Swanne P. Gordon

Adaptive Changes in Life History and Survival following a New Guppy Introduction

Numerous studies of wild populations have shown that phenotypic traits can change adaptively on short timescales, but very few studies have considered coincident changes in major fitness components. We here examine adaptive changes in life‐history traits and survival rates for wild guppies introduced into new environments. Female life‐history traits in the derived (Damier River) populations diverged from the ancestral (Yarra River) population, as a result of adaptation to predation regime (high vs. low) and other aspects of the local river. Moreover, some components of the derived Damier populations, particularly juveniles, now show higher survival in the Damier than do contemporary representatives from the ancestral Yarra population. These results suggest that adaptive change can improve survival rates after fewer than 10 years (fewer than 30 guppy generations) in a new environment.

Spatiotemporal variation in linear natural selection on body color in wild guppies (Poecilia reticulata).

We conducted 10 mark–recapture experiments in natural populations of Trinidadian guppies to test hypotheses concerning the role of viability selection in geographic patterns of male color variation. Previous work has reported that male guppies are more colorful in low‐predation sites than in high‐predation sites. This pattern of phenotypic variation has been theorized to reflect differences in the balance between natural (viability) selection that disfavors bright male color (owing to predation) and sexual selection that favors bright color (owing to female choice). Our results support the prediction that male color is disfavored by viability selection in both predation regimes. However, it does not support the prediction that viability selection against male color is weaker in low‐predation experiments. Instead, some of the most intense bouts of selection against color occurred in low‐predation experiments. Our results illustrate considerable spatiotemporal variation in selection among experiments, but such variation was not generally correlated with local patterns of color diversity. More complex selective interactions, possibly including the indirect effects of predators on variation in mating behavior, as well as other environmental factors, might be required to more fully explain patterns of secondary sexual trait variation in this system.

Beyond lifetime reproductive success: the posthumous reproductive dynamics of male Trinidadian guppies

In semelparous populations, dormant germ banks (e.g. seeds) have been proposed as important in maintaining genotypes that are adaptive at different times in fluctuating environments. Such hidden storage of genetic diversity need not be exclusive to dormant banks. Genotype diversity may be preserved in many iteroparous animals through sperm-storage mechanisms in females. This allows males to reproduce posthumously and increase the effective sizes of seemingly female-biased populations. Although long-term sperm storage has been demonstrated in many organisms, the understanding of its importance in the wild is very poor. We here show the prevalence of male posthumous reproduction in wild Trinidadian guppies, through the combination of mark–recapture and pedigree analyses of a multigenerational individual-based dataset. A significant proportion of the reproductive population consisted of dead males, who could conceive up to 10 months after death (the maximum allowed by the length of the dataset), which is more than twice the estimated generation time. Demographic analysis shows that the fecundity of dead males can play an important role in population growth and selection.

Predation-associated differences in sex linkage of wild guppy coloration.

Evolutionary theory predicts that the sex linkage of sexually selected traits can influence the direction and rate of evolutionary change, and also itself be subject to selection. Theory abounds on how sex‐specific selection, mate choice, or other phenomena should favor different types of sex‐linked inheritance, yet evidence in nature remains limited. Here, we use hormone assays in Trinidadian guppies to explore the extent to which linkage of male coloration differs among populations adapted to varying predation regimes. Results show there is consistently higher degree of X‐ and autosomal linkage in body coloration among populations adapted to low‐predation environments. More strikingly, analyses of an introduced population of guppies from a high‐ to a low‐predation environment suggest that this difference can change in 50 years or less.

Selection analysis on the rapid evolution of a secondary sexual trait

Evolutionary analyses of population translocations (experimental or accidental) have been important in demonstrating speed of evolution because they subject organisms to abrupt environmental changes that create an episode of selection. However, the strength of selection in such studies is rarely measured, limiting our understanding of the evolutionary process. This contrasts with long-term, mark–recapture studies of unmanipulated populations that measure selection directly, yet rarely reveal evolutionary change. Here, we present a study of experimental evolution of male colour in Trinidadian guppies where we tracked both evolutionary change and individual-based measures of selection. Guppies were translocated from a predator-rich to a low-predation environment within the same stream system. We used a combination of common garden experiments and monthly sampling of individuals to measure the phenotypic and genetic divergence of male coloration between ancestral and derived fish. Results show rapid evolutionary increases in orange coloration in both populations (1 year or three generations), replicating the results of previous studies. Unlike previous studies, we linked this evolution to an individual-based analysis of selection. By quantifying individual reproductive success and survival, we show, for the first time, that males with more orange and black pigment have higher reproductive success, but males with more black pigment also have higher risk of mortality. The net effect of selection is thus an advantage of orange but not black coloration, as reflected in the evolutionary response. This highlights the importance of considering all components of fitness when understanding the evolution of sexually selected traits in the wild.

Colour polymorphism torn apart by opposing positive frequency‐dependent selection, yet maintained in space

Polymorphic warning signals in aposematic species are enigmatic because predator learning and discrimination should select for the most common coloration, resulting in positive frequency-dependent survival selection. Here, we investigated whether differential mating success could create sufficiently strong negative frequency-dependent selection for rare morphs to explain polymorphic (white and yellow) warning coloration in male wood tiger moths (Parasemia plantaginis). We conducted an experiment in semi-natural conditions where we estimated mating success for both white and yellow male moths under three different morph frequencies. Contrary to expectations, mating success was positively frequency-dependent: white morph males had high relative fitness when common, likewise yellow morph males had high relative fitness when instead they were common. We hence built a model parameterized with our data to examine whether polymorphism can be maintained despite two sources of positive frequency dependence. The model includes known spatial variation in the survival advantage enjoyed by the yellow morph and assumes that relative mating success follows our experimentally derived values. It predicts that polymorphism is possible under migration for up to approximately 20% exchange of individuals between subpopulations in each generation. Our results suggest that differential mating success combined with spatial variation in predator communities may operate as a selection mosaic that prevents complete fixation of either morph.

Does sexual selection evolve following introduction to new environments

The rate of evolution of mating preferences and mate signalling traits can influence local adaptation and diversification under environmental change. However, the rate of evolution of female preferences has not been directly examined in natural populations. An opportunity to do so arose through the introduction of high-predation Trinidadian guppies, Poecilia reticulata, from the Yarra River into high- and low-predation environments in the Damier River. Nine years (13–26 guppy generations) after the introduction, we tested whether female preferences for key aspects of male colour differed between the rivers and between introduced high- and low-predation populations. Based on two independent laboratory experiments, we conclude that little divergence in female preferences has apparently occurred between any of the populations, or between predation regimes. In combination with previous work, these results suggest that the evolution of guppy colour and female preferences are influenced by factors in addition to just predation, and that female preferences may generally take longer to evolve than other types of traits, particularly in populations that experience weak or fluctuating sexual selection gradients.

Rapid Changes in the Sex Linkage of Male Coloration in Introduced Guppy Populations

Theory predicts that the sex linkage of sexually selected traits can influence the direction and rate of evolution and should itself evolve in response to sex-specific selection. Some studies have found intraspecific differences in sex linkage associated with differences in selection pressures, but we know nothing about how fast these differences can evolve. Here we show that introduced guppy populations showing rapid evolution of male coloration also show rapid changes in sex-linkage patterns. A comparison, using hormonal manipulations in females, of introduced populations of different ages suggests a consistent increase of autosomal or X-linked coloration 2 years after introduction from high- to low-predation environments. Twenty years after introduction, populations already show the same pattern of coloration inheritance typical of natural low-predation populations in similar habitats. These results highlight that the contemporary evolution of sexually selected traits ought to be studied in concert with contemporary changes in linkage relationships.

Predator-induced Contemporary Evolution, Phenotypic Plasticity, and the Evolution of Reaction Norms in Guppies

An increasingly large number of studies have demonstrated the ability of populations to undergo contemporary or rapid evolution. Little explored in this regard is the role of phenotypic plasticity, although it can influence eco-evolutionary dynamics and hence evolutionary rates. Here we quantify the evolution of life history and plasticity in Trinidadian guppies transplanted from high to novel low predation environments. Common-garden results show that after only nine years, or 13–27 generations, the introduced guppies have diverged from their ancestral population in both litter size and offspring weight and in the plastic response of both traits to food availability. Given these findings, it is clear that local adaptation includes both changes in mean traits and changes in plasticity.

Transparency reduces predator detection in chemically protected clearwing butterflies

1. Predation is an important selective pressure and some prey have evolved warning colour signals advertising unpalatability (i.e. aposematism) as an antipredator strategy. Unexpectedly, some butterfly species from the unpalatable tribe Ithomiini possess transparent wings, an adaptation rare on land but common in water where it helps avoiding predator detection. 2. We tested if transparency of butterfly wings was associated with decreased detectability by predators, by comparing four butterfly species exhibiting different degrees of transparency, ranging from fully opaque to largely transparent. We tested our prediction using using both wild birds and humans in behavioural experiments. Vision modelling predicted detectability to be similar for these two predator types. 3. In concordance with predictions, more transparent species were almost never the first detected items and were detected less often than the opaque species by both birds and humans, suggesting that transparency enhances crypsis. However, humans could learn to better detect the most transparent species over time. Our study demonstrates for the first time that transparency on land likely decreases detectability by visual predators.