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

<p>Abstract</p> <p>Background</p> <p>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.</p> <p>Results</p> <p>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.</p> <p>Conclusion</p> <p>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.</p

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

High-protein paternal diet confers an advantage to sons in sperm competition

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

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

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.SRKZ and ML were supported by the Australian (ARC) Discovery Grant (DP180100818) awarded to SN. JM was supported by EMBL core funding and the NIH Common Fund (UM1-H G006370). AMS was supported by an ARC fellowship (DE180101520)

No Intra-Locus Sexual Conflict over Reproductive Fitness or Ageing in Field Crickets

Differences in the ways in which males and females maximize evolutionary fitness can lead to intra-locus sexual conflict in which genes delivering fitness benefits to one sex are costly when expressed in the other. Trade-offs between current reproductive effort and future reproduction and survival are fundamental to the evolutionary biology of ageing. This leads to the prediction that sex differences in the optimization of age-dependent reproductive effort may generate intra-locus sexual conflict over ageing rates. Here we test for intra-locus sexual conflict over age-dependent reproductive effort and longevity in the black field cricket, Teleogryllus commodus. Using a half-sib breeding design, we show that the most important components of male and female reproductive effort (male calling effort and the number of eggs laid by females) were positively genetically correlated, especially in early adulthood. However, the genetic relationships between longevity and reproductive effort were different for males and females, leading to low genetic covariation between male and female longevity. The apparent absence of intra-locus sexual conflict over ageing suggests that male and female longevity can evolve largely independently of one another

The diversity of population responses to environmental change

This is the final version. Available from Wiley via the DOI in this record.Data available from the Dryad Digital Repository: https:// doi.org/10.5061/dryad.d5f54s7The 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.Max Planck Society, Marie Curie FellowshipERCGerman Research FoundationSwiss National Science FoundationNational Science FoundationNational Institute of AgingRamon y Cajal Research GrantWenner-Gren FoundationLeakey FoundationNational Geographic SocietyZoological Society of San DiegoUniversity of PennsylvaniaArgentinean National Council of Researc

Data from: High-protein paternal diet confers an advantage to sons in sperm competition

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

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

PaternityDataDietaryTransgenEffects

Results of sperm competition outcomes (i.e. numbers of offspring sired) of sons of fathers that had been reared on either a 4:1 protein:carbohydrate (P:C) ratio ("high", H) or 1:1 P:C ratio ("low", L)