Sexual selection and speciation in the Anthropocene.

Anthropogenic change threatens global biodiversity by causing severe ecological disturbance and extinction. Here, we consider the effects of anthropogenic change on one process that generates biodiversity. Sexual selection (a potent evolutionary force and driver of speciation) is highly sensitive to the environment and, thus, vulnerable to anthropogenic ecological change. Anthropogenic alterations to sexual display and mate preference can make it harder to distinguish between conspecific and heterospecific mates or can weaken divergence via sexual selection, leading to higher rates of hybridization and biodiversity loss. Occasionally, anthropogenically altered sexual selection can abet diversification, but this appears less likely than biodiversity loss. In our rapidly changing world, a full understanding of sexual selection and speciation requires a global change perspective.

A conceptual framework for understanding stress-induced physiological and transgenerational effects on population responses to climate change.

Organisms are experiencing higher average temperatures and greater temperature variability because of anthropogenic climate change. Some populations respond to changes in temperature by shifting their ranges or adjusting their phenotypes via plasticity and/or evolution, while others go extinct. Predicting how populations will respond to temperature changes is challenging because extreme and unpredictable climate changes will exert novel selective pressures. For this reason, there is a need to understand the physiological mechanisms that regulate organismal responses to temperature changes. In vertebrates, glucocorticoid hormones mediate physiological and behavioral responses to environmental stressors and thus are likely to play an important role in how vertebrates respond to global temperature changes. Glucocorticoids have cascading effects that influence the phenotype and fitness of individuals, and some of these effects can be transmitted to offspring via trans- or intergenerational effects. Consequently, glucocorticoid-mediated responses could affect populations and could even be a powerful driver of rapid evolutionary change. Here, we present a conceptual framework that outlines how temperature changes due to global climate change could affect population persistence via glucocorticoid responses within and across generations (via epigenetic modifications). We briefly review glucocorticoid physiology, the interactions between environmental temperatures and glucocorticoid responses, and the phenotypic consequences of glucocorticoid responses within and across generations. We then discuss possible hypotheses for how glucocorticoid-mediated phenotypic effects might impact fitness and population persistence via evolutionary change. Finally, we pose pressing questions to guide future research. Understanding the physiological mechanisms that underpin the responses of vertebrates to elevated temperatures will help predict population-level responses to the changing climates we are experiencing.

Genetic and Phenotypic Consequences of Local Transitions between Sexual and Parthenogenetic Reproduction in the Wild.

AbstractTransitions from sexual to asexual reproduction have occurred in numerous lineages, but it remains unclear why asexual populations rarely persist. In facultatively parthenogenetic animals, all-female populations can arise when males are absent or become extinct, and such populations could help to understand the genetic and phenotypic changes that occur in the initial stages of transitions to asexuality. We investigated a naturally occurring spatial mosaic of mixed-sex and all-female populations of the facultatively parthenogenetic Australian phasmid Megacrania batesii. Analysis of single-nucleotide polymorphisms indicated multiple independent transitions between reproductive modes. All-female populations had much lower heterozygosity and allelic diversity than mixed-sex populations, but we found few consistent differences in fitness-related traits between population types. All-female populations exhibited more frequent and severe deformities in their (flight-incapable) wings but did not show higher rates of appendage loss. All-female populations also harbored more ectoparasites in swamp (but not beach) habitats. Reproductive mode explained little variation in female body size, fecundity, or egg hatch rate. Our results suggest that transitions to parthenogenetic reproduction can lead to dramatic genetic changes with little immediate effect on performance. All-female M. batesii populations appear to consist of high-fitness genotypes that might be able to thrive for many generations in relatively constant and benign environments but could be vulnerable to environmental challenges, such as increased parasite abundance.

Dietary restriction and lifespan: adaptive reallocation or somatic sacrifice?

Reducing overall food intake, or lowering the proportion of protein relative to other macronutrients, can extend the lifespan of diverse organisms. A number of mechanistic theories have been developed to explain this phenomenon, mostly assuming that the molecules connecting diet to lifespan are evolutionarily conserved. A recent study using Drosophila melanogaster females has pinpointed a single essential micronutrient that can explain how lifespan is changed by dietary restriction. Here, we propose a likely mechanism for this observation, which involves a trade-off between lifespan and reproduction, but in a manner that is conditional on the dietary supply of an essential micronutrient - a sterol. Importantly, these observations argue against previous evolutionary theories that rely on constitutive resource reallocation or damage directly inflicted by reproduction. Instead, they are compatible with a model in which the inverse relationship between lifespan and food level is caused by the consumer suffering from varying degrees of malnutrition when maintained on lab food. The data also indicate that animals on different lab foods may suffer from different nutritional imbalances and that the mechanisms by which dietary restriction benefits the lifespan of different species may vary. This means that translating the mechanistic findings from lab animals to humans will not be simple and should be interpreted in light of the range of challenges that have shaped each organism's lifespan in the wild and the composition of the natural diets upon which they would feed.

Effects of genetic vs. environmental quality on condition-dependent morphological and life history traits in a neriid fly.

Condition is assumed to reflect both genes and environment, enabling condition-dependent signals to reveal genetic quality. However, because the phenotypic effects of variation in genetic quality could be masked by environmental heterogeneity, the contribution of genetic quality to phenotypic variation in fitness-related traits and condition-dependent signals remains unclear. We compared effects of ecologically relevant manipulations of environmental quality (nutrient dilution in the larval diet) and genetic quality (one generation of inbreeding) on male and female morphology, life history and reproductive performance in the neriid fly Telostylinus angusticollis. We found that larval diet quality had strong, positive effects on male and female body size, male secondary sexual traits, and aspects of male and female reproductive performance. By contrast, inbreeding had weak effects on most traits, and no trait showed clear and consistent effects of both environmental and genetic quality. Indeed, inbreeding effects on body size and male competitive performance were of opposite sign in rich vs. poor larval diet treatment groups. Our results suggest that environmental quality strongly affects condition, but the effects of genetic quality are subtle and environment-dependent in this species. These findings raise questions about the genetic architecture of condition and the potential for condition-dependent traits to function as signals of genetic quality.

The Biology of Aging in Insects: From Drosophila to Other Insects and Back.

An enormous amount of work has been done on aging in Drosophila melanogaster, a classical genetic and molecular model system, but also in numerous other insects. However, these two extensive bodies of work remain poorly integrated to date. Studies in Drosophila often explore genetic, developmental, physiological, and nutrition-related aspects of aging in the lab, while studies in other insects often explore ecological, social, and somatic aspects of aging in both lab and natural populations. Alongside exciting genomic and molecular research advances in aging in Drosophila, many new studies have also been published on aging in various other insects, including studies on aging in natural populations of diverse species. However, no broad synthesis of these largely separate bodies of work has been attempted. In this review, we endeavor to synthesize these two semi-independent literatures to facilitate collaboration and foster the exchange of ideas and research tools. While lab studies of Drosophila have illuminated many fundamental aspects of senescence, the stunning diversity of aging patterns among insects, especially in the context of their rich ecology, remains vastlyunderstudied. Coupled with field studies and novel, more easily applicable molecular methods, this represents a major opportunity for deepening our understanding of the biology of aging in insects and beyond.

Does female resistance to mating select for live-fast-die-young strategies in males? A comparative analysis in the genus Drosophila.

Female promiscuity is a pervasive selective force on male reproductive traits, and the strength of sexual selection is predicted to influence the trade-off between lifespan and reproduction. In species where sexual selection is intense, males are predicted to invest in sexual strategies that shorten their lifespan, potentially resulting in female-biased sexual dimorphism in longevity. However, comparative analyses have provided contrasting results, potentially due to the use of broad mating system categories or sexual size dimorphism as a proxy for sexual selection. Here, we used female remating rate (i.e. female promiscuity) as a more direct measure of sexual selection strength and conducted a phylogenetic comparative analysis of the relationship between female remating rate and sexual dimorphism in lifespan in 29 species of Drosophila. We did not find strong evidence that female remating rate was correlated with sexual dimorphism in lifespan. However, we found that male and female lifespans are positively correlated among species and that phylogeny and residual variance (i.e. variation in non-phylogenetic factors) are important in determining female remating rate, male and female lifespans separately, and the correlation between male and female lifespan. We suggest that variation in the nature of sexual competition and variation between studies could account for some of the unexplained variation among species in the relation between female remating rate and sexual dimorphism in lifespan.

Parental dietary protein effects on offspring viability in insects and other oviparous invertebrates: a meta-analysis.

Dietary protein is a key regulator of reproductive effort in animals, but protein consumption also tends to accelerate senescence and reduce longevity. Given this protein-mediated trade-off between reproduction and survival, how does protein consumption by parents affect the viability of their offspring? In insects, protein consumption by females enhances fecundity, but trade-offs between offspring quantity and quality could result in negative effects of protein consumption on offspring viability. Likewise, protein consumption by males tends to enhance the expression of sexual traits but could have negative effects on offspring viability, mediated by epigenetic factors transmitted via the ejaculate. It remains unclear whether dietary protein has consistent effects on offspring viability across species, and whether these effects are sex-specific. To address this, we conducted a meta-analysis of experimental studies that examined the effects of protein content in the maternal and/or paternal diet in insects and other oviparous invertebrates. We did not find consistent effects of paternal or maternal protein consumption on offspring viability. Rather, effects of dietary protein on offspring vary in both magnitude and sign across taxonomic groups. Further studies are needed to determine how the effects of dietary protein on offspring relate to variation in reproductive biology across species. Our findings also highlight important gaps in the literature and limitations in experiment design.

Sperm depletion in relation to developmental nutrition and genotype in Drosophila melanogaster.

Nutrient limitation during development can restrict the ability of adults to invest in costly fitness traits, and genotypes can vary in their sensitivity to developmental nutrition. However, little is known about how genotype and nutrition affect male ability to maintain ejaculate allocation and achieve fertilization across successive matings. Using 17 isogenic lines of Drosophila melanogaster, we investigated how variation in developmental nutrition affects males' abilities to mate, transfer sperm, and sire offspring when presented with successive virgin females. We found that, with each successive mating, males required longer to initiate copulation, transferred fewer sperm, and sired fewer offspring. Males reared on a low-nutrient diet transferred fewer sperm than those reared on nutritionally superior diets, but the rate at which males depleted their sperm, as well as their reproductive performance, was largely independent of diet. Genotype and the genotype × diet interaction explained little of the variation in these male reproductive traits. Our results show that sperm depletion can occur rapidly and impose substantial fitness costs for D. melanogaster males across multiple genotypes and developmental environments.

A comparison of two methods for estimating measurement repeatability in morphometric studies.

Measurement repeatability is often reported in morphometric studies as an index of the contribution of measurement error to trait measurements. However, the common method of remeasuring a mounted specimen fails to capture some components of measurement error and could therefore yield inflated repeatability estimates. Remounting specimens between successive measurements is likely to provide more realistic estimates of repeatability, particularly for structures that are difficult to measure.Using measurements of 22 somatic and genitalic traits of the neriid fly Telostylinus angusticollis, we compared repeatability estimates obtained via remeasurement of a specimen that is mounted once (single-mounted method) versus remeasurement of a specimen that is remounted between measurements (remounted method). We also asked whether the difference in repeatability estimates obtained via the two methods depends on trait size, trait type (somatic vs. genitalic), sclerotization, or sex.Repeatability estimates obtained via the remounted method were lower than estimates obtained via the single-mounted method for each of the 22 traits, and the difference between estimates obtained via the two methods was generally greater for small structures (such as genitalic traits) than for large structures (such as legs and wings). However, the difference between estimates obtained via the two methods did not depend on trait type (genitalic or somatic), tissue type (soft or sclerotized) or sex.Remounting specimens between successive measurements can provide more accurate estimates of measurement repeatability than remeasuring from a single mount, especially for small structures that are difficult to measure.

Development time mediates the effect of larval diet on ageing and mating success of male antler flies in the wild.

High-quality developmental environments often improve individual performance into adulthood, but allocating toward early life traits, such as growth, development rate and reproduction, may lead to trade-offs with late-life performance. It is, therefore, uncertain how a rich developmental environment will affect the ageing process (senescence), particularly in wild insects. To investigate the effects of early life environmental quality on insect life-history traits, including senescence, we reared larval antler flies (Protopiophila litigata) on four diets of varying nutrient concentration, then recorded survival and mating success of adult males released in the wild. Declining diet quality was associated with slower development, but had no effect on other life-history traits once development time was accounted for. Fast-developing males were larger and lived longer, but experienced more rapid senescence in survival and lower average mating rate compared to slow developers. Ultimately, larval diet, development time and body size did not predict lifetime mating success. Thus, a rich environment led to a mixture of apparent benefits and costs, mediated by development time. Our results indicate that 'silver spoon' effects can be complex and that development time mediates the response of adult life-history traits to early life environmental quality.

Sexual dimorphism in trait variability and its eco-evolutionary and statistical implications.

Biomedical and clinical sciences are experiencing a renewed interest in the fact that males and females differ in many anatomic, physiological, and behavioural traits. Sex differences in trait variability, however, are yet to receive similar recognition. In medical science, mammalian females are assumed to have higher trait variability due to estrous cycles (the 'estrus-mediated variability hypothesis'); historically in biomedical research, females have been excluded for this reason. Contrastingly, evolutionary theory and associated data support the 'greater male variability hypothesis'. Here, we test these competing hypotheses in 218 traits measured in >26,900 mice, using meta-analysis methods. Neither hypothesis could universally explain patterns in trait variability. Sex bias in variability was trait-dependent. While greater male variability was found in morphological traits, females were much more variable in immunological traits. Sex-specific variability has eco-evolutionary ramifications, including sex-dependent responses to climate change, as well as statistical implications including power analysis considering sex difference in variance.

Males and females differ in appearance, physiology and behavior. But we do not fully understand the health and evolutionary consequences of these differences. One reason for this is that, until recently, females were often excluded from medical studies. This made it difficult to know if a treatment would perform as well in females as males. To correct this, organizations that fund research now require scientists to include both sexes in studies. This has led to some questions about how to account for sex differences in studies. One reason females have historically been excluded from medical studies is that some scientists assumed that they would have more variable responses to a particular treatment based on their estrous cycles. Other scientists, however, believe that males of a given species might be more variable because of the evolutionary pressures they face in competing for mates. Better understanding how males and females vary would help scientists better design studies to ensure they provide accurate answers. Now, Zajitschek et al. debunk both the idea that males are more variable and the idea that females are more variable. To do this, Zajitschek et al. analyzed differences in 218 traits, like body size or certain behaviors, among nearly 27,000 male and female mice. This showed that neither male mice nor female mice were universally more different from other mice of their sex across all features. Instead, sex differences in how much variation existed in male or female mice depended on the individual trait. For example, males varied more in physical features like size, while females showed more differences in their immune systems. The results suggest it is particularly important to consider sex-specific variability in both medical and other types of studies. To help other researchers better design experiments to factor in such variability, Zajitschek et al. created an interactive tool that will allow scientists to look at sex-based differences in individual features among male or female mice.

Mapping the past, present and future research landscape of paternal effects.

BACKGROUND: Although in all sexually reproducing organisms an individual has a mother and a father, non-genetic inheritance has been predominantly studied in mothers. Paternal effects have been far less frequently studied, until recently. In the last 5 years, research on environmentally induced paternal effects has grown rapidly in the number of publications and diversity of topics. Here, we provide an overview of this field using synthesis of evidence (systematic map) and influence (bibliometric analyses). RESULTS: We find that motivations for studies into paternal effects are diverse. For example, from the ecological and evolutionary perspective, paternal effects are of interest as facilitators of response to environmental change and mediators of extended heredity. Medical researchers track how paternal pre-fertilization exposures to factors, such as diet or trauma, influence offspring health. Toxicologists look at the effects of toxins. We compare how these three research guilds design experiments in relation to objects of their studies: fathers, mothers and offspring. We highlight examples of research gaps, which, in turn, lead to future avenues of research. CONCLUSIONS: The literature on paternal effects is large and disparate. Our study helps in fostering connections between areas of knowledge that develop in parallel, but which could benefit from the lateral transfer of concepts and methods.

Condition dependence of phenotypic integration and the evolvability of genitalic traits in a neriid fly.

The spectacular diversity of insect male genitalia, and their relative insensitivity to the environment, have long puzzled evolutionary biologists and taxonomists. We asked whether the unusual evolvability of male genitalia could be associated with low morphological integration of genitalic traits, by comparison with male somatic traits and female traits. We also asked whether this pattern was robust to variation in resource availability during development, which affects adult condition. To address these questions, we manipulated larval diet quality in a split-brood design and compared levels of integration of male and female genitalic and somatic traits in the neriid fly, Telostylinus angusticollis. We found that male genitalic traits were substantially less integrated than male somatic traits, and less integrated than female genitalic traits. Female genitalic traits were also less integrated than female somatic traits, but the difference was less pronounced than in males. However, integration of male genitalic traits was negatively condition-dependent, with high-condition males exhibiting lower trait integration than low-condition males. Finally, genitalic traits exhibited lower larval diet × family interactions than somatic traits. These results could help explain the unusually high evolvability of male genitalic traits in insects.

Parental breeding age effects on descendants' longevity interact over 2 generations in matrilines and patrilines.

Individuals within populations vary enormously in mortality risk and longevity, but the causes of this variation remain poorly understood. A potentially important and phylogenetically widespread source of such variation is maternal age at breeding, which typically has negative effects on offspring longevity. Here, we show that paternal age can affect offspring longevity as strongly as maternal age does and that breeding age effects can interact over 2 generations in both matrilines and patrilines. We manipulated maternal and paternal ages at breeding over 2 generations in the neriid fly Telostylinus angusticollis. To determine whether breeding age effects can be modulated by the environment, we also manipulated larval diet and male competitive environment in the first generation. We found separate and interactive effects of parental and grand-parental ages at breeding on descendants' mortality rate and life span in both matrilines and patrilines. These breeding age effects were not modulated by grand-parental larval diet quality or competitive environment. Our findings suggest that variation in maternal and paternal ages at breeding could contribute substantially to intrapopulation variation in mortality and longevity.

The paradox of obligate sex: The roles of sexual conflict and mate scarcity in transitions to facultative and obligate asexuality.

The maintenance of obligate sex in animals is a long-standing evolutionary paradox. To solve this puzzle, evolutionary models need to explain why obligately sexual populations consistently resist invasion by facultative strategies that combine the benefits of both sexual and asexual reproduction. Sexual antagonism and mate availability are thought to shape the occurrence of reproductive modes in facultative systems. But it is unclear how such factors interact with each other to influence facultative invasions and transitions to obligate asexuality. Using individual-based models, we clarify how sexually antagonistic coevolution and mate availability affect the likelihood that a mutant allele that gives virgin females the ability to reproduce parthenogenetically will invade an obligately sexual population. We show that male coercion cannot stop the allele from spreading because mutants generally benefit by producing at least some offspring asexually prior to encountering males. We find that effects of sexual conflict can lead to positive frequency-dependent dynamics, where the spread of the allele is promoted by effective (no-cost) resistance when males are common, and by mate limitation when sex ratios are female-biased. However, once the mutant allele fixes, effective coercion prevents the complete loss of sex unless linkage disequilibrium can build up between the allele and alleles for effective resistance. Our findings clarify how limitations of female resistance imposed by the genetic architecture of sexual antagonism can promote the maintenance of sexual reproduction. At the same time, our finding of widespread obligate sex when costs of parthenogenesis are high suggests that developmental constraints could contribute to the rarity of facultative reproductive strategies in nature.

Comparing ageing and the effects of diet supplementation in wild vs. captive antler flies, Protopiophila litigata.

Few studies have simultaneously compared ageing within genetically similar populations in both laboratory and natural environments. Such comparisons are important for interpreting laboratory studies, because factors such as diet could affect ageing in environment-dependent ways. Using a natural population of antler flies (Protopiophila litigata), we conducted separate factorial experiments in 2012 and 2013 that compared age-specific male survival and mating success in laboratory cages versus a natural field environment while supplementing their diets with protein or sugar. We found consistent and substantial increases in both survival and mating rates in the laboratory compared to the field, but remarkably, despite these large differences actuarial ageing was only higher in the laboratory than in the field in 2012 and similar in the two environments in 2013. In both years, there was no difference between environments in reproductive ageing. We found that males fed protein had a higher mortality rate than males fed sugar (strong and low support in 2012 and 2013, respectively). In contrast, diet did not strongly impact average mating rates, actuarial ageing or reproductive ageing in either experiment. Our results provide the first evidence that the negative effect of protein on life span reported in many laboratory studies can also occur in wild populations, although perhaps less consistently. They also highlight how laboratory environments can influence life-history traits and suggest caution when extrapolating from the laboratory to the field.

Effects of nutrient limitation on sperm and seminal fluid: a systematic review and meta-analysis.

Theory predicts that costly sexual traits should be reduced when individuals are in poor condition (i.e. traits should exhibit condition-dependent expression). It is therefore widely expected that male ejaculate traits, such as sperm and seminal fluid, will exhibit reduced quantity and quality when dietary nutrients are limited. However, reported patterns of ejaculate condition dependence are highly variable, and there has been no comprehensive synthesis of underlying sources of such variation in condition-dependent responses. In particular, it remains unclear whether all ejaculate traits are equally sensitive to nutrient intake, and whether such traits are particularly sensitive to certain dietary nutrients, respond more strongly to nutrients during specific life stages, or respond more strongly in some taxonomic groups. We systematically reviewed these potential sources of variation through a meta-analysis across 50 species of arthropods and vertebrates (from 71 papers and 348 effect sizes). We found that overall, ejaculate traits are moderately reduced when dietary nutrients are limited, but we also detected substantial variation in responses. Seminal fluid quantity was strongly and consistently condition dependent, while sperm quantity was moderately condition dependent. By contrast, aspects of sperm quality (particularly sperm viability and morphology) were less consistently reduced under nutrient limitation. Ejaculate traits tended to respond in a condition-dependent manner to a wide range of dietary manipulations, especially to caloric and protein restriction. Finally, while all major taxa for which sufficient data exist (i.e. arthropods, mammals, fish) showed condition dependence of ejaculate traits, we detected some taxonomic differences in the life stage that is most sensitive to nutrient limitation, and in the degree of condition dependence of specific ejaculate traits. Together, these biologically relevant factors accounted for nearly 20% of the total variance in ejaculate responses to nutrient limitation. Interestingly, body size showed considerably stronger condition-dependent responses compared to ejaculate traits, suggesting that ejaculate trait expression may be strongly canalised to protect important reproductive functions, or that the cost of producing an ejaculate is relatively low. Taken together, our findings show that condition-dependence of ejaculate traits is taxonomically widespread, but there are also many interesting, biologically relevant sources of variation that require further investigation. In particular, further research is needed to understand the differences in selective pressures that result in differential patterns of ejaculate condition dependence across taxa and ejaculate traits.