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.

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.

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.

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.

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.

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.

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.

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.

Developmental diet irreversibly shapes male post-copulatory traits in the neriid fly Telostylinus angusticollis.

Nutrient availability has been shown to influence investment in many fitness-related traits, including male reproductive success. Many studies have demonstrated that a reduction in nutrient availability alters male post-copulatory trait expression, with some studies demonstrating an effect of developmental nutrients and others, an effect of adult nutrients. However, few studies have manipulated both developmental and adult nutrients in the same experiment. Therefore, it is not clear what life-stage has the greatest effect on post-copulatory trait expression, and if the effects of developmental and adult nutrients can interact. Here, we investigate effects of developmental and adult nutrition on male testes and accessory gland size, sperm movement within the female reproductive tract and sperm length in the neriid fly, Telostylinus angusticollis. We found that males fed a nutrient-poor developmental diet produced sperm with a reduced tail beat frequency and had smaller testes and accessory glands compared to males fed a nutrient-rich developmental diet. In contrast, we found no effects of adult nutrition on any traits measured, although sperm length was correlated with body size and male age but unaffected by nutrition at any stage. Therefore, investment in adult post-copulatory traits is determined early on by developmental nutrients in male neriid flies, and this effect is not altered by adult nutrient availability.

Epigenetic paternal effects as costly, condition-dependent traits.

It is now recognized that post-copulatory traits, such as sperm and ejaculate production can impose metabolic costs, and such traits are therefore expected to exhibit condition-dependent expression, whereby, low condition individuals experience a greater marginal cost of investment compared to high condition individuals. Ejaculates are especially costly in species where males invest in offspring quality through nutrient-rich spermatophores or other seminal nuptial gifts. However, recent evidence shows that, in species where males do not provision females or offspring, males can still influence offspring development through paternal effects mediated by epigenetic factors, such as non-coding RNAs, DNA methylation and chromatin structure. Because such epigenetic paternal effects do not involve the transfer of substantial quantities of resources, such as nutrients, the costs of conferring such effects have not been considered. Here we argue that if selection favours paternal investment in offspring quality through epigenetic factors, then the epigenetic machinery required to bring about such effects may also be expected to evolve strongly condition-dependent expression. We outline indirect evidence suggesting that epigenetic paternal effects could impose substantial metabolic costs, consider the conditions under which selection may act on such effects, and suggest ways to test for differential costs and condition-dependence of these effects. Incorporating epigenetic paternal effects into condition-dependent life history theory will further our understanding of the heritability of fitness and the evolution of paternal investment strategies.

Sex-biased transcriptome divergence along a latitudinal gradient.

Sex-dependent gene expression is likely an important genomic mechanism that allows sex-specific adaptation to environmental changes. Among Drosophila species, sex-biased genes display remarkably consistent evolutionary patterns; male-biased genes evolve faster than unbiased genes in both coding sequence and expression level, suggesting sex differences in selection through time. However, comparatively little is known of the evolutionary process shaping sex-biased expression within species. Latitudinal clines offer an opportunity to examine how changes in key ecological parameters also influence sex-specific selection and the evolution of sex-biased gene expression. We assayed male and female gene expression in Drosophila serrata along a latitudinal gradient in eastern Australia spanning most of its endemic distribution. Analysis of 11 631 genes across eight populations revealed strong sex differences in the frequency, mode and strength of divergence. Divergence was far stronger in males than females and while latitudinal clines were evident in both sexes, male divergence was often population specific, suggesting responses to localized selection pressures that do not covary predictably with latitude. While divergence was enriched for male-biased genes, there was no overrepresentation of X-linked genes in males. By contrast, X-linked divergence was elevated in females, especially for female-biased genes. Many genes that diverged in D. serrata have homologs also showing latitudinal divergence in Drosophila simulans and Drosophila melanogaster on other continents, likely indicating parallel adaptation in these distantly related species. Our results suggest that sex differences in selection play an important role in shaping the evolution of gene expression over macro- and micro-ecological spatial scales.

Why do the well-fed appear to die young? A new evolutionary hypothesis for the effect of dietary restriction on lifespan.

Dietary restriction (DR) famously extends lifespan and reduces fecundity across a diverse range of species. A prominent hypothesis suggests that these life-history responses evolved as a survival-enhancing strategy whereby resources are redirected from reproduction to somatic maintenance, enabling organisms to weather periods of resource scarcity. We argue that this hypothesis is inconsistent with recent evidence and at odds with the ecology of natural populations. We consider a wealth of molecular, medical, and evolutionary research, and conclude that the lifespan extension effect of DR is likely to be a laboratory artifact: in contrast with captivity, most animals living in natural environments may fail to achieve lifespan extension under DR. What, then, is the evolutionary significance of the suite of responses that extend lifespan in the laboratory? We suggest that these responses represent a highly conserved nutrient recycling mechanism that enables organisms to maximize immediate reproductive output under conditions of resource scarcity.

Differential effects of genetic vs. environmental quality in Drosophila melanogaster suggest multiple forms of condition dependence.

Condition is a central concept in evolutionary ecology, but the roles of genetic and environmental quality in condition-dependent trait expression remain poorly understood. Theory suggests that condition integrates genetic, epigenetic and somatic factors, and therefore predicts alignment between the phenotypic effects of genetic and environmental quality. To test this key prediction, we manipulated both genetic (mutational) and environmental (dietary) quality in Drosophila melanogaster and examined responses in morphological and chemical (cuticular hydrocarbon, CHC) traits in both sexes. While the phenotypic effects of diet were consistent among genotypes, effects of mutation load varied in magnitude and direction. Average effects of diet and mutation were aligned for most morphological traits, but non-aligned for the male sexcombs and CHCs in both sexes. Our results suggest the existence of distinct forms of condition dependence, one integrating both genetic and environmental effects and the other purely environmental. We propose a model to account for these observations.

Revisiting telegony: offspring inherit an acquired characteristic of their mother's previous mate.

Newly discovered non-genetic mechanisms break the link between genes and inheritance, thereby also raising the possibility that previous mating partners could influence traits in offspring sired by subsequent males that mate with the same female ('telegony'). In the fly Telostylinus angusticollis, males transmit their environmentally acquired condition via paternal effects on offspring body size. We manipulated male condition, and mated females to two males in high or low condition in a fully crossed design. Although the second male sired a large majority of offspring, offspring body size was influenced by the condition of the first male. This effect was not observed when females were exposed to the first male without mating, implicating semen-mediated effects rather than female differential allocation based on pre-mating assessment of male quality. Our results reveal a novel type of transgenerational effect with potential implications for the evolution of reproductive strategies.

Does ecology shape geographical parthenogenesis? Evidence from the facultatively parthenogenetic stick insect Megacrania batesii.

Closely related sexual and parthenogenetic species often show distinct distribution patterns, known as geographical parthenogenesis. Similar patterns, characterized by the existence of separate sexual and parthenogenetic populations across their natural range, can also be found in facultative parthenogens - species in which every female is capable of both sexual and parthenogenetic reproduction. The underlying mechanisms driving this phenomenon in nature remain unclear. Features of the habitat, such as differences in host-plant phenotypes or niche breadth, could favour sexual or asexual reproductive modes and thus help to explain geographical parthenogenesis in natural insect populations. Megacrania batesii is a facultatively parthenogenetic stick insect that displays geographical parthenogenesis in the wild. We aimed to explore whether sexual and parthenogenetic populations of M. batesii displayed niche differentiation or variations in niche breadth that could explain the separation of the two population types. To do this, we sampled host plants from across the range of M. batesii and quantified phenotypic traits that might affect palatability or accessibility for M. batesii, including leaf thickness, toughness, spike size and density, plant height, and chemical composition. We also quantified host-plant density, which could affect M. batesii dispersal. We found little evidence of phenotypic differences between host plants supporting sexual versus asexual M. batesii populations, and no difference in host-plant density or niche breadth between the two population types. Our results suggest that habitat parameters do not play a substantial role in shaping patterns of geographical parthenogenesis in wild populations of M. batesii. Instead, population sex ratio variation could result from interactions between the sexes or dispersal dynamics.

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.

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.

Sex-specific fitness consequences of nutrient intake and the evolvability of diet preferences.

The acquisition of nutrients is fundamental for the maintenance of bodily functions, growth, and reproduction in animals. As a result, fitness can be maximized only when animals are able to direct their attention to foods that reflect their current nutritional needs. Despite significant literature documenting the fitness consequences of nutrient composition and preference, less is known about the underlying genetic architecture of the dietary preferences themselves, specifically, the degree to which they can respond to selection. We addressed this by integrating evolutionary quantitative genetics and nutritional geometry to examine the shape of the sex-specific fitness surfaces and the availability of genetic variance for macronutrient preferences in the fruit fly Drosophila melanogaster. Combining these analyses, we found that the microevolutionary potential of carbohydrate and protein preference was above average in this population, because the expected direction of selection was relatively well aligned with the major axis of the genetic variance-covariance matrix, G. We also found that potential exists for sexually antagonistic genetic constraint in this system; macronutrient blends maximizing fitness differed between the sexes, and cross-sex genetic correlations for their consumption were positive. However, both sexes were displaced from their feeding optima, generating similar directional selection on males and females, with the combined effect being that minimal sex-specific genetic constraints currently affect dietary preferences in this population.