The evolution of developmental thresholds and reaction norms for age and size at maturity.

Developing organisms typically mature earlier and at larger sizes in favorable growth conditions, while in rarer cases, maturity is delayed. The rarer reaction norm is easily accommodated by general life history models, whereas the common pattern is not. Theory suggests that a solution to this paradox lies in the existence of critical size thresholds at which maturation or metamorphosis can commence, and in the evolution of these threshold sizes in response to environmental variation. For example, ephemeral environments might favor the evolution of smaller thresholds, enabling earlier maturation. The threshold model makes two unique and untested predictions. First, reaction norms for age and size should steepen, and even change sign, with decreases in threshold size; second, food reductions at sizes below the threshold should delay maturation, while those occurring after the threshold should accelerate maturation. We test these predictions through food manipulations in five damselfly species that theory suggests should differ in threshold size. The results provide strong support for the threshold model's predictions. In all species, early food reductions delayed maturation, while late reductions accelerated maturation. Reaction norms were steeper, and the effect of food reductions changed from decelerating to accelerating at a much smaller size in species from ephemeral habitats. These results support the view that developmental thresholds can account for the widespread observation of negative correlations between age and size at maturity. Moreover, evolution of the threshold appears to be both predictable and central to the observed diversity of reaction norms for age and size at maturity.

Transcriptome-based Phylogeny of the Semi-aquatic Bugs (Hemiptera: Heteroptera: Gerromorpha) Reveals Patterns of Lineage Expansion in a Series of New Adaptive Zones.

Key innovations enable access to new adaptive zones and are often linked to increased species diversification. As such, innovations have attracted much attention, yet their concrete consequences on the subsequent evolutionary trajectory and diversification of the bearing lineages remain unclear. Water striders and relatives (Hemiptera: Heteroptera: Gerromorpha) represent a monophyletic lineage of insects that transitioned to live on the water-air interface and that diversified to occupy ponds, puddles, streams, mangroves and even oceans. This lineage offers an excellent model to study the patterns and processes underlying species diversification following the conquest of new adaptive zones. However, such studies require a reliable and comprehensive phylogeny of the infraorder. Based on whole transcriptomic datasets of 97 species and fossil records, we reconstructed a new phylogeny of the Gerromorpha that resolved inconsistencies and uncovered strong support for previously unknown relationships between some important taxa. We then used this phylogeny to reconstruct the ancestral state of a set of adaptations associated with water surface invasion (fluid locomotion, dispersal and transition to saline waters) and sexual dimorphism. Our results uncovered important patterns and dynamics of phenotypic evolution, revealing how the initial event of water surface invasion enabled multiple subsequent transitions to new adaptive zones on the water surfaces. This phylogeny and the associated transcriptomic datasets constitute highly valuable resources, making Gerromorpha an attractive model lineage to study phenotypic evolution.

Ecology, the pace-of-life, epistatic selection and the maintenance of genetic variation in life-history genes.

Evolutionary genetics has long struggled with understanding how functional genes under selection remain polymorphic in natural populations. Taking as a starting point that natural selection is ultimately a manifestation of ecological processes, we spotlight an underemphasized and potentially ubiquitous ecological effect that may have fundamental effects on the maintenance of genetic variation. Negative frequency dependency is a well-established emergent property of density dependence in ecology, because the relative profitability of different modes of exploiting or utilizing limiting resources tends to be inversely proportional to their frequency in a population. We suggest that this may often generate negative frequency-dependent selection (NFDS) on major effect loci that affect rate-dependent physiological processes, such as metabolic rate, that are phenotypically manifested as polymorphism in pace-of-life syndromes. When such a locus under NFDS shows stable intermediate frequency polymorphism, this should generate epistatic selection potentially involving large numbers of loci with more minor effects on life-history (LH) traits. When alternative alleles at such loci show sign epistasis with a major effect locus, this associative NFDS will promote the maintenance of polygenic variation in LH genes. We provide examples of the kind of major effect loci that could be involved and suggest empirical avenues that may better inform us on the importance and reach of this process.

Direct and indirect effects of male genital elaboration in female seed beetles.

Our understanding of coevolution between male genitalia and female traits remains incomplete. This is perhaps especially true for genital traits that cause internal injuries in females, such as the spiny genitalia of seed beetles where males with relatively long spines enjoy a high relative fertilization success. We report on a new set of experiments, based on extant selection lines, aimed at assessing the effects of long male spines on females in Callosobruchus maculatus. We first draw on an earlier study using microscale laser surgery, and demonstrate that genital spines have a direct negative (sexually antagonistic) effect on female fecundity. We then ask whether artificial selection for long versus short spines resulted in direct or indirect effects on female lifetime offspring production. Reference females mating with males from long-spine lines had higher offspring production, presumably due to an elevated allocation in males to those ejaculate components that are beneficial to females. Remarkably, selection for long male genital spines also resulted in an evolutionary increase in female offspring production as a correlated response. Our findings thus suggest that female traits that affect their response to male spines are both under direct selection to minimize harm but are also under indirect selection (a good genes effect), consistent with the evolution of mating and fertilization biases being affected by several simultaneous processes.

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.

Oxygen Limitation at the Larval Stage and the Evolution of Maternal Investment per Offspring in Aquatic Environments.

Oxygen limitation and surface area to volume relationships of the egg were long thought to constrain egg size in aquatic environments, but more recent evidence indicates that egg size per se does not influence oxygen availability to embryos. Here, we suggest that investment per offspring is nevertheless constrained in aquatic anamniotes by virtue of oxygen transport in free-living larvae. Drawing on the well-supported assumption that oxygen limitation is relatively pronounced in aquatic versus terrestrial environments and that oxygen limitation is particularly severe in warm aquatic environments, we employ comparative methods in the Amphibia to investigate this problem. Across hundreds of species and two major amphibian clades, the slope of species mean egg diameter over habitat temperature is negative for species with aquatic larvae but is positive or neutral for species featuring terrestrial eggs and no larvae. Yet across species with aquatic larvae, the negative slope of egg diameter over temperature is similar whether eggs are laid terrestrially or aquatically, consistent with an oxygen constraint arising at the larval stage. Finally, egg size declines more strongly with temperature for species that cannot breathe aerially before metamorphosis compared with those that can. Our results suggest that oxygen transport in larvae (not eggs) constrains investment per offspring. This study further extends the generality of temperature-dependent oxygen limitation as a mechanism driving the temperature-size rule in aquatic systems.

The Genomics of Sexual Conflict.

Sexual dimorphism is a substantial contributor to the diversity observed in nature, extending from elaborate traits to the expression level of individual genes. Sexual conflict and sexually antagonistic coevolution are thought to be central forces driving the dimorphism of the sexes and its diversity. We have substantial data to support this at the phenotypic level but much less at the genetic level, where distinguishing the role of conflict from other forms of sex-biased selection and from other processes is challenging. Here we discuss the powerful effects sexual conflict may have on genome evolution and critically evaluate the supporting evidence. Although there is much potential for sexual conflict to affect genome evolution, we have relatively little compelling evidence of a genomic signature of sexual conflict. A central obstacle is the mismatch between taxa in which we understand sexually antagonistic selection and those in which we understand genetics.

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.

The role of ecology, neutral processes and antagonistic coevolution in an apparent sexual arms race.

Some of the strongest examples of a sexual 'arms race' come from observations of correlated evolution in sexually antagonistic traits among populations. However, it remains unclear whether these cases truly represent sexually antagonistic coevolution; alternatively, ecological or neutral processes might also drive correlated evolution. To investigate these alternatives, we evaluated the contributions of intersex genetic correlations, ecological context, neutral genetic divergence and sexual coevolution in the correlated evolution of antagonistic traits among populations of Gerris incognitus water striders. We could not detect intersex genetic correlations for these sexually antagonistic traits. Ecological variation was related to population variation in the key female antagonistic trait (spine length, a defence against males), as well as body size. Nevertheless, population covariation between sexually antagonistic traits remained substantial and significant even after accounting for all of these processes. Our results therefore provide strong evidence for a contemporary sexual arms race.

Explaining the apparent paradox of persistent selection for early flowering.

Decades of observation in natural plant populations have revealed pervasive phenotypic selection for early flowering onset. This consistent pattern seems at odds with life-history theory, which predicts stabilizing selection on age and size at reproduction. Why is selection for later flowering rare? Moreover, extensive evidence demonstrates that flowering time can and does evolve. What maintains ongoing directional selection for early flowering? Several non-mutually exclusive processes can help to reconcile the apparent paradox of selection for early flowering. We outline four: selection through other fitness components may counter observed fecundity selection for early flowering; asymmetry in the flowering-time-fitness function may make selection for later flowering hard to detect; flowering time and fitness may be condition-dependent; and selection on flowering duration is largely unaccounted for. In this Viewpoint, we develop these four mechanisms, and highlight areas where further study will improve our understanding of flowering-time evolution.

Why organisms age: Evolution of senescence under positive pleiotropy?

Two classic theories maintain that aging evolves either because of alleles whose deleterious effects are confined to late life or because of alleles with broad pleiotropic effects that increase early-life fitness at the expense of late-life fitness. However, empirical studies often reveal positive pleiotropy for fitness across age classes, and recent evidence suggests that selection on early-life fitness can decelerate aging and increase lifespan, thereby casting doubt on the current consensus. Here, we briefly review these data and promote the simple argument that aging can evolve under positive pleiotropy between early- and late-life fitness when the deleterious effect of mutations increases with age. We argue that this hypothesis makes testable predictions and is supported by existing evidence.

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.

Gene-environment interplay in Drosophila melanogaster: chronic food deprivation in early life affects adult exploratory and fitness traits.

Early life adversity has known impacts on adult health and behavior, yet little is known about the gene-environment interactions (GEIs) that underlie these consequences. We used the fruit fly Drosophila melanogaster to show that chronic early nutritional adversity interacts with rover and sitter allelic variants of foraging (for) to affect adult exploratory behavior, a phenotype that is critical for foraging, and reproductive fitness. Chronic nutritional adversity during adulthood did not affect rover or sitter adult exploratory behavior; however, early nutritional adversity in the larval period increased sitter but not rover adult exploratory behavior. Increasing for gene expression in the mushroom bodies, an important center of integration in the fly brain, changed the amount of exploratory behavior exhibited by sitter adults when they did not experience early nutritional adversity but had no effect in sitters that experienced early nutritional adversity. Manipulation of the larval nutritional environment also affected adult reproductive output of sitters but not rovers, indicating GEIs on fitness itself. The natural for variants are an excellent model to examine how GEIs underlie the biological embedding of early experience.

Male bias in distributions of additive genetic, residual, and phenotypic variances of shared traits.

Despite a shared genetic architecture between males and females, sexual differences are widespread. The extent of this shared genetic architecture, reflected in the intersexual genetic correlation, has previously been correlated with the extent of phenotypic sexual dimorphism in shared traits. However, the magnitude of the difference in sex-specific additive genetic variances may also fuel sexual dimorphism. To explore the correlation between additive genetic variance dimorphism and phenotypic dimorphism, we conducted a literature search. We targeted traits expressed in both sexes and excluded sex-limited traits. The mean difference between the sexes in additive genetic variance was not significantly different from 0. However, the distribution of the sexual difference in additive genetic variance had a significant male-biased skew. This pattern persists even after removing traits explicitly related to reproduction. Furthermore, male traits had more residual and phenotypic variance than homologous female traits (as measured by both the mean and the skew), and this difference was not necessarily due to the difference between sexual traits and nonsexual traits. We found no evidence that sex chromosome system could explain sex differences in additive genetic, nonadditive genetic, or phenotypic variances. Finally, we found a significant correlation between the extent of sexual dimorphism in additive genetic variances and the extent of phenotypic sexual dimorphism. Understanding why traits have sex-specific patterns of variation awaits further investigation.

The effect of epistasis on sexually antagonistic genetic variation.

There is increasing evidence of segregating sexually antagonistic (SA) genetic variation for fitness in laboratory and wild populations, yet the conditions for the maintenance of such variation can be restrictive. Epistatic interactions between genes can contribute to the maintenance of genetic variance in fitness and we suggest that epistasis between SA genes should be pervasive. Here, we explore its effect on SA genetic variation in fitness using a two locus model with negative epistasis. Our results demonstrate that epistasis often increases the parameter space showing polymorphism for SA loci. This is because selection in one locus is affected by allele frequencies at the other, which can act to balance net selection in males and females. Increased linkage between SA loci had more marginal effects. We also show that under some conditions, large portions of the parameter space evolve to a state where male benefit alleles are fixed at one locus and female benefit alleles at the other. This novel effect of epistasis on SA loci, which we term the 'equity effect', may have important effects on population differentiation and may contribute to speciation. More generally, these results support the suggestion that epistasis contributes to population divergence.

The interactive effects of competition and predation risk on dispersal in an insect.

Dispersal dynamics have significant consequences for ecological and evolutionary processes. Previous work has demonstrated that dispersal can be context-dependent. However, factors affecting dispersal are typically considered in isolation, despite the probability that individuals make dispersal decisions in response to multiple, possibly interacting factors. We examined whether two ecological factors, predation risk and intraspecific competition, have interactive effects on dispersal dynamics. We performed a factorial experiment in mesocosms using backswimmers (Notonecta undulata), flight-capable, semi-aquatic insects. Emigration rates increased with density, and increased with predation risk at intermediate densities; however, predation had minimal effects on emigration at high and low densities. Our results indicate that factorial experiments may be required to understand dispersal dynamics under realistic ecological conditions.

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.

The effects of selective history and environmental heterogeneity on inbreeding depression in experimental populations of Drosophila melanogaster.

Inbreeding depression varies considerably among populations, but only some aspects of this variation have been thoroughly studied. Because inbreeding depression requires genetic variation, factors that influence the amount of standing variation can affect the magnitude of inbreeding depression. Environmental heterogeneity has long been considered an important contributor to the maintenance of genetic variation, but its effects on inbreeding depression have been largely ignored by empiricists. Here we compare inbreeding depression, measured in two environments, for 20 experimental populations of Drosophila melanogaster that have been maintained under four different selection regimes, including two types of environmentally homogeneous selection and two types environmentally heterogeneous selection. In line with theory, we find considerably higher inbreeding depression in populations from heterogeneous selection regimes. We also use our data set to test whether inbreeding depression is correlated with either stress or the phenotypic coefficient of variation (CV), as suggested by some recent studies. Though both of these factors are significant predictors of inbreeding depression in our study, there is an effect of assay environment on inbreeding depression that cannot be explained by either stress or CV.

Sexual conflict and the function of genitalic claws in guppies (Poecilia reticulata).

Poeciliid fish, freshwater fish with internal fertilization, are known for the diversity of structures on the male intromittent organ, the gonopodium. Prominent among these, in some species, is a pair of claws at its tip. We conducted a manipulative study of these claws in the guppy, Poecilia reticulata, to determine if these aid in transferring sperm to resistant females. We compared the sperm transfer rates of clawed versus surgically declawed males attempting to mate with either receptive or unreceptive (i.e. resistant) females. Our analyses demonstrate that the gonopodial claws function to increase sperm transfer to unreceptive females during uncooperative matings but not during receptive matings. Up to threefold more sperm were transferred to unreceptive females by clawed than declawed males. These data suggest that the claw is a sexually antagonistic trait, functioning to aid in transferring sperm to resistant females, and implicate sexual conflict as a selective force in the diversification of the gonopodium in the Poeciliidae.