Female preference for rare males is maintained by indirect selection in Trinidadian guppies.

When females prefer mates with rare phenotypes, sexual selection can maintain rather than deplete genetic variation. However, there is no consensus on why this widespread and frequently observed preference might evolve and persist. We examine the fitness consequences of female preference for rare male color patterns in a natural population of Trinidadian guppies, using a pedigree that spans 10 generations. We demonstrate (i) a rare male reproductive advantage, (ii) that females that mate with rare males gain an indirect fitness advantage through the mating success of their sons, and (iii) the fitness benefit that females accrue through their "sexy sons" evaporates for their grandsons as their phenotype becomes common. Counter to prevailing theory, we show that female preference can be maintained through indirect selection.

Life histories as mosaics: Plastic and genetic components differ among traits that underpin life-history strategies.

Life-history phenotypes emerge from clusters of traits that are the product of genes and phenotypic plasticity. If the impact of the environment differs substantially between traits, then life histories might not evolve as a cohesive whole. We quantified the sensitivity of components of the life history to food availability, a key environmental difference in the habitat occupied by contrasting ecotypes, for 36 traits in fast- and slow-reproducing Trinidadian guppies. Our dataset included six putatively independent origins of the slow-reproducing, derived ecotype. Traits varied substantially in plastic and genetic control. Twelve traits were influenced only by food availability (body lengths, body weights), five only by genetic differentiation (interbirth intervals, offspring sizes), 10 by both (litter sizes, reproductive timing), and nine by neither (fat contents, reproductive allotment). Ecotype-by-food interactions were negligible. The response to low food was aligned with the genetic difference between high- and low-food environments, suggesting that plasticity was adaptive. The heterogeneity among traits in environmental sensitivity and genetic differentiation reveals that the components of the life history may not evolve in concert. Ecotypes may instead represent mosaics of trait groups that differ in their rate of evolution.

Predicting evolution over multiple generations in deteriorating environments using evolutionarily explicit Integral Projection Models.

Human impacts on the natural world often generate environmental trends that can have detrimental effects on distributions of phenotypic traits. We do not have a good understanding of how deteriorating environments might impact evolutionary trajectories across multiple generations, even though effects of environmental trends are often significant in the statistical quantitative genetic analyses of phenotypic trait data that are used to estimate additive genetic (co)variances. These environmental trends capture reaction norms, where the same (average) genotype expresses different phenotypic trait values in different environments. Not incorporated into the predictive models typically parameterised from statistical analyses to predict evolution, such as the breeder's equation. We describe how these environmental effects can be incorporated into multi-generational, evolutionarily explicit, structured population models before exploring how these effects can influence evolutionary dynamics. The paper is primarily a description of the modelling approach, but we also show how incorporation into models of the types of environmental trends that human activity has generated can have considerable impacts on the evolutionary dynamics that are predicted.

The evolution of size-dependent competitive interactions promotes species coexistence.

Theory indicates that competing species coexist in a community when intraspecific competition is stronger than interspecific competition. When body size determines the outcome of competitive interactions between individuals, coexistence depends also on how resource use and the ability to compete for these resources change with body size. Testing coexistence theory in size-structured communities, therefore, requires disentangling the effects of size-dependent competitive abilities and niche shifts. Here, we tested the hypothesis that the evolution of species- and size-dependent competitive asymmetries increased the likelihood of coexistence between interacting species. We experimentally estimated the effects of size-dependent competitive interactions on somatic growth rates of two interacting fish species, Trinidadian guppies Poecilia reticulata and killifish Rivulus hartii. We controlled for the effects of size-dependent changes in the niche at two competitive settings representing the early (allopatric) and late (sympatric) evolutionary stages of a killifish-guppy community. We fitted the growth data to a model that incorporates species- and size-dependent competitive asymmetries to test whether changes in the competitive interactions across sizes increased the likelihood of species coexistence from allopatry to sympatry. We found that guppies are competitively superior to killifish but were less so in sympatric populations. The decrease in the effects of interspecific competition on the fitness of killifish and increase in the interspecific effect on guppies' fitness increased the likelihood that sympatric guppies and killifish will coexist. However, while the competitive asymmetries between the species changed consistently between allopatry and sympatry between drainages, the magnitude of the size-dependent competitive asymmetries varied between drainages. These results demonstrate the importance of integrating evolution and trait-based interactions into the research on how species coexist.

Environmental Change, If Unaccounted, Prevents Detection of Cryptic Evolution in a Wild Population.

AbstractDetecting contemporary evolution requires demonstrating that genetic change has occurred. Mixed effects models allow estimation of quantitative genetic parameters and are widely used to study evolution in wild populations. However, predictions of evolution based on these parameters frequently fail to match observations. Here, we applied three commonly used quantitative genetic approaches to predict the evolution of size at maturity in a wild population of Trinidadian guppies. Crucially, we tested our predictions against evolutionary change observed in common-garden experiments performed on samples from the same population. We show that standard quantitative genetic models underestimated or failed to detect the cryptic evolution of this trait as demonstrated by the common-garden experiments. The models failed because (1) size at maturity and fitness both decreased with increases in population density, (2) offspring experienced higher population densities than their parents, and (3) selection on size was strongest at high densities. When we accounted for environmental change, predictions better matched observations in the common-garden experiments, although substantial uncertainty remained. Our results demonstrate that predictions of evolution are unreliable if environmental change is not appropriately captured in models.

Eco-Evolutionary Feedbacks Predict the Time Course of Rapid Life-History Evolution.

Organisms can change their environment and in doing so change the selection they experience and how they evolve. Population density is one potential mediator of such interactions because high population densities can impact the ecosystem and reduce resource availability. At present, such interactions are best known from theory and laboratory experiments. Here we quantify the importance of such interactions in nature by transplanting guppies from a stream where they co-occur with predators into tributaries that previously lacked both guppies and predators. If guppies evolve solely because of the immediate reduction in mortality rate, the strength of selection and rate of evolution should be greatest at the outset and then decline as the population adapts to its new environment. If indirect effects caused by the increase in guppy population density in the absence of predation prevail, then there should be a lag in guppy evolution because time is required for them to modify their environment. The duration of this lag is predicted to be associated with the environmental modification caused by guppies. We observed a lag in life-history evolution associated with increases in population density and altered ecology. How guppies evolved matched predictions derived from evolutionary theory that incorporates such density effects.

Competitive asymmetry and local adaptation in Trinidadian guppies.

The outcome of competition between individuals often depends on body size. These competitive asymmetries can drive variation in demographic rates, influencing the ecology and evolution of life histories. The magnitude and direction of such asymmetries differ among taxa, yet little is known empirically about how adaptation to resource limitation alters competitive asymmetries. Here, we investigate the relationship between size-dependent competitive ability and adaptation to resource limitation. We examined size-dependent competition in two ecotypes of Trinidadian guppy, adapted to high or low levels of resource competition. Using aquaria-based competition experiments, we describe how the size and ecotype of competitors influence somatic growth rate, whilst controlling for the confounding effect of niche differentiation. We replicated our study across two independent evolutionary origins of the "competitive" ecotype. The two "competitive" ecotypes differed markedly in size-dependent asymmetry, indicating that adaptation to resource limitation alone is insufficient to explain changes in size-dependent competitive asymmetry. For one origin, the ecotype adapted to resource limitation was a superior competitor over a wide range of size pairings. The equivalence of competitors varied over fivefold, dependent on size and ecotype; in three of four populations, larger individuals had a competitive advantage. Our results demonstrate that competitive asymmetry has strong effects on somatic growth. Because somatic growth contributes to demographic parameters, intraspecific trait variation is likely to play a key role in regulating demographic rates. Our findings imply that the evolution of size-dependent asymmetries under conditions of intense competition is likely to be constrained by niche availability, although further research is needed to verify this.