Suzanne C. Mills

Quantitative measure of sexual selection with respect to the operational sex ratio: a comparison of selection indices

Despite numerous indices proposed to predict the evolution of mating systems, a unified measure of sexual selection has remained elusive. Three previous studies have compared indices of sexual selection under laboratory conditions. Here, we use a genetic study to compare the most widely used measures of sexual selection in natural populations. We explored the mating and reproductive successes of male and female bank voles, Clethrionomys glareolus, across manipulated operational sex ratios (OSRs) by genotyping all adult and pup bank voles on 13 islands using six microsatellite loci. We used Batemans principles (Is and I and Bateman gradients) and selection coefficients (s′ and β′) to evaluate, for the first time, the genetic mating system of bank voles and compared these measures with alternative indices of sexual selection (index of monopolization and Morisitas index) across the OSRs. We found that all the sexual selection indices show significant positive intercorrelations for both males and females, suggesting that Batemans principles are an accurate and a valid measure of the mating system. The Bateman gradient, in particular, provides information over and above that of other sexual selection indices. Male bank voles show a greater potential for sexual selection than females, and Bateman gradients indicate a polygynandrous mating system. Selection coefficients reveal strong selection gradients on male bank vole plasma testosterone level rather than body size.

Testosterone‐Mediated Effects on Fitness‐Related Phenotypic Traits and Fitness

The physiological and behavioral mechanisms underlying life‐history trade‐offs are a continued source of debate. Testosterone (T) is one physiological factor proposed to mediate the trade‐off between reproduction and survival. We use phenotypic engineering and multiple laboratory and field fitness‐related phenotypic traits to test the effects of elevated T between two bank vole Myodes glareolus groups: dominant and subordinate males. Males with naturally high T levels showed higher social status (laboratory dominance) and mobility (distance between capture sites) than low‐T males, and the effect of T on immune response was also T group specific, suggesting that behavioral strategies may exist in male bank voles due to the correlated responses of T. Exogenous T enhanced social status, mate searching (polygon of capture sites), mobility, and reproductive success (relative measure of pups sired). However, exogenous T also resulted in the reduction of immune function, but only in males from the high‐T group. This result may be explained either by the immunosuppression costs of T or by differential sensitivity of different behavioral strategies to steroids. Circulating T levels were found to be heritable; therefore, female bank voles would derive indirect genetic benefits via good genes from mating with males signaling dominance.

Gonadotropin Hormone Modulation of Testosterone, Immune Function, Performance, and Behavioral Trade‐Offs among Male Morphs of the Lizard Uta stansburiana

Sexual selection predicts that trade‐offs maintain trait variation in alternative reproductive strategies. Experiments often focus on testosterone (T), but the gonadotropins follicle‐stimulating hormone and luteinizing hormone may provide a clearer understanding of the pleiotropic relationships among traits. We assess the activational role of gonadotropins on T and corticosterone regulation in traits expressed by polymorphic male side‐blotched lizards Uta stansburiana. Gonadotropins are found to enhance and suppress multiple physiological, morphological, and behavioral traits independently, as well as indirectly via T, and we demonstrate selective trade‐offs between reproduction and survival. The OBY locus, a genetic marker in our model vertebrate mating system, allows characterization of the interaction between genotype and hormone treatment on male traits. Our results suggest that oo, ob, and bb males are near their physiological and behavioral capacity for reproductive success, whereas yy and by males are maintained below their physiological maximum. Both by and yy morphs show trait plasticity, and we demonstrate that gonadotropins are likely proximate effectors that govern not only trait differences between alternative mating strategies but also morph plasticity. Gonadotropins clearly represent an important mechanism maintaining variation in physiological, morphological, and behavioral traits, as well as potentially maintaining the immunosuppression costs of male sexual signals.

FITNESS TRADE-OFFS MEDIATED BY IMMUNOSUPPRESSION COSTS IN A SMALL MAMMAL

Trade‐offs are widespread between life‐history traits, such as reproduction and survival. However, their underlying physiological and behavioral mechanisms are less clear. One proposed physiological factor involves the trade‐off between investment in male reproductive effort and immunity. Based on this hypothesis, we investigated differences in fitness between artificially selected immune response bank vole groups, Myodes glareolus. Significant heritability of immune response was found and a correlated response in testosterone levels to selection on immune function. Male reproductive effort, reproductive success, and survival of first generation offspring were assessed and we demonstrate a relationship between laboratory measured immune parameters and fitness parameters in field enclosures. We identify a trade‐off between reproductive effort and survival with immune response and parasites as mediators. However, this trade‐off results in equal male fitness in natural conditions, potentially demonstrating different male signaling strategies for either reproductive effort or survival. Females gain indirect genetic benefits for either genetic disease resistance or male reproductive effort, but not both. Immune response is genetically variable, genetically linked to testosterone and may indirectly maintain genetic variation for sexually selected traits. Evidence for both a genetic and a field trade‐off between reproductive effort and survival indicates an evolutionary constraint on fitness traits.

Negative Frequency-Dependent Selection of Sexually Antagonistic Alleles in Myodes glareolus

Selection of rare-male types in a population can maintain genetic variation that benefits one sex but harms the other. Sexually antagonistic genetic variation, where optimal values of traits are sex-dependent, is known to slow the loss of genetic variance associated with directional selection on fitness-related traits. However, sexual antagonism alone is not sufficient to maintain variation indefinitely. Selection of rare forms within the sexes can help to conserve genotypic diversity. We combined theoretical models and a field experiment with Myodes glareolus to show that negative frequency-dependent selection on male dominance maintains variation in sexually antagonistic alleles. In our experiment, high-dominance male bank voles were found to have low-fecundity sisters, and vice versa. These results show that investigations of sexually antagonistic traits should take into account the effects of social interactions on the interplay between ecology and evolution, and that investigations of genetic variation should not be conducted solely under laboratory conditions.

Intralocus sexual conflict for fitness: sexually antagonistic alleles for testosterone

Intralocus sexual conflict occurs when a trait encoded by the same genetic locus in the two sexes has different optima in males and females. Such conflict is widespread across taxa, however, the shared phenotypic traits that mediate the conflict are largely unknown. We examined whether the sex hormone, testosterone (T), that controls sexual differentiation, contributes to sexually antagonistic fitness variation in the bank vole, Myodes glareolus. We compared (opposite-sex) sibling reproductive fitness in the bank vole after creating divergent selection lines for T. This study shows that selection for T was differentially associated with son versus daughter reproductive success, causing a negative correlation in fitness between full siblings. Our results demonstrate the presence of intralocus sexual conflict for fitness in this small mammal and that sexually antagonistic selection is acting on T. We also found a negative correlation in fitness between parents and their opposite-sex progeny (e.g. father–daughter), highlighting a dilemma for females, as the indirect genetic benefits of selecting reproductively successful males (high T) are lost with daughters. We discuss mechanisms that may mitigate this disparity between progeny quality.

Intra‐ and Intersexual Trade‐Offs between Testosterone and Immune System: Implications for Sexual and Sexually Antagonistic Selection

Parasites indirectly affect life‐history evolution of most species. Combating parasites requires costly immune defenses that are assumed to trade off with other life‐history traits. In vertebrate males, immune defense is thought to trade off with reproductive success, as androgens enhancing sexual signaling can suppress immunity. The phenotypic relationship between male androgen levels and immune function has been addressed in many experimental studies. However, these do not provide information on either intra‐ or intersex genetic correlations, necessary for understanding sexual and sexually antagonistic selection theories. We measured male and female humoral antibody responses to a novel antigen (bovine gamma globulin), total immunoglobulin G, and the male testosterone level of a laboratory population of the bank vole (Myodes glareolus). Although we studied five traits, factor‐analytic modeling of the additive genetic (co)variance matrix within a restricted maximum likelihood–animal model supported genetic variation in three dimensions. Sixty‐five percent of the genetic variation contrasted testosterone with both immune measures in both sexes; consequently, selection for the male trait (testosterone) will have correlated effects on the immune system not only in males but also in females. Thus, our study revealed an intra‐ and intersexual genetic trade‐off between immunocompetence and male reproductive effort, of which only indirect evidence has existed so far.

Anthropogenic noise playback impairs embryonic development and increases mortality in a marine invertebrate

Human activities can create noise pollution and there is increasing international concern about how this may impact wildlife. There is evidence that anthropogenic noise may have detrimental effects on behaviour and physiology in many species but there are few examples of experiments showing how fitness may be directly affected. Here we use a split-brood, counterbalanced, field experiment to investigate the effect of repeated boat-noise playback during early life on the development and survival of a marine invertebrate, the sea hare Stylocheilus striatus at Moorea Island (French Polynesia). We found that exposure to boat-noise playback, compared to ambient-noise playback, reduced successful development of embryos by 21% and additionally increased mortality of recently hatched larvae by 22%. Our work, on an understudied but ecologically and socio-economically important taxon, demonstrates that anthropogenic noise can affect individual fitness. Fitness costs early in life have a fundamental influence on population dynamics and resilience, with potential implications for community structure and function.

INFANTICIDE IN THE EVOLUTION OF REPRODUCTIVE SYNCHRONY: EFFECTS ON REPRODUCTIVE SUCCESS

Abstract Synchronous breeding in animals and plants has stimulated both a theoretical and empirical examination of the possible benefits of active synchronization. The selective pressures of predation and infanticide are the strongest candidates proposed to explain the evolution of reproductive synchrony. Alternatively, breeding asynchronously with conspecifics may ensure a greater availability of resources per breeder. However, the possible fitness benefits resulting from active asynchronization have not yet received attention in evolutionary ecology. Here we present a hypothesis, based on a graphical model, illustrating the costs and benefits of the two modes of reproduction. We tested the hypothesis empirically using a 2 × 2 full factorial study design, where reproductive synchrony and infanticide tactics were manipulated in enclosed populations of the bank vole. The results reveal a relationship between infanticide tactics and breeding synchrony as illustrated by our hypothesis. In general, female reproductive success (number and size of offspring surviving to weaning) was significantly lower in infanticidal populations. Moreover, an asynchronous breeding pattern proved to be advantageous in the noninfanticidal population but this advantage of asynchrony was lost as infanticide became common in the population. Our findings support the idea that synchronous reproduction could have evolved as a counterstrategy against infanticide.

Metabarcoding dietary analysis of coral dwelling predatory fish demonstrates the minor contribution of coral mutualists to their highly partitioned, generalist diet

Understanding the role of predators in food webs can be challenging in highly diverse predator/prey systems composed of small cryptic species. DNA based dietary analysis can supplement predator removal experiments and provide high resolution for prey identification. Here we use a metabarcoding approach to provide initial insights into the diet and functional role of coral-dwelling predatory fish feeding on small invertebrates. Fish were collected in Moorea (French Polynesia) where the BIOCODE project has generated DNA barcodes for numerous coral associated invertebrate species. Pyrosequencing data revealed a total of 292 Operational Taxonomic Units (OTU) in the gut contents of the arc-eye hawkfish (Paracirrhites arcatus), the flame hawkfish (Neocirrhites armatus) and the coral croucher (Caracanthus maculatus). One hundred forty-nine (51%) of them had species-level matches in reference libraries (>98% similarity) while 76 additional OTUs (26%) could be identified to higher taxonomic levels. Decapods that have a mutualistic relationship with Pocillopora and are typically dominant among coral branches, represent a minor contribution of the predators’ diets. Instead, predators mainly consumed transient species including pelagic taxa such as copepods, chaetognaths and siphonophores suggesting non random feeding behavior. We also identified prey species known to have direct negative interactions with stony corals, such as Hapalocarcinus sp, a gall crab considered a coral parasite, as well as species of vermetid snails known for their deleterious effects on coral growth. Pocillopora DNA accounted for 20.8% and 20.1% of total number of sequences in the guts of the flame hawkfish and coral croucher but it was not detected in the guts of the arc-eye hawkfish. Comparison of diets among the three fishes demonstrates remarkable partitioning with nearly 80% of prey items consumed by only one predator. Overall, the taxonomic resolution provided by the metabarcoding approach highlights a highly complex interaction web and demonstrates that levels of trophic partitioning among coral reef fishes have likely been underestimated. Therefore, we strongly encourage further empirical approaches to dietary studies prior to making assumptions of trophic equivalency in food web reconstruction.