Sperm storage by males causes changes in sperm phenotype and influences the reproductive fitness of males and their sons

Recent studies suggest that environmentally induced effects on sperm phenotype can influence offspring phenotype beyond the classic Mendelian inheritance mechanism. However, establishing whether such effects are conveyed purely through ejaculates, independently of maternal environmental effects, remains a significant challenge. Here, we assess whether environmentally induced effects on sperm phenotype affects male reproductive success and offspring fitness. We experimentally manipulated the duration of sperm storage by males, and thus sperm age, in the internally fertilizing fish Poecilia reticulata. We first confirm that sperm ageing influences sperm quality and consequently males reproductive success. Specifically, we show that aged sperm exhibit impaired velocity and are competitively inferior to fresh sperm when ejaculates compete to fertilize eggs. We then used homospermic (noncompetitive) artificial insemination to inseminate females with old or fresh sperm and found that male offspring arising from fertilizations by experimentally aged sperm suffered consistently impaired sperm quality when just sexually mature (four months old) and subsequently as adults (13 months old). Although we have yet to determine whether these effects have a genetic or epigenetic basis, our analyses provide evidence that environmentally induced variation in sperm phenotype constitutes an important source of variation in male reproductive fitness that has far reaching implications for offspring fitness

Divergent artificial selection for female reproductive investment has a sexually concordant effect on male reproductive success

This is the final version of the article. Available from Wiley via the DOI in this record.Depending on the genetic architecture of male and female fitness, sex-specific selection can have negative, positive, or neutral consequences for the opposite sex. Theory predicts that conflict between male and female function may drive the breakdown of intrasexual genetic correlations, allowing sexual dimorphism in sexually antagonistic traits. Reproductive traits are the epitome of this, showing highly differentiated proximate functions between the sexes. Here we use divergent artificial selection lines for female reproductive investment to test how female-specific selection on a sex-limited trait affects male reproductive success in a precocial bird, the Japanese quail (Coturnix japonica). We demonstrate that selection for increased egg investment in females positively affects male reproductive success both in competitive and non-competitive mating situations. This increased reproductive success was linked to a relatively larger left testis in males originating from lines selected for high female reproductive investment. Given that female quail have functional gonads only on their left side, this correlated response indicates that selection has acted on the shared developmental basis of male and female gonads. Our study thereby provides evidence for a positive genetic correlation between key reproductive traits in males and females despite a high degree of sexual dimorphism, and suggests that, in this system, selection on reproductive function is sexually concordant.The study was financially supported by the Swiss National Science Foundation (PP00P3_128386 and PP00P3_157455 to BT and P2ZHP3_164962 to JLP)

Dietary restriction fails to extend life in stressful environments

Moderate dietary restriction often prolongs life in laboratory animals, and this response has been interpreted as an adaptive strategy that promotes survival during famine. However, dietary restriction can also increase frailty, and it therefore remains unclear whether restricted diets prolong life under stressful conditions like those experienced by wild animals. We manipulated adult dietary protein of Drosophila melanogaster across a gradient of ambient temperature, and examined effects on survival. To test for trade-offs, we also quantified reproduction, and performance of F1, F2 and F3 descendants. We found that protein restriction increased longevity of one or both sexes at benign ambient temperatures (25°C and 27°C), but failed to extend longevity of flies maintained in cold (21°C and 23°C) or hot (29°C) conditions. Instead, in females, protein restriction resulted in strongly elevated mortality at cold temperatures. Protein restriction also generally reduced reproductive performance, and did not consistently enhance performance of F1, F2 or F3 descendants. Taken together, our results challenge the long-held idea that extended longevity of diet-restricted laboratory animals represents an adaptive survival strategy in natural populations. Our findings suggest instead that this response is an artefact of benign laboratory conditions, and that DR-induced life extension might not be achieved in the more stressful conditions experienced in the wild

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

Degree of adaptive male mate choice is positively correlated with female quality variance

When the cost of reproduction for males and variance in female quality are high, males are predicted to show adaptive mate choice. Using Drosophila melanogaster, we test this prediction and show that sperm limited males preferentially mated with young and/or well fed females. The preferred females had higher reproductive output – direct evidence of adaptive precopulatory male mate choice. Our most striking finding is the strong positive correlation between the degree of mating bias showed by the males and the variance in the fitness of the females. We discuss the possible mechanism for such adaptive male mate choice and propose that such choice has important consequences with respect to the existing understanding of the mating system and the evolution of aging

Reappraising Sexual Coevolution and the Sex Roles

Over recent decades, new ideas have radically altered how we see sex and reproduction. The implications of these ideas are still being explored, yielding intriguing discoveries

Increased copulation duration before ejaculate transfer is associated with larger spermatophores, and male genital titillators, across bushcricket taxa

Copulation duration varies considerably across species, but few comparative studies have examined factors that might underlie such variation. We examined the relationship between copulation duration (prior to spermatophore transfer), the complexity of titillators (sclerotized male genital contact structures), spermatophore mass and male body mass across 54 species of bushcricket. Using phylogenetic comparative analyses, we found that copulation duration was much longer in species with titillators than those without, but it was not longer in species with complex compared with simple titillators. A positive relationship was found between spermatophore size and copulation duration prior to ejaculate transfer, which supports the hypothesis that this represents a period of mate assessment. The slope of this relationship was steeper in species with simple rather than complex titillators. Although the data suggest that the presence of titillators is necessary to maintain long copulation prior to ejaculate transfer, mechanisms underlying this association remain unclear

Behavioral metabolution: the adaptive and evolutionary potential of metabolism-based chemotaxis

We use a minimal model of metabolism-based chemotaxis to show how a coupling between metabolism and behavior can affect evolutionary dynamics in a process we refer to as behavioral metabolution. This mutual influence can function as an in-the-moment, intrinsic evaluation of the adaptive value of a novel situation, such as an encounter with a compound that activates new metabolic pathways. Our model demonstrates how changes to metabolic pathways can lead to improvement of behavioral strategies, and conversely, how behavior can contribute to the exploration and fixation of new metabolic pathways. These examples indicate the potentially important role that the interplay between behavior and metabolism could have played in shaping adaptive evolution in early life and protolife. We argue that the processes illustrated by these models can be interpreted as an unorthodox instantiation of the principles of evolution by random variation and selective retention. We then discuss how the interaction between metabolism and behavior can facilitate evolution through (i) increasing exposure to environmental variation, (ii) making more likely the fixation of some beneficial metabolic pathways, (iii) providing a mechanism for in-the-moment adaptation to changes in the environment and to changes in the organization of the organism itself, and (iv) generating conditions that are conducive to speciatio

Response to multi-generational selection under elevated [CO₂] in two temperature regimes suggests enhanced carbon assimilation and increased reproductive output in <em>Brassica napus</em> L.

Functional plant traits are likely to adapt under the sustained pressure imposed by environmental changes through natural selection. Employing Brassica napus as a model, a multi-generational study was performed to investigate the potential trajectories of selection at elevated [CO(2)] in two different temperature regimes. To reveal phenotypic divergence at the manipulated [CO(2)] and temperature conditions, a full-factorial natural selection regime was established in a phytotron environment over the range of four generations. It is demonstrated that a directional response to selection at elevated [CO(2)] led to higher quantities of reproductive output over the range of investigated generations independent of the applied temperature regime. The increase in seed yield caused an increase in aboveground biomass. This suggests quantitative changes in the functions of carbon sequestration of plants subjected to increased levels of CO(2) over the generational range investigated. The results of this study suggest that phenotypic divergence of plants selected under elevated atmospheric CO(2) concentration may drive the future functions of plant productivity to be different from projections that do not incorporate selection responses of plants. This study accentuates the importance of phenotypic responses across multiple generations in relation to our understanding of biogeochemical dynamics of future ecosystems. Furthermore, the positive selection response of reproductive output under increased [CO(2)] may ameliorate depressions in plant reproductive fitness caused by higher temperatures in situations where both factors co-occur

Senescence and Sexual Selection in a Pelagic Copepod

The ecology of senescence in marine zooplankton is not well known. Here we demonstrate senescence effects in the marine copepod Oithona davisae and show how sex and sexual selection accelerate the rate of ageing in the males. We show that adult mortality increases and male mating capacity and female fertility decrease with age and that the deterioration in reproductive performance is faster for males. Males have a limited mating capacity because they can fertilize < 2 females day−1 and their reproductive life span is 10 days on average. High female encounter rates in nature (>10 day−1), a rapid age-dependent decline in female fertility, and a high mortality cost of mating in males are conducive to the development of male choosiness. In our experiments males in fact show a preference for mating with young females that are 3 times more fertile than 30-day old females. We argue that this may lead to severe male-male competition for young virgin females and a trade-off that favours investment in mate finding over maintenance. In nature, mate finding leads to a further elevated mortality of males, because these swim rapidly in their search for attractive partners, further relaxing fitness benefits of maintenance investments. We show that females have a short reproductive period compared to their average longevity but virgin females stay fertile for most of their life. We interpret this as an adaptation to a shortage of males, because a long life increases the chance of fertilization and/or of finding a high quality partner. The very long post reproductive life that many females experience is thus a secondary effect of such an adaptation