Predictable and Divergent Change in the Multivariate P Matrix during Parallel Adaptation.

AbstractAdaptation to replicated environmental conditions can be remarkably predictable, suggesting that parallel evolution may be a common feature of adaptive radiation. An open question, however, is how phenotypic variation itself evolves during repeated adaptation. Here, we use a dataset of morphological measurements from 35 populations of threespine stickleback, consisting of 16 parapatric lake-stream pairs and three marine populations, to understand how phenotypic variation has evolved during transitions from marine to freshwater environments and during subsequent diversification across the lake-stream boundary. We find statistical support for divergent phenotypic covariance (P) across populations, with most diversification of P occurring among freshwater populations. Despite a close correspondence between within-population phenotypic variation and among-population divergence, we find that variation in P is unrelated to total variation in population means across the set of populations. For lake-stream pairs, we find that theoretical predictions for microevolutionary change can explain more than 30% of divergence in P matrices across the habitat boundary. Together, our results indicate that divergence in variance structure occurs primarily in dimensions of trait space with low phenotypic integration, correlated with disparate lake and stream environments. Our findings illustrate how conserved and divergent features of multivariate variation can underlie adaptive radiation.

Genotype × Environment interaction and the evolution of sexual dimorphism: adult nutritional environment mediates selection and expression of sex-specific genetic variance in Drosophila melanogaster.

Sexual conflict plays a key role in the dynamics of adaptive evolution in sexually reproducing populations, and theory suggests an important role for variance in resource acquisition in generating or masking sexual conflict over fitness and life history traits. Here, I used a quantitative genetic genotype × environment experiment in Drosophila melanogaster to test the theoretical prediction that variance in resource acquisition mediates variation in sex-specific component fitness. Holding larval conditions constant, I found that adult nutritional environments characterized by high protein content resulted in reduced survival of both sexes and lower male reproductive success compared to an environment of lower protein content. Despite reduced mean fitness of both sexes in high protein environments, I found a sex*treatment interaction for the relationship between resource acquisition and fitness; estimates of the adaptive landscape indicate males were furthest from their optimum resource acquisition level in high protein environments, and females were furthest in low protein environments. Expression of genetic variance in resource acquisition and survival was highest for each sex in the environment it was best adapted to, although the treatment effects on expression of genetic variance eroded in the path from resource acquisition to total fitness. Cross-sex genetic correlations were strongly positive for resource acquisition, survival, and total fitness and negative for mating success, although estimation error was high for all. These results demonstrate that environmental effects on resource acquisition can have predictable consequences for the expression of sex-specific genetic variance but also that these effects of resource acquisition can erode through life history.

Rapid evolution of ecological sexual dimorphism driven by resource competition.

Sex differences in ecologically important traits are common in animals and plants, and prompted Darwin to first propose an ecological cause of sexual dimorphism. Despite theoretical plausibility and Darwin's original notion, a role for ecological resource competition in the evolution of sexual dimorphism has never been directly demonstrated and remains controversial. I used experimental evolution in Drosophila melanogaster to test the hypothesis that resource competition can drive the evolution of sex differences in diet. Following just three generations of adaptation, offspring from flies evolved in low-resource, high-competition environments show elevated sexual dimorphism in diet preference compared to both the ancestor and populations evolved on high-resource availability. This increased sexual dimorphism was the result of divergence in male sucrose intake and female yeast intake consistent with the differential nutritional requirements of the sexes. These results provide the first real-time direct evidence for evolution of sexual dimorphism driven by resource competition.

Phenotypic plasticity is aligned with phenological adaptation on both micro- and macroevolutionary timescales.

In seasonally variable environments, phenotypic plasticity in phenology may be critical for adaptation to fluctuating environmental conditions. Using an 18-generation longitudinal dataset from natural damselfly populations, we show that phenology has strongly advanced. Individual fitness data suggest this is likely an adaptive response towards a temperature-dependent optimum. A laboratory experiment revealed that developmental plasticity qualitatively matches the temperature dependence of selection, partially explaining observed advance in phenology. Expanding our analysis to the macroevolutionary level, we use a database of over 1-million occurrence records and spatiotemporally matched temperature data from 49 Swedish Odonate species to infer macroevolutionary dynamics of phenology. Phenological plasticity was more closely aligned with adaptation for species that have recently colonised northern latitudes, but with higher phenological mismatch at lower latitudes. Our results show that phenological plasticity plays a key role in microevolutionary dynamics within a single species, and such plasticity may have facilitated post-Pleistocene range expansion in this insect clade.

Complex community-wide consequences of consumer sexual dimorphism.

Sexual dimorphism is a ubiquitous source of within-species variation, yet the community-level consequences of sex differences remain poorly understood. Here, we analyse a bitrophic model of two competing resource species and a sexually reproducing consumer species. We show that consumer sex differences in resource acquisition can have striking consequences for consumer-resource coexistence, abundance and dynamics. Under both direct interspecific competition and apparent competition between two resource species, sexual dimorphism in consumers' attack rates can mediate coexistence of the resource species, while in other cases can lead to exclusion when stable coexistence is typically expected. Slight sex differences in total resource acquisition also can reverse competitive outcomes and lead to density cycles. These effects are expected whenever both consumer sexes require different amounts or types of resources to reproduce. Our results suggest that consumer sexual dimorphism, which is common, has wide-reaching implications for the assembly and dynamics of natural communities.

Extinction and the temporal distribution of macroevolutionary bursts.

Phenotypic evolution through deep time is slower than expected from microevolutionary rates. This is the paradox of stasis. Previous models suggest stasis occurs because populations track adaptive peaks that remain relatively stable on million-year intervals, raising the equally perplexing question of why these large changes are so rare. Here, we consider the possibility that peaks can move more rapidly than populations can adapt, resulting in extinction. We model peak movement with explicit population dynamics, parameterized with published microevolutionary estimates. Allowing extinction greatly increases the parameter space of peak movements that yield the appearance of stasis observed in real data through deep time. Extreme peak displacements, regardless of their frequency, will rarely result in an equivalent degree of trait evolution because of extinction. Thus, larger peak displacements will rarely be inferred using trait data from extant species or observed in fossil records. Our work highlights population ecology as an important contributor to macroevolutionary dynamics, presenting an alternative perspective on the paradox of stasis, where apparent constraint on phenotypic evolution in deep time reflects our restricted view of the subset of earth's lineages that were fortunate enough to reside on relatively stable peaks.

Peak shifts and extinction under sex-specific selection.

A well-known property of sexual selection combined with a cross-sex genetic correlation (rmf) is that it can facilitate a peak shift on the adaptive landscape. How do these diversifying effects of sexual selection + rmf balance with the constraints imposed by such sexual antagonism, to affect the macroevolution of sexual dimorphism? Here, I extend existing quantitative genetic models of evolution on complex adaptive landscapes. Beyond recovering classical predictions for the conditions promoting a peak shift, I show that when rmf is moderate to strong, relatively weak sexual selection is required to induce a peak shift in males only. Increasing the strength of sexual selection leads to a sexually concordant peak shift, suggesting that macroevolutionary rates of sexual dimorphism may be largely decoupled from the strength of within-population sexual selection. Accounting explicitly for demography further reveals that sex-specific peak shifts may be more likely to be successful than concordant shifts in the face of extinction, especially when natural selection is strong. An overarching conclusion is that macroevolutionary patterns of sexual dimorphism are unlikely to be readily explained by within-population estimates of selection or constraint alone.

Habitat partitioning during character displacement between the sexes.

Ecological differences between the sexes are often interpreted as evidence of within-species ecological character displacement (ECD), a hypothesis with almost no direct tests. Here, we experimentally test two predictions that are direct corollaries of ECD between the sexes, in a salamander. First, we find support for the prediction that each sex has a growth rate advantage in the aquatic microhabitat where it is most commonly found. Second, we test the prediction that selection for ECD in the breeding environment may affect partial migration out of this environment. We found that phenotype-dependent migration resulted in a shift in the phenotypic distribution across treatments, with the highest sexual dimorphism occurring among residents at high founding density, suggesting that migration and ECD can both be driven by competition. Our work illustrates how complex patterns of habitat partitioning evolve during ECD between the sexes and suggest ECD and partial migration can interact to effect both ecological dynamics and evolution of sexual dimorphism.

Ecological Character Displacement between the Sexes.

Theory suggests that the evolution of sexual dimorphism in ecologically relevant traits can evolve purely through competition between the sexes for a shared resource. Although more parsimonious hypotheses exist for the evolution of ecological sexual dimorphisms, there are some underappreciated reasons to expect that competition may often play some role in the evolution of sexual dimorphism. Here, we build on past work to outline a set of sufficient criteria to demonstrate a role for resource competition in the evolution of sexual dimorphism, the most critical of which is that resource competition can be directly linked to sexual divergence along the axis of ecologically relevant dimorphism. We then compare the geometry of fitness surfaces across experimental manipulations of density and sex ratio in a semiaquatic salamander (Notophthalmus viridescens). We find consistent disruptive selection on multivariate sexual dimorphism in feeding morphology, which increases in strength with density. Fitness and the strength of divergent selection are negative-frequency dependent in the manner expected under competition-driven divergence between the sexes. Our results constitute direct evidence of resource competition as a driver of sexually antagonist selection and consequently the evolution of sexual dimorphism, providing an illustration of how cause and effect can be separated in studies of sexual divergence in morphology and ecology. We suggest that resource competition may often contribute to sexual divergence jointly with other sources of sex-biased selection, especially when ecological opportunity is sex specific.

Independent evolution of the sexes promotes amphibian diversification.

Classic ecological theory predicts that the evolution of sexual dimorphism constrains diversification by limiting morphospace available for speciation. Alternatively, sexual selection may lead to the evolution of reproductive isolation and increased diversification. We test contrasting predictions of these hypotheses by examining the relationship between sexual dimorphism and diversification in amphibians. Our analysis shows that the evolution of sexual size dimorphism (SSD) is associated with increased diversification and speciation, contrary to the ecological theory. Further, this result is unlikely to be explained by traditional sexual selection models because variation in amphibian SSD is unlikely to be driven entirely by sexual selection. We suggest that relaxing a central assumption of classic ecological models-that the sexes share a common adaptive landscape-leads to the alternative hypothesis that independent evolution of the sexes may promote diversification. Once the constraints of sexual conflict are relaxed, the sexes can explore morphospace that would otherwise be inaccessible. Consistent with this novel hypothesis, the evolution of SSD in amphibians is associated with reduced current extinction threat status, and an historical reduction in extinction rate. Our work reconciles conflicting predictions from ecological and evolutionary theory and illustrates that the ability of the sexes to evolve independently is associated with a spectacular vertebrate radiation.

Correlated evolution of allometry and sexual dimorphism across higher taxa.

Empirical evidence suggests that Rensch's rule of allometric scaling of male and female body size, which states that body size divergence is greater across males than across females of a clade, is not universal. In fact, quantitative genetic theory indicates that the sex under historically stronger directional selection will exhibit greater interspecific variance in size. Thus, the pattern of covariance between allometry of male and female body size and sexual size dimorphism (SSD) across related clades allows a test of this causal hypothesis for macroevolutionary trends in SSD. We compiled a data set of published body size estimates from the amphibians, a class with predominantly female-biased SSD, to examine variation in allometry and SSD among clades. Our results indicate that females become the more size-variant sex across species in a family as the magnitude of SSD in that family increases. This rejects Rensch's rule and implicates selection on females as a driver of both amphibian allometry and SSD. Further, when we combine our data into a single analysis of allometry for the class, we find a significant nonlinear allometric relationship between female body size and male body size. These data suggest that allometry changes significantly as a function of size. Our results illustrate that the relationship between female size and male size varies with both the degree of sexual dimorphism and the body size of a clade.

Condition dependence and the paradox of missing plasticity costs.

Phenotypic plasticity plays a key role in adaptation to changing environments. However, plasticity is neither perfect nor ubiquitous, implying that fitness costs may limit the evolution of phenotypic plasticity in nature. The measurement of such costs of plasticity has proved elusive; decades of experiments show that fitness costs of plasticity are often weak or nonexistent. Here, we show that this paradox could potentially be explained by condition dependence. We develop two models differing in their assumptions about how condition dependence arises; both models show that variation in condition can readily mask costs of plasticity even when such costs are substantial. This can be shown simply in a model where plasticity itself evolves condition dependence, which would be expected if costly. Yet similar effects emerge from an alternative model where trait expression itself is condition-dependent. In this more complex model, the average condition in each environment and genetic covariance in condition across environments both determine when costs of plasticity can be revealed. Analogous to the paradox of missing trade-offs between life history traits, our models show that variation in condition can mask costs of plasticity even when costs exist, and suggest this conclusion may be robust to the details of how condition affects trait expression. Our models suggest that condition dependence can also account for the often-observed pattern of elevated plasticity costs inferred in stressful environments, the maintenance of genetic variance in plasticity, and provides insight into experimental and biological scenarios ideal for revealing a cost of phenotypic plasticity.

Behavioral and physiological female responses to male sex ratio bias in a pond-breeding amphibian.

INTRODUCTION: The phenomenon of sexual conflict has been well documented, and in populations with biased operational sex ratios the consequences for the rarer sex can be severe. Females are typically a limited resource and males often evolve aggressive mating behaviors, which can improve individual fitness for the male while negatively impacting female condition and fitness. In response, females can adjust their behavior to minimize exposure to aggressive mating tactics or minimize the costs of mating harassment. While male-male competition is common in amphibian mating systems, little is known about the consequences or responses of females. The red-spotted newt (Notophthalmus viridescens) is a common pond-breeding amphibian with a complex, well-studied mating system where males aggressively court females. Breeding populations across much of its range have male-biased sex ratios and we predicted that female newts would have behavioral mechanisms to mitigate mating pressure from males. We conducted four experiments examining the costs and behavioral responses of female N. viridescens exposed to a male-biased environment. RESULTS: In field enclosures, we found that female newts exposed to a male-biased environment during the five-month breeding season ended with lower body condition compared to those in a female-biased environment. Shorter-term exposure to a male-biased environment for five weeks caused a decrease in circulating total leukocyte and lymphocyte abundance in blood, which suggests females experienced physiological stress. In behavioral experiments, we found that females were more agitated in the presence of male chemical cues and females in a male-biased environment spent more time in refuge than those in a female-biased environment. CONCLUSIONS: Our results indicate that male-biased conditions can incur costs to females of decreased condition and potentially increased risk of infection. However, we found that females can also alter their behavior and microhabitat use under a male-biased sex ratio. Consistent with surveys showing reduced detection probabilities for females, our research suggests that females avoid male encounters using edge and substrate habitat. Our work illustrates the integrated suite of impacts that sexual conflict can have on the structure and ecology of a population.

Interacting phenotypes and the coevolutionary process: Interspecific indirect genetic effects alter coevolutionary dynamics.

Coevolution occurs when species interact to influence one another's fitness, resulting in reciprocal evolutionary change. In many coevolving lineages, trait expression in one species is modified by the genotypes and phenotypes of the other, forming feedback loops reminiscent of models of intraspecific social evolution. Here, we adapt the theory of within-species social evolution, characterized by indirect genetic effects and social selection imposed by interacting individuals, to the case of interspecific interactions. In a trait-based model, we derive general expressions for multivariate evolutionary change in two species and the expected between-species covariance in evolutionary change when selection varies across space. We show that reciprocal interspecific indirect genetic effects can dominate the coevolutionary process and drive patterns of correlated evolution beyond what is expected from direct selection alone. In extreme cases, interspecific indirect genetic effects can lead to coevolution when selection does not covary between species or even when one species lacks genetic variance. Moreover, our model indicates that interspecific indirect genetic effects may interact in complex ways with cross-species selection to determine the course of coevolution. Importantly, our model makes empirically testable predictions for how different forms of reciprocal interactions contribute to the coevolutionary process.

Male and female reproductive fitness costs of an immune response in natural populations.

Parasites can mediate host fitness both directly, via effects on survival and reproduction, or indirectly by inducing host immune defense with costly side-effects. The evolution of immune defense is determined by a complex interplay of costs and benefits of parasite infection and immune response, all of which may differ for male and female hosts in sexual lineages. Here, we examine fitness costs associated with an inducible immune defense in a fish-cestode host-parasite system. Cestode infection induces peritoneal fibrosis in threespine stickleback (Gasterosteus aculeatus), constraining cestode growth and sometimes encasing and killing the parasite. Surveying two wild populations of stickleback, we confirm that the presence of fibrosis scar tissue is associated with reduced parasite burden in both male and female fish. However, fibrotic fish had lower foraging success and reproductive fitness (reduced female egg production and male nesting success), indicating strong costs of the lingering immunopathology. Consistent with substantial sexually concordant fitness effects of immune response, we find alignment of multivariate selection across the sexes despite sexual antagonism over morphological shape. Although both sexes experienced costs of fibrosis, the net impacts are unequal because in the two study populations females had higher cestode exposure. To evaluate whether this difference in risk should drive sex-specific immune strategies, we analyze a quantitative genetic model of host immune response to a trophically transmitted parasite. The model and empirical data illustrate how shared costs and benefits of immune response lead to shared evolutionary interests of male and female hosts, despite unequal infection risks across the sexes.

A multivariate view of parallel evolution.

A growing number of empirical studies have quantified the degree to which evolution is geometrically parallel by estimating and interpreting pairwise angles between multiple replicate lineages' evolutionary change vectors in multivariate trait space. Similar comparisons, of distance in trait space, are used to assess the degree of convergence. These approaches amount to element-by-element interpretation of distance matrices, typically testing for differences among replicate evolutionary vectors, compared to a null hypothesis of perfect parallelism. We suggest a complimentary set of approaches, co-opted from evolutionary quantitative genetics, involving eigen analysis and comparison of among-lineage covariance matrices. Such approaches allow one to identify multiple major axes of evolutionary change (e.g., alternative adaptive solutions), and also allow for the definition of biologically tenable null hypotheses, such as drift, against which empirical patterns can be tested. Reanalysis of a dataset of multivariate evolution across a replicated lake/stream gradient in threespine stickleback reveals that most of the variation in the direction of evolutionary change can be captured in just a few dimensions, indicating a greater extent of parallelism than previously appreciated. We suggest that applying such multivariate approaches may often be necessary to fully understand the extent and form of parallel and convergent evolution.

Climatic factors and species range position predict sexually antagonistic selection across taxa.

Sex differences in selection are ubiquitous in sexually reproducing organisms. When the genetic basis of traits is shared between the sexes, such sexually antagonistic selection (SAS) creates a potential constraint on adaptive evolution. Theory and laboratory experiments suggest that environmental variation and the degree of local adaptation may all affect the frequency and intensity of SAS. Here, we capitalize on a large database of over 700 spatially or temporally replicated estimates of sex-specific phenotypic selection from wild populations, combined with data on microclimates and geographical range information. We performed a meta-analysis to test three predictions from SAS theory, that selection becomes more concordant between males and females: (1) in more stressful environments, (2) in more variable environments and (3) closer to the edge of the species' range. We find partial empirical support for all three predictions. Within-study analyses indicate SAS decreases in extreme environments, as indicated by a relationship with maximum temperature, minimum precipitation and evaporative potential (PET). Across studies, we found that the average level of SAS at high latitudes was lower, where environmental conditions are typically less stable. Finally, we found evidence for reduced SAS in populations that are far from the centre of their geographical range. However, and notably, we also found some evidence of reduced average strength of selection in these populations, which is in contrast to predictions from classical theoretical models on range limit evolution. Our results suggest that environmental lability and species range position predictably influence sex-specific selection and sexual antagonism in the wild.This article is part of the theme issue 'Linking local adaptation with the evolution of sex differences'.

On the standardization of fitness and traits in comparative studies of phenotypic selection.

Comparisons of the strength and form of phenotypic selection among groups provide a powerful approach for testing adaptive hypotheses. A central and largely unaddressed issue is how fitness and phenotypes are standardized in such studies; standardization across or within groups can qualitatively change conclusions whenever mean fitness differs between groups. We briefly reviewed recent relevant literature, and found that selection studies vary widely in their scale of standardization, but few investigators motivated their rationale for chosen standardization approaches. Here, we propose that the scale at which fitness should be relativized should reflect whether selection is likely to be hard or soft; that is, the scale at which populations (or hypothetical populations in the case of a contrived experiment) are regulated. We argue that many comparative studies of selection are implicitly or explicitly focused on soft selection (i.e., frequency and density-dependent selection). In such studies, relative fitness should preferably be calculated using within-group means, although this approach is taken only occasionally. Related difficulties arise for the standardization of phenotypes. The appropriate scale at which standardization should take place depends on whether groups are considered to be fixed or random. We emphasize that the scale of standardization is a critical decision in empirical studies of selection that should always warrant explicit justification.

Disruptive natural selection predicts divergence between the sexes during adaptive radiation.

Evolution of sexual dimorphism in ecologically relevant traits, for example, via resource competition between the sexes, is traditionally envisioned to stall the progress of adaptive radiation. An alternative view is that evolution of ecological sexual dimorphism could in fact play an important positive role by facilitating sex-specific adaptation. How competition-driven disruptive selection, ecological sexual dimorphism, and speciation interact during real adaptive radiations is thus a critical and open empirical question. Here, we examine the relationships between these three processes in a clade of salamanders that has recently radiated into divergent niches associated with an aquatic life cycle. We find that morphological divergence between the sexes has occurred in a combination of head shape traits that are under disruptive natural selection within breeding ponds, while divergence among species means has occurred independently of this disruptive selection. Further, we find that adaptation to aquatic life is associated with increased sexual dimorphism across taxa, consistent with the hypothesis of clade-wide character displacement between the sexes. Our results suggest the evolution of ecological sexual dimorphism may play a key role in niche divergence among nascent species and demonstrate that ecological sexual dimorphism and ecological speciation can and do evolve concurrently in the early stages of adaptive radiation.

Parasitism and the expression of sexual dimorphism.

Although a negative covariance between parasite load and sexually selected trait expression is a requirement of few sexual selection models, such a covariance may be a general result of life-history allocation trade-offs. If both allocation to sexually selected traits and to somatic maintenance (immunocompetence) are condition dependent, then in populations where individuals vary in condition, a positive covariance between trait expression and immunocompetence, and thus a negative covariance between trait and parasite load, is expected. We test the prediction that parasite load is generally related to the expression of sexual dimorphism across two breeding seasons in a wild salamander population and show that males have higher trematode parasite loads for their body size than females and that a key sexually selected trait covaries negatively with parasite load in males. We found evidence of a weaker negative relationship between the analogous female trait and parasite infection. These results underscore that parasite infection may covary with expression of sexually selected traits, both within and among species, regardless of the model of sexual selection, and also suggest that the evolution of condition dependence in males may affect the evolution of female trait expression.