Predation risk and the evolution of a vertebrate stress response: Parallel evolution of stress reactivity and sexual dimorphism.

Predation risk is often invoked to explain variation in stress responses. Yet, the answers to several key questions remain elusive, including the following: (1) how predation risk influences the evolution of stress phenotypes, (2) the relative importance of environmental versus genetic factors in stress reactivity and (3) sexual dimorphism in stress physiology. To address these questions, we explored variation in stress reactivity (ventilation frequency) in a post-Pleistocene radiation of live-bearing fish, where Bahamas mosquitofish (Gambusia hubbsi) inhabit isolated blue holes that differ in predation risk. Individuals of populations coexisting with predators exhibited similar, relatively low stress reactivity as compared to low-predation populations. We suggest that this dampened stress reactivity has evolved to reduce energy expenditure in environments with frequent and intense stressors, such as piscivorous fish. Importantly, the magnitude of stress responses exhibited by fish from high-predation sites in the wild changed very little after two generations of laboratory rearing in the absence of predators. By comparison, low-predation populations exhibited greater among-population variation and larger changes subsequent to laboratory rearing. These low-predation populations appear to have evolved more dampened stress responses in blue holes with lower food availability. Moreover, females showed a lower ventilation frequency, and this sexual dimorphism was stronger in high-predation populations. This may reflect a greater premium placed on energy efficiency in live-bearing females, especially under high-predation risk where females show higher fecundities. Altogether, by demonstrating parallel adaptive divergence in stress reactivity, we highlight how energetic trade-offs may mould the evolution of the vertebrate stress response under varying predation risk and resource availability.

Maladaptive migration behaviour in hybrids links to predator-mediated ecological selection.

Different migratory species have evolved distinct migratory characteristics that improve fitness in their particular ecological niches. However, when such species hybridize, migratory traits from parental species can combine maladaptively and cause hybrids to fall between parental fitness peaks, with potential consequences for hybrid viability and species integrity. Here, we take advantage of a natural cross-breeding incident to study migratory behaviour in naturally occurring hybrids as well as in their parental species and explore links between migratory traits and predation risk. To achieve this, we used electronic tags and passive telemetry to record detailed individual migration patterns (timing and number of migratory trips) in two common freshwater fish species, roach Rutilus rutilus, common bream Abramis brama as well as their hybrids. Next, we scanned for tags regurgitated by a key avian predator (great cormorant Phalacrocorax carbo) at nearby roosting sites, allowing us to directly link migratory behaviour to predation risk in the wild. We found that hybrid individuals showed a higher number of short, multi-trip movements between lake and stream habitats as compared to both parental species. The mean date of first lake departure differed between bream and roach by more than 10 days, while hybrids departed in two distinct peaks that overlapped with the parental species' averages. Moreover, the probability of cormorant predation increased with multi-trip movement frequency across species and was higher for hybrids. Our data provide novel insights into hybrid viability, with links to predator-mediated ecological selection. Increased exposure to predators via maladaptive migratory behaviour reduces hybrid survival and can thereby reinforce species integrity.

Mating competition among females: testing the distinction between natural and sexual selection in an insect.

In species where females compete for mates, the male often provides the female with resources in addition to gametes. A recently suggested definition of sexual selection proposed that if females only benefit from additional resources that come with each mating and not additional gametes, female intrasexual competition for mating opportunities would result in natural selection rather than sexual selection. The nuptial gift-giving bushcricket Kawanaphila nartee has dynamic sex roles and has been a textbook example of sexual selection acting on females via mating competition. We investigated whether females of this species gain fitness benefits from nuptial gifts, additional ejaculates or both by controlling the number of matings and whether the female was allowed to consume the nutritious gift (spermatophylax) at mating. We found that egg production per day of life increased with the number of additional matings, both with and without spermatophylax consumption, but consuming the spermatophylax had an additional positive effect on the number of eggs. These effects were particularly strong in females with shorter lifespans. We discuss how the recently suggested definition of sexual selection applies to nuptial-feeding insects and conclude that both natural and sexual selections influence mating competition in K. nartee females.

Sexually antagonistic co-evolution can explain female display signals and male sensory adaptations.

The prevalence and diversity of female ornaments poses a challenge to evolutionary theory because males should prefer mates that spend resources on offspring rather than ornaments. Among dance flies, there is extraordinary variation in sexual dimorphism. Females of many species have conspicuous ornaments (leg scales and inflatable abdominal sacs). Meanwhile males of some species have exaggerated regions of their eyes with larger ommatidial facets that allow for regionally elevated photosensitivity and/or acuity. Here, we conduct a comparative study of these traits using both species descriptions available from the literature, as well as quantitative measures of eyes and ornaments from wild-caught flies. We show a conspicuous covariance across species between exaggerated male dorsal eye regions and the extent of female ornaments: species with highly ornamented females have males with more exaggerated eyes. We discuss this pattern in the context of competing hypotheses for the evolution of these traits and propose a plausible role for sexually antagonistic coevolution.

Male and female preferences for nest characteristics under paternal care.

Nests play a critical role for offspring development across the animal kingdom. Nest quality may contribute to the builder's extended phenotype and serve as an ornament during mate choice. We examined male and female nest choice in the common goby (Pomatoschistus microps), a benthic fish with male-only parental care where females deposit eggs in male-built nests. Using prebuilt nest models, we independently manipulated two candidate nest quality traits: (a) nest entrance width with a role in oxygen ventilation, and (b) extent of sand cover with a role in camouflage. In simultaneous choice trials, male gobies exhibited no preference for any nest model type. This suggests that initial characteristics of a nesting substrate have minor importance for males, which usually remodel the nest. Females were given a choice between two males occupying either entrance- or cover-manipulated nests. The same pair of males was then exposed to a second female but now with alternated nest types assigned. Most females were consistent in choosing the same, typically the heavier male of the two regardless of nest properties. However, the females that chose the same nest regardless of the male preferred low over high sand coverage and narrow over wide nest entrance. Our results indicate that females base their mating decision on a combination of male phenotype and nest traits. While we found no indication that females are attracted to highly decorated nests, our study is the first in fishes to disentangle a preference for narrow (and thus more protective) nest entrances independent of nest coverage.

Low-latitude zooplankton pigmentation plasticity in response to multiple threats.

Crustacean copepods in high-latitude lakes frequently alter their pigmentation facultatively to defend themselves against prevailing threats, such as solar ultraviolet radiation (UVR) and visually oriented predators. Strong seasonality in those environments promotes phenotypic plasticity. To date, no one has investigated whether low-latitude copepods, experiencing continuous stress from UVR and predation threats, exhibit similar inducible defences. We here investigated the pigmentation levels of Bahamian 'blue hole' copepods, addressing this deficit. Examining several populations varying in predation risk, we found the lowest levels of pigmentation in the population experiencing the highest predation pressure. In a laboratory experiment, we found that, in contrast with our predictions, copepods from these relatively constant environments did show some changes in pigmentation subsequent to the removal of UVR; however, exposure to water from different predation regimes induced minor and idiosyncratic pigmentation change. Our findings suggest that low-latitude zooplankton in inland environments may exhibit reduced, but non-zero, levels of phenotypic plasticity compared with their high-latitude counterparts.