Brief Communications: Rapid and Costly Ageing in Wild Male Flies

Ageing (senescence) has never been demonstrated convincingly in any insect in the wild, where mean life-spans are probably much shorter than in the laboratory1, and most evidence for senescence in other wild animals (such as mammals) is limited to their reduced survival with age2. Here we show that ageing is detectable in wild populations of a very short-lived insect, the antler fly (Protopiophila litigata), and causes debilitating and costly effects that force a decline not only in survival probability, but also in the reproductive rate of males. Our findings argue against the possibility of a trade-off between fitness components, whereby survival may decline without senescence if investment in reproduction increases with age3, and indicate that ageing rates are subject to intense selection in the wild. Although theory predicts the evolution of rapid senescence in organisms that experience high extrinsic (age-independent) mortality rates4, it has been suggested that very few individuals in these groups (such as insects or small mammals) survive long enough in the wild to exhibit detectable5,6 senescence. We tested for senescence in a wild population of the antler fly, a small dipteran that breeds exclusively on discarded antlers of moose and deer. The tendency of adult flies to spend their lives on a single antler, as well as the long duration of their mating (2.3 h; reference 7), facilitate the acquisition of field data on mating success and survival. We surveyed mating aggregations on nine moose antlers every 2 h over 72 days, and recorded the presence and mating status (single or coupled) of each of 609 individually marked males8

Offspring size variation within broods as a bet-hedging strategy in unpredictable environments

Offspring size is strikingly variable within species. Although theory can account for variation in offspring size among mothers, an adaptive explanation for variation within individual broods has proven elusive. Theoretical considerations of this problem assume that producing offspring that are too small results in reduced offspring viability, but producing offspring that are too large (for that environment) results only in a lost opportunity for increased fecundity. However, logic and recent evidence suggest that offspring above a certain size will also have lower fitness, such that mothers face fitness penalties on either side of an optimum. Although theory assuming intermediate optima has been developed for other diversification traits, the implications of this idea for selection on intra-brood variance in offspring size have not been explored theoretically. Here we model the fitness of mothers producing offspring of uniform vs. variable size in unpredictably variable environments and compare these two strategies under a variety of conditions. Our model predicts that producing variably sized offspring results in higher mean maternal fitness and less variation in fitness among generations when there is a maximum and minimum viable offspring size, and many mothers under- or over-estimate this optimum. This effect is especially strong when the viable offspring size range is narrow relative to the range of environmental variation. To determine whether this prediction is consistent with empirical evidence, we compare within- and among-mother variation in offspring size for 5 phyla of marine invertebrates with different developmental modes corresponding to contrasting levels of environmental predictability. Our comparative analysis reveals that in the developmental mode in which mothers are unlikely to anticipate the relationship between offspring size and performance, size-variation within mothers exceeds variation among mothers, but the converse is true when optimal offspring size is likely to be more predictable. Together, our results support the hypothesis that variation in offspring size within broods can reflect an adaptive strategy for dealing with unpredictably variable environments. We suggest that when there is a minimum and a maximum viable offspring size and the environment is unpredictable, selection will act on both the mean and variance of offspring size

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

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)

Complex coordination of cell plasticity by a PGC-1α-controlled transcriptional network in skeletal muscle

Skeletal muscle cells exhibit an enormous plastic capacity in order to adapt to external stimuli. Even though our overall understanding of the molecular mechanisms that underlie phenotypic changes in skeletal muscle cells remains poor, several factors involved in the regulation and coordination of relevant transcriptional programs have been identified in recent years. For example, the peroxisome proliferator-activated receptor γ coactivator-1α (PGC-1α) is a central regulatory nexus in the adaptation of muscle to endurance training. Intriguingly, PGC-1α integrates numerous signaling pathways and translates their activity into various transcriptional programs. This selectivity is in part controlled by differential expression of PGC-1α variants and post-translational modifications of the PGC-1α protein. PGC-1α-controlled activation of transcriptional networks subsequently enables a spatio-temporal specification and hence allows a complex coordination of changes in metabolic and contractile properties, protein synthesis and degradation rates and other features of trained muscle. In this review, we discuss recent advances in our understanding of PGC-1α-regulated skeletal muscle cell plasticity in health and disease

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

Evolution and Biodiversity: the evolutionary basis of biodiversity and its potential for adaptation to global change

Biodiversity has a key role in maintaining healthy ecosystems and thereby sustaining ecosystem services to the ever-growing human population. To get an idea of the range of ecosystem services that we use daily, think of how much energy and time it would cost to make Mars (or some other Earth-like planet) hospitable for human life, for example, in terms of atmosphere regulation, freshwater production, soil formation, nutrient cycles, regulation of climate, etc. On our own planet, that process took four billion years and required the contribution of a vast amount of functions performed by different life forms, ultimately driven by evolution and that is only the top of the (melting) iceberg.This Special Issue builds on the numerous contributions made during the EPBRS meeting on ‘Evolution and Biodiversity’ (Mallorca, 12–15 April 2010) and the preparatory e-conference chaired by J. Mergeay and managed by F. Grant. The meeting was funded by the Spanish Research Council (CSIC), the Spanish Diversitas Committee and EU-FW6 project BIOSTRAT. A full-report of the e-conference is available at: http://www.epbrs.org/PDF/EvolutionandBiodiversity_longversion_final.pdf. We thank A. Hendry for assistance during the editorial process.Peer Reviewe

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