Adaptive Maternal Effects Shape Offspring Phenotype and Survival in Natal Environments.

AbstractMaternal effects can give newborns a head start in life by adjusting natal phenotypes to natal environments, yet their strength and adaptiveness are often difficult to investigate in natural populations. Here, we studied anticipatory maternal effects and their adaptiveness in common lizards in a seminatural experimental system. Specifically, we investigated how maternal environments (i.e., vegetation cover) and maternal phenotype (i.e., activity levels and body length) can shape offspring phenotype. We further studied whether such maternal effects influenced offspring survival in natal environments varying with respect to vegetation cover, conspecific density, and, consequently, maternal fitness. More active females from dense vegetation habitats produced bigger offspring than their less active counterparts, the contrary being true for sparse vegetation habitats. Moreover, females from dense vegetation habitats produced more active offspring and more active offspring survived better in dense vegetation habitats, resulting in greater maternal fitness through maternal effects. These results suggest adaptive anticipatory maternal effects, induced by vegetation structure and mediated by activity levels that may shape early-life prospects in natal environments.

The diversity of population responses to environmental change.

The current extinction and climate change crises pressure us to predict population dynamics with ever-greater accuracy. Although predictions rest on the well-advanced theory of age-structured populations, two key issues remain poorly explored. Specifically, how the age-dependency in demographic rates and the year-to-year interactions between survival and fecundity affect stochastic population growth rates. We use inference, simulations and mathematical derivations to explore how environmental perturbations determine population growth rates for populations with different age-specific demographic rates and when ages are reduced to stages. We find that stage- vs. age-based models can produce markedly divergent stochastic population growth rates. The differences are most pronounced when there are survival-fecundity-trade-offs, which reduce the variance in the population growth rate. Finally, the expected value and variance of the stochastic growth rates of populations with different age-specific demographic rates can diverge to the extent that, while some populations may thrive, others will inevitably go extinct.

Costs and benefits of giant sperm and sperm storage organs in Drosophila melanogaster.

In Drosophila, long sperm are favoured in sperm competition based on the length of the female's primary sperm storage organ, the seminal receptacle (SR). This sperm-SR interaction, together with a genetic correlation between the traits, suggests that the coevolution of exaggerated sperm and SR lengths may be driven by Fisherian runaway selection. Here, we explore the costs and benefits of long sperm and SR genotypes, both in the sex that carries them and in the sex that does not. We measured male and female fitness in inbred lines of Drosophila melanogaster derived from four populations previously selected for long sperm, short sperm, long SRs or short SRs. We specifically asked: What are the costs and benefits of long sperm in males and long SRs in females? Furthermore, do genotypes that generate long sperm in males or long SRs in females impose a fitness cost on the opposite sex? Answers to these questions will address whether long sperm are an honest indicator of male fitness, male post-copulatory success is associated with male precopulatory success, female choice benefits females or is costly, and intragenomic conflict could influence evolution of these traits. We found that both sexes have increased longevity in long sperm and long SR genotypes. Males, but not females, from long SR lines had higher fecundity. Our results suggest that sperm-SR coevolution is facilitated by both increased viability and indirect benefits of long sperm and SRs in both sexes.

Paternal personality and social status influence offspring activity in zebrafish.

BACKGROUND: Evidence for the transmission of non-genetic information from father to offspring is rapidly accumulating. While the impact of chemical and physical factors such as toxins or diet on the fitness of the parents and their offspring have been studied extensively, the importance of behavioural and social circumstances has only recently been recognised. Behavioural traits such as personality characteristics can be relatively stable, and partly comprise a genetic component but we know little about the non-genetic transmission of plastic behavioural traits from parents to offspring. We investigated the relative effect of personality and of social dominance as indicators at the opposite ends of the plasticity range on offspring behaviour in the zebrafish (Danio rerio). We assessed male boldness, a behavioural trait that has previously been shown previously to possess genetic underpinnings, and experimentally manipulated male social status to assess the association between the two types of behaviour and their correlation with offspring activity. RESULTS: We found a clear interaction between the relatively stable and putative genetic effects based on inherited differences in personality and the experimentally induced epigenetic effects from changes in the social status of the father on offspring activity. CONCLUSIONS: Our study shows that offspring behaviour is determined by a combination of paternal personality traits and on-genetic effects derived from the social status of the father.

Paternal diet affects differential gene expression, but not sperm competition, in sons.

Parental environment can widely influence offspring phenotype, but paternal effects in the absence of parental care remain poorly understood. We asked if protein content in the larval diet of fathers affected paternity success and gene expression in their sons. We found that males reared on high-protein diet had sons that fared better during sperm competition, suggesting that postcopulatory sexual selection is subject to transgenerational paternal effects. Moreover, immune response genes were downregulated in sons of low-protein fathers, while genes involved in metabolic and reproductive processes were upregulated.

Evolution under dietary restriction increases male reproductive performance without survival cost.

Dietary restriction (DR), a reduction in nutrient intake without malnutrition, is the most reproducible way to extend lifespan in a wide range of organisms across the tree of life, yet the evolutionary underpinnings of the DR effect on lifespan are still widely debated. The leading theory suggests that this effect is adaptive and results from reallocation of resources from reproduction to somatic maintenance, in order to survive periods of famine in nature. However, such response would cease to be adaptive when DR is chronic and animals are selected to allocate more resources to reproduction. Nevertheless, chronic DR can also increase the strength of selection resulting in the evolution of more robust genotypes. We evolved Drosophila melanogaster fruit flies on 'DR', 'standard' and 'high' adult diets in replicate populations with overlapping generations. After approximately 25 generations of experimental evolution, male 'DR' flies had higher fitness than males from 'standard' and 'high' populations. Strikingly, this increase in reproductive success did not come at a cost to survival. Our results suggest that sustained DR selects for more robust male genotypes that are overall better in converting resources into energy, which they allocate mostly to reproduction.

The Metatron: an experimental system to study dispersal and metaecosystems for terrestrial organisms.

Dispersal of organisms generates gene flow between populations. Identifying factors that influence dispersal will help predict how species will cope with rapid environmental change. We developed an innovative infrastructure, the Metatron, composed of 48 interconnected patches, designed for the study of terrestrial organism movement as a model for dispersal. Corridors between patches can be flexibly open or closed. Temperature, humidity and illuminance can be independently controlled within each patch. The modularity and adaptability of the Metatron provide the opportunity for robust experimental design for the study of 'meta-systems'. We describe a pilot experiment on populations of the butterfly Pieris brassicae and the lizard Zootoca vivipara in the Metatron. Both species survived and showed both disperser and resident phenotypes. The Metatron offers the opportunity to test theoretical models in spatial ecology.

Short-term variation in sperm competition causes sperm-mediated epigenetic effects on early offspring performance in the zebrafish.

The inheritance of non-genetic factors is increasingly seen to play a major role in ecology and evolution. While the causes and consequences of epigenetic effects transmitted from the mother to the offspring have received ample attention, much less is known about how variation in the condition of the father affects the offspring. Here, we manipulated the intensity of sperm competition experienced by male zebrafish Danio rerio to investigate the potential for sperm-mediated epigenetic effects over a relatively short period of time. We found that the rapid responses of males to varying intensity of sperm competition not only affected sperm traits as shown previously, but also the performance of the resulting offspring. We observed that males exposed to high intensity of sperm competition produced faster swimming and more motile sperm, and sired offspring that hatched over a narrower time frame but exhibited a lower survival rate than males exposed to low intensity of sperm competition. Our results provide striking evidence for short-term paternal effects and the possible fitness consequences of such sperm-mediated non-genetic factors not only for the resulting offspring but also for the female.

Why ageing stops: heterogeneity explains late-life mortality deceleration in nematodes.

While ageing is commonly associated with exponential increase in mortality with age, mortality rates paradoxically decelerate late in life resulting in distinct mortality plateaus. Late-life mortality plateaus have been discovered in a broad variety of taxa, including humans, but their origin is hotly debated. One hypothesis argues that deceleration occurs because the individual probability of death stops increasing at very old ages, predicting the evolution of earlier onset of mortality plateaus under increased rate of extrinsic mortality. By contrast, heterogeneity theory suggests that mortality deceleration arises from individual differences in intrinsic lifelong robustness and predicts that variation in robustness between populations will result in differences in mortality deceleration. We used experimental evolution to directly test these predictions by independently manipulating extrinsic mortality rate (high or low) and mortality source (random death or condition-dependent) to create replicate populations of nematodes, Caenorhabditis remanei that differ in the strength of selection in late-life and in the level of lifelong robustness. Late-life mortality deceleration evolved in response to differences in mortality source when mortality rate was held constant, while there was no consistent response to differences in mortality rate. These results provide direct experimental support for the heterogeneity theory of late-life mortality deceleration.

The importance of habitat resistance for movement decisions in the common lizard, Lacerta vivipara.

BACKGROUND: Movement behaviour can be influenced by a multitude of biotic and abiotic factors. Here, we investigate the speed of movement in relation to environmental and individual phenotypic properties in subadult common lizards (Lacerta vivipara). We aim to disentangle the importance of substrate, cover, humidity, basking opportunity and individual phenotype on moving tendencies in 12 treatment combinations, at which each lizard was tested. RESULTS: We find that movement behaviour depends on the starting conditions, the physical properties of the dispersal corridor, and on the individuals' phenotype. Specifically, the presence of cover and substrate providing suitable traction in the corridor had positive effects on individual movement decisions. Additionally, we find high phenotypic variation in the propensity to move dependent on the presence of cover. Individual back patterns also strongly affected movement decisions in interaction with the physical properties of the dispersal corridor. CONCLUSIONS: Our results highlight the importance of understanding the habitat resistance for movement patterns, with humid habitats with covering vegetation providing the best conditions to initiate movement in the common lizard. In addition, population effects, differences in back pattern phenotype and individual plasticity were identified as key parameters influencing movement behaviour.

Effects of developmental and adult environments on ageing.

Developmental and adult environments can interact in complex ways to influence the fitness of individuals. Most studies investigating effects of the environment on fitness focus on environments experienced and traits expressed at a single point in an organism's life. However, environments vary with time, so the effects of the environments that organisms experience at different ages may interact to affect how traits change throughout life. Here, we test whether thermal stress experienced during development leads individuals to cope better with thermal stress as adults. We manipulated temperature during both development and adulthood and measured a range of life-history traits, including senescence, in male and female seed beetles (Callosobruchus maculatus). We found that thermal stress during development reduced adult reproductive performance of females. In contrast, life span and age-dependent mortality were affected more by adult than developmental environments, with high adult temperatures decreasing longevity and increasing age-dependent mortality. Aside from an interaction between developmental and adult environments to affect age-dependent changes in male weight, we did not find any evidence of a beneficial acclimation response to developmental thermal stress. Overall, our results show that effects of developmental and adult environments can be both sex and trait specific, and that a full understanding of how environments interact to affect fitness and ageing requires the integrated study of conditions experienced during different stages of ontogeny.

Sex-specific fitness effects of nutrient intake on reproduction and lifespan.

Diet affects both lifespan and reproduction [1-9], leading to the prediction that the contrasting reproductive strategies of the sexes should result in sex-specific effects of nutrition on fitness and longevity [6, 10] and favor different patterns of nutrient intake in males and females. However, males and females share most of their genome and intralocus sexual conflict may prevent sex-specific diet optimization. We show that both male and female longevity were maximized on a high-carbohydrate low-protein diet in field crickets Teleogryllus commodus, but male and female lifetime reproductive performances were maximized in markedly different parts of the nutrient intake landscape. Given a choice, crickets exhibited sex-specific dietary preference in the direction that increases reproductive performance, but this sexual dimorphism in preference was incomplete, with both sexes displaced from the optimum diet for lifetime reproduction. Sexes are, therefore, constrained in their ability to reach their sex-specific dietary optima by the shared biology of diet choice. Our data suggest that sex-specific selection has thus far failed fully to resolve intralocus sexual conflict over diet optimization. Such conflict may be an important factor linking nutrition and reproduction to lifespan and aging.

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.

Demographic costs of inbreeding revealed by sex-specific genetic rescue effects.

BACKGROUND: Inbreeding can slow population growth and elevate extinction risk. A small number of unrelated immigrants to an inbred population can substantially reduce inbreeding and improve fitness, but little attention has been paid to the sex-specific effects of immigrants on such "genetic rescue". We conducted two subsequent experiments to investigate demographic consequences of inbreeding and genetic rescue in guppies. RESULTS: Populations established from pairs of full siblings that were descended either from two generations of full-sibling inbreeding or unrelated outbred guppies did not grow at different rates initially, but when the first generation offspring started breeding, outbred-founded populations grew more slowly than inbred-founded populations. In a second experiment, adding two outbred males to the inbred populations resulted in significantly faster population growth than in control populations where no immigrants were added. Adding females resulted in growth at a rate intermediate to the control and male-immigrant treatments. CONCLUSION: The slower growth of the outbred-founded than inbred-founded populations is the opposite of what would be expected under inbreeding depression unless many deleterious recessive alleles had already been selectively purged in the inbreeding that preceded the start of the experiment, and that significant inbreeding depression occurred when the first generation offspring in outbred-founded populations started to inbreed. The second experiment revealed strong inbreeding depression in the inbred founded populations, despite the apparent lack thereof in these populations earlier on. Moreover, the fact that the addition of male immigrants resulted in the highest levels of population growth suggests that sex-specific genetic rescue may occur in promiscuous species, with male rescue resulting in higher levels of outbreeding than female rescue.

Sexual dimorphism in life history: age, survival, and reproduction in male and female field crickets Teleogryllus commodus under seminatural conditions.

Males and females differ in their reproductive strategies. Accordingly, sexually dimorphic optima in the allocation of resources to reproduction should select for sex-specific life histories, including sex-specific resolution of the key trade-off between reproduction and longevity. While males are expected to increase reproductive effort with increasing age under sexual selection theory, female reproductive effort should rather decrease after maturity, due to waning selection pressure at older ages. Sex differences in reproductive trade-offs and in the external mortality hazards experienced during the population's evolutionary history are both likely to shape sex differences in reproductive and actuarial (age-specific mortality) aging. Despite the importance of small-bodied, short-lived animals as laboratory models for life-history and aging studies, very little is known about sex differences in life-history patterns under natural conditions. Here, we tested for sex-specific patterns of reproductive and actuarial aging in field crickets under near-natural conditions. Both males and females showed actuarial senescence, with females exhibiting more rapid aging than males but with a later onset. Female and male reproductive effort showed a senescent decrease, with the peaks at different ages. Our findings provide the first demonstration of sexual dimorphism in age-dependent patterns of both survival and reproduction in an insect under near-natural conditions.

Sex effects on life span and senescence in the wild when dates of birth and death are unknown.

Males and females allocate and schedule reproductive effort in very different ways. Because the timing and amount of reproductive effort influence survival and thus the optimization of life histories, mortality and senescence are predicted to be sex specific. However, age-specific mortality rates of wild animals are often difficult to quantify in natural populations. Studies that report mortality rates from natural populations are, therefore, almost entirely confined to long-lived, easy-to-track species such as large mammals and birds. Here, we employ a novel approach using capture-mark-recapture data from a wild population of black field crickets (Teleogryllus commodus) to test for sex differences in demographic aging. In this species, the age of captured adults cannot be readily determined, and animals cannot be reliably captured or observed every night, resulting in demographic data on individuals whose dates of birth and death are unknown. We implement a recently developed life-table analysis for wild-caught individuals of unknown age, in combination with a well-established capture-mark-recapture methodology that models probabilistic dates of death. This unified analytical framework makes it possible to test for aging in wild, hard-to-track animals. Using these methods to fit Gompertz models of age-specific mortality, we show that male crickets have higher mortality rates throughout life than female crickets. Furthermore, males and females both exhibit increasing mortality rates with age, indicating senescence, but the rate of senescence is not sex specific. Thus, observed sex differences in longevity are probably due to differences in baseline mortality rather than aging. Our findings illustrate the complexity of the relationships between sex, background mortality, and senescence rate in wild populations, showing that the elevated mortality rate of males need not be coupled with an elevated rate of aging.

Evolution Under Dietary Restriction Decouples Survival From Fecundity in Drosophila melanogaster Females.

One of the key tenets of life-history theory is that reproduction and survival are linked and that they trade-off with each other. When dietary resources are limited, reduced reproduction with a concomitant increase in survival is commonly observed. It is often hypothesized that this dietary restriction effect results from strategically reduced investment in reproduction in favor of somatic maintenance to survive starvation periods until resources become plentiful again. We used experimental evolution to test this "waiting-for-the-good-times" hypothesis, which predicts that selection under sustained dietary restriction will favor increased investment in reproduction at the cost of survival because "good-times" never come. We assayed fecundity and survival of female Drosophila melanogaster fruit flies that had evolved for 50 generations on three different diets varying in protein content-low (classic dietary restriction diet), standard, and high-in a full-factorial design. High-diet females evolved overall increased fecundity but showed reduced survival on low and standard diets. Low-diet females evolved reduced survival on low diet without corresponding increase in reproduction. In general, there was little correspondence between the evolution of survival and fecundity across all dietary regimes. Our results contradict the hypothesis that resource reallocation between fecundity and somatic maintenance underpins life span extension under dietary restriction.

Reconciling strong stabilizing selection with the maintenance of genetic variation in a natural population of black field crickets (Teleogryllus commodus).

Genetic variation in single traits, including those closely related to fitness, is pervasive and generally high. By contrast, theory predicts that several forms of selection, including stabilizing selection, will eliminate genetic variation. Stabilizing selection in natural populations tends to be stronger than that assumed in theoretical models of the maintenance of genetic variation. The widespread presence of genetic variation in the presence of strong stabilizing selection is a persistent problem in evolutionary genetics that currently has no compelling explanation. The recent insight that stabilizing selection often acts most strongly on trait combinations via correlational selection may reconcile this problem. Here we show that for a set of male call properties in the cricket Teleogryllus commodus, the pattern of multivariate stabilizing sexual selection is closely associated with the degree of additive genetic variance. The multivariate trait combinations experiencing the strongest stabilizing selection harbored very little genetic variation while combinations under weak selection contained most of the genetic variation. Our experiment provides empirical support for the prediction that a small number of trait combinations experiencing strong stabilizing selection will have reduced genetic variance and that genetically independent trait combinations experiencing weak selection can simultaneously harbor much higher levels of genetic variance.

Antagonistic pleiotropy in species with separate sexes, and the maintenance of genetic variation in life-history traits and fitness.

Antagonistic pleiotropy (AP)-where alleles of a gene increase some components of fitness at a cost to others-can generate balancing selection, and contribute to the maintenance of genetic variation in fitness traits, such as survival, fecundity, fertility, and mate competition. Previous theory suggests that AP is unlikely to maintain variation unless antagonistic selection is strong, or AP alleles exhibit pronounced differences in genetic dominance between the affected traits. We show that conditions for balancing selection under AP expand under the likely scenario that the strength of selection on each fitness component differs between the sexes. Our model also predicts that the vast majority of balanced polymorphisms have sexually antagonistic effects on total fitness, despite the absence of sexual antagonism for individual fitness components. We conclude that AP polymorphisms are less difficult to maintain than predicted by prior theory, even under our conservative assumption that selection on components of fitness is universally sexually concordant. We discuss implications for the maintenance of genetic variation, and for inferences of sexual antagonism that are based on sex-specific phenotypic selection estimates-many of which are based on single fitness components.