation in the social environment. We used full-sibling split-families as ‘treatment’ social environments, and reared focal females alongside each treatment family, describing the mate preferences of the focal females. With this method, we detected substantial genetic variation in social influence on mate preferences. The mate preferences of focal females varied according to the treatment families along with which they grew up. We discuss the evolutionary implications of the presence of such genetic variation in social influence on mate preferences, including potential contributions to the maintenance of genetic variation, the promotion of divergence, and the adaptive evolution of social effects on fitness-related traits.     

Molecular phenotyping of maternally mediated parallel adaptive divergence within Rana arvalis and Rana temporaria

When similar selection acts on the same traits in multiple species or populations, parallel evolution can result in similar phenotypic changes, yet the underlying molecular architecture of parallel phenotypic divergence can be variable. Maternal effects can influence evolution at ecological timescales and facilitate local adaptation, but their contribution to parallel adaptive divergence is unclear. In this study, we (i) tested for variation in embryonic acid tolerance in a common garden experiment and (ii) used molecular phenotyping of egg coats to investigate the molecular basis of maternally mediated parallel adaptive divergence in two amphibian species (Rana arvalis and Rana temporaria). Our results on three R. arvalis and two R. temporaria populations show that adaptive divergence in embryonic acid tolerance is mediated via maternally derived egg coats in both species. We find extensive polymorphism in egg jelly coat glycoproteins within both species and that acid‐tolerant clutches have more negatively charged egg jelly – indicating that the glycosylation status of the jelly coat proteins is under divergent selection in acidified environments, likely due to its impact on jelly water balance. Overall, these data provide evidence for parallel mechanisms of adaptive divergence in two species. Our study highlights the importance of studying intraspecific molecular variation in egg coats and, specifically, their glycoproteins, to increase understanding of underlying forces maintaining variation in jelly coats.     

Imprints of Natural Selection Along Environmental Gradients in Phenology-Related Genes of Quercus petraea

We explored single nucleotide polymorphism (SNP) variation in candidate genes for bud burst from Quercus petraea populations sampled along gradients of latitude and altitude in Western Europe. SNP diversity was monitored for 106 candidate genes, in 758 individuals from 32 natural populations. We investigated whether SNP variation reflected the clinal pattern of bud burst observed in common garden experiments. We used different methods to detect imprints of natural selection (F_ST outlier, clinal variation at allelic frequencies, association tests) and compared the results obtained for the two gradients. F_ST outlier SNPs were found in 15 genes, 5 of which were common to both gradients. The type of selection differed between the two gradients (directional or balancing) for 3 of these 5. Clinal variations were observed for six SNPs, and one cline was conserved across both gradients. Association tests between the phenotypic or breeding values of trees and SNP genotypes identified 14 significant associations, involving 12 genes. The results of outlier detection on the basis of population differentiation or clinal variation were not very consistent with the results of association tests. The discrepancies between these approaches may reflect the different hierarchical levels of selection considered (inter- and intrapopulation selection). Finally, we obtained evidence for convergent selection (similar for gradients) and clinal variation for a few genes, suggesting that comparisons between parallel gradients could be used to screen for major candidate genes responding to natural selection in trees.     

Genomic clustering of adaptive loci during parallel evolution of an Australian wildflower

The build‐up of the phenotypic differences that distinguish species has long intrigued biologists. These differences are often inherited as stable polymorphisms that allow the cosegregation of adaptive variation within species, and facilitate the differentiation of complex phenotypes between species. It has been suggested that the clustering of adaptive loci could facilitate this process, but evidence is still scarce. Here, we used QTL analysis to study the genetic basis of phenotypic differentiation between coastal populations of the Australian wildflower Senecio lautus. We found that a genomic region consistently governs variation in several of the traits that distinguish these contrasting forms. Additionally, some of the taxon‐specific traits controlled by this QTL cluster have evolved repeatedly during the adaptation to the same habitats, suggesting that it could mediate divergence between locally adapted forms. This cluster contains footprints of divergent natural selection across the range of S. lautus, which suggests that it could have been instrumental for the rapid diversification of this species.     

Testing limits to adaptation along altitudinal gradients in rainforest Drosophila

Given that evolution can generate rapid and dramatic shifts in the ecological tolerance of a species, what prevents populations adapting to expand into new habitat at the edge of their distributions? Recent population genetic models have focused on the relative costs and benefits of migration between populations. On the one hand, migration may limit adaptive divergence by preventing local populations from matching their local selective optima. On the other hand, migration may also contribute to the genetic variance necessary to allow populations to track these changing optima. Empirical evidence for these contrasting effects of gene flow in natural situations are lacking, largely because it remains difficult to acquire. Here, we develop a way to explore theoretical models by estimating genetic divergence in traits that confer stress resistance along similar ecological gradients in rainforest Drosophila. This approach allows testing for the coupling of clinal divergence with local density, and the effects of genetic variance and the rate of change of the optimum on the response to selection. In support of a swamping effect of migration on phenotypic divergence, our data show no evidence for a cline in stress-related traits where the altitudinal gradient is steep, but significant clinal divergence where it is shallow. However, where clinal divergence is detected, sites showing trait means closer to the presumed local optimum have more genetic variation than sites with trait means distant from their local optimum. This pattern suggests that gene flow also aids a sustained response to selection.     

The costs of being male: are there sex-specific effects of uniparental mitochondrial inheritance?

Eukaryotic cells typically contain numerous mitochondria, each with multiple copies of their own genome, the mtDNA. Uniparental transmission of mitochondria, usually via the mother, prevents the mixing of mtDNA from different individuals. While on the one hand, this should resolve the potential for selection for fast-replicating mtDNA variants that reduce organismal fitness, maternal inheritance will, in theory, come with another set of problems that are specifically relevant to males. Maternal inheritance implies that the mitochondrial genome is never transmitted through males, and thus selection can target only the mtDNA sequence when carried by females. A consequence is that mtDNA mutations that confer male-biased phenotypic expression will be prone to evade selection, and accumulate. Here, we review the evidence from the ecological, evolutionary and medical literature for male specificity of mtDNA mutations affecting fertility, health and ageing. While such effects have been discovered experimentally in the laboratory, their relevance to natural populations—including the human population—remains unclear. We suggest that the existence of male expression-biased mtDNA mutations is likely to be a broad phenomenon, but that these mutations remain cryptic owing to the presence of counter-adapted nuclear compensatory modifier mutations, which offset their deleterious effects.     

The effects of sex-biased gene expression and X-linkage on rates of adaptive protein sequence evolution in Drosophila

A faster rate of adaptive evolution of X-linked genes compared with autosomal genes may be caused by the fixation of new recessive or partially recessive advantageous mutations (the Faster-X effect). This effect is expected to be largest for mutations that affect only male fitness and absent for mutations that affect only female fitness. We tested these predictions in Drosophila melanogaster by using genes with different levels of sex-biased expression and by estimating the extent of adaptive evolution of non-synonymous mutations from polymorphism and divergence data. We detected both a Faster-X effect and an effect of male-biased gene expression. There was no evidence for a strong association between the two effects—modest levels of male-biased gene expression increased the rate of adaptive evolution on both the autosomes and the X chromosome, but a Faster-X effect occurred for both unbiased genes and female-biased genes. The rate of genetic recombination did not influence the magnitude of the Faster-X effect, ruling out the possibility that it reflects less Hill–Robertson interference for X-linked genes.     

Adaptive basis of geographic variation: genetic,phenotypic and environmental differences among beach mouse populations

A major goal in evolutionary biology is to understand how and why populations differentiate, both genetically and phenotypically, as they invade a novel habitat. A classical example of adaptation is the pale colour of beach mice, relative to their dark mainland ancestors, which colonized the isolated sandy dunes and barrier islands on Florida''s Gulf Coast. However, much less is known about differentiation among the Gulf Coast beach mice, which comprise five subspecies linearly arrayed on Florida''s shoreline. Here, we test the role of selection in maintaining variation among these beach mouse subspecies at multiple levels—phenotype, genotype and the environments they inhabit. While all beach subspecies have light pelage, they differ significantly in colour pattern. These subspecies are also genetically distinct: pair-wise F_st-values range from 0.23 to 0.63 and levels of gene flow are low. However, we did not find a correlation between phenotypic and genetic distance. Instead, we find a significant association between the average ‘lightness’ of each subspecies and the brightness of the substrate it inhabits: the two most genetically divergent subspecies occupy the most similar habitats and have converged on phenotype, whereas the most genetically similar subspecies occupy the most different environments and have divergent phenotypes. Moreover, allelic variation at the pigmentation gene, Mc1r, is statistically correlated with these colour differences but not with variation at other genetic loci. Together, these results suggest that natural selection for camouflage—via changes in Mc1r allele frequency—contributes to pigment differentiation among beach mouse subspecies.     

Conserving marine biodiversity: insights from life-history trait candidate genes in Atlantic cod (Gadus morhua)

Recent technological developments have facilitated an increased focus on identifying genomic regions underlying adaptive trait variation in natural populations, and it has been advocated that this information should be important for designating population units for conservation. In marine fishes, phenotypic studies have suggested adaptation through divergence of life-history traits among natural populations, but the distribution of adaptive genetic variation in these species is still relatively poorly known. In this study, we extract information about the geographical distribution of genetic variation for 33 single nucleotide polymorphisms (SNPs) associated with life-history trait candidate genes, and compare this to variation in 70 putatively neutral SNPs in Atlantic cod (Gadus morhua). We analyse samples covering the major population complexes in the eastern Atlantic and find strong evidence for non-neutral levels and patterns of population structuring for several of the candidate gene-associated markers, including two SNPs in the growth hormone 1 gene. Thus, this study aligns with findings from phenotypic studies, providing molecular data strongly suggesting that these or closely linked genes are under selection in natural populations of Atlantic cod. Furthermore, we find that patterns of variation in outlier markers do not align with those observed at selectively neutral markers, and that outlier markers identify conservation units on finer geographical scales than those revealed when analysing only neutral markers. Accordingly, results also suggest that information about adaptive genetic variation will be useful for targeted conservation and management in this and other marine species.     

Molecular population genetics and evolution of Drosophila meiosis genes

While many functional elements of the meiotic process are well characterized in model organisms, the genetic basis of most of the natural phenotypic variation observed in meiotic pathways has not been determined. To begin to address this issue, we characterized patterns of polymorphism and divergence in the protein-coding regions of 33 genes across 31 lines of Drosophila melanogaster and 6 lines of Drosophila simulans. We sequenced genes known to be involved in chromosome segregation, recombination, DNA repair, and related heterochromatin binding. As expected, we found several of the genes to be highly conserved, consistent with purifying selection. However, a subset of genes showed patterns of polymorphism and divergence typical of other types of natural selection. Moreover, several intriguing differences between the two Drosophila lineages were evident: along the D. simulans lineage we consistently found evidence of adaptive protein evolution, whereas along the D. melanogaster lineage several loci exhibited patterns consistent with the maintenance of protein variation.     

Standing genetic variation in host preference for mutualist microbial symbionts

Many models of mutualisms show that mutualisms are unstable if hosts lack mechanisms enabling preferential associations with mutualistic symbiotic partners over exploitative partners. Despite the theoretical importance of mutualism-stabilizing mechanisms, we have little empirical evidence to infer their evolutionary dynamics in response to exploitation by non-beneficial partners. Using a model mutualism—the interaction between legumes and nitrogen-fixing soil symbionts—we tested for quantitative genetic variation in plant responses to mutualistic and exploitative symbiotic rhizobia in controlled greenhouse conditions. We found significant broad-sense heritability in a legume host''s preferential association with mutualistic over exploitative symbionts and selection to reduce frequency of associations with exploitative partners. We failed to detect evidence that selection will favour the loss of mutualism-stabilizing mechanisms in the absence of exploitation, as we found no evidence for a fitness cost to the host trait or indirect selection on genetically correlated traits. Our results show that genetic variation in the ability to preferentially reduce associations with an exploitative partner exists within mutualisms and is under selection, indicating that micro-evolutionary responses in mutualism-stabilizing traits in the face of rapidly evolving mutualistic and exploitative symbiotic bacteria can occur in natural host populations.     

Quantifying the genetic component of phenotypic variation in unpedigreed wild plants: tailoring genomic scan for within-population use

The study of adaptive genetic variation in natural populations is central to evolutionary biology. Quantitative genetics methods, however, are hardly applicable to long-lived organisms, and current knowledge on adaptive genetic variation in wild plants mostly refers to annuals and short-lived perennials. Studies on long-lived species are essential to explore possible life-history correlates of genetic variation, selection, and trait heritability. In this paper, we propose a method based on molecular markers to quantify the genetic basis of individual phenotypic differences in wild plants under natural conditions. Rather than focusing on inferring individual relatedness to estimate the heritability of phenotypic traits, we directly estimate the proportion of observed phenotypic variance that is statistically accounted for by genotypic differences between individuals. This is achieved by (i) identifying loci that are correlated across individuals with the phenotypic trait of interest by means of an amplified fragment length polymorphism (AFLP)-based explorative genomic scan, and (ii) fitting multiple regression and linear random effect models to estimate the effects of genotype, environment and genotype × environment on phenotypes. We apply this method to estimate genotypic and environmental effects on cumulative maternal fecundity in a wild population of the long-lived Viola cazorlensis monitored for 20 years. Results show that between 56–63% (depending on estimation method) of phenotypic variance in fecundity is accounted for by genotypic differences in 11 AFLP loci that are significantly related to fecundity. Genotype × environment effects accounted for 38% of fecundity variance, which may help to explain the unexpectedly high levels of genetic variance for fecundity found.     

Integrating QTL mapping and genome scans towards the characterization of candidate loci under parallel selection in the lake whitefish (Coregonus clupeaformis)

As natural selection must act on underlying genetic variation, discovering the number and location of loci under the influence of selection is imperative towards understanding adaptive divergence in evolving populations. Studies employing genome scans have hypothesized that the action of divergent selection should reduce gene flow at the genomic locations implicated in adaptation and speciation among natural populations, yet once 'outlier' patterns of variation have been identified the function and role of such loci needs to be confirmed. We integrated adaptive QTL mapping and genomic scans among diverging sympatric pairs of the lake whitefish (Coregonus clupeaformis) species complex in order to test the hypothesis that differentiation between dwarf and normal ecotypes at growth-associated QTL was maintained by directional selection. We found evidence of significantly high levels of molecular divergence among eight growth QTL where two of the strongest candidate loci under the influence of directional selection exhibited parallel reductions of gene flow over multiple populations.