A polygenic basis for birth weight in a wild population of red deer (Cervus elaphus).

The genetic architecture of traits under selection has important consequences for the response to selection and potentially for population viability. Early QTL mapping studies in wild populations have reported loci with large effect on trait variation. However, these results are contradicted by more recent genome-wide association analyses, which strongly support the idea that most quantitative traits have a polygenic basis. This study aims to re-evaluate the genetic architecture of a key morphological trait, birth weight, in a wild population of red deer (Cervus elaphus), using genomic approaches. A previous study using 93 microsatellite and allozyme markers and linkage mapping on a kindred of 364 deer detected a pronounced QTL on chromosome 21 explaining 29% of the variance in birth weight, suggesting that this trait is partly controlled by genes with large effects. Here, we used data for more than 2,300 calves genotyped at >39,000 SNP markers and two approaches to characterise the genetic architecture of birth weight. First, we performed a genome-wide association (GWA) analysis, using a genomic relatedness matrix to account for population structure. We found no SNPs significantly associated with birth weight. Second, we used genomic prediction to estimate the proportion of variance explained by each SNP and chromosome. This analysis confirmed that most genetic variance in birth weight was explained by loci with very small effect sizes. Third, we found that the proportion of variance explained by each chromosome was slightly positively correlated with its size. These three findings highlight a highly polygenic architecture for birth weight, which contradicts the previous QTL study. These results are probably explained by the differences in how associations are modelled between QTL mapping and GWA. Our study suggests that models of polygenic adaptation are the most appropriate to study the evolutionary trajectory of this trait.

Maternal effects do not resolve the paradox of stasis in birth weight in a wild red deer populaton.

In natural populations, quantitative traits seldom show short-term evolution at the rate predicted by evolutionary models. Resolving this "paradox of stasis" is a key goal in evolutionary biology, as it directly challenges our capacity to predict evolutionary change. One particularly promising hypothesis to explain the lack of evolutionary responses in a key offspring trait, body weight, is that positive selection on juveniles is counterbalanced by selection against maternal investment in offspring growth, given that reproduction is costly for the mothers. Here, we used data from one of the longest individual-based studies of a wild mammal population to test this hypothesis. We first showed that despite positive directional selection on birth weight, and heritable variation for this trait, no genetic change has been observed for birth weight over the past 47 years in the study population. Contrarily to our expectation, we found no evidence of selection against maternal investment in birth weight-if anything, selection favors mothers that produce large calves. Accordingly, we show that genetic change in birth weight over the study period is actually lower than that predicted from models including selection on maternal performance; ultimately our analysis here only deepens rather than resolves the paradox of stasis.

Larval diet affects adult reproduction, but not survival, independent of the effect of injury and infection in Drosophila melanogaster.

Early-life conditions have profound effects on many life-history traits, where early-life diet affects both juvenile development, and adult survival and reproduction. Early-life diet also has consequences for the ability of adults to withstand environmental challenges such as starvation, temperature and desiccation. However, it is less well known how early-life diet influences the consequences of infection in adults. Here we test whether varying the larval diet of female Drosophila melanogaster (through altering protein to carbohydrate ratio, P:C) influences the long-term consequences of injury and infection with the bacterial pathogen Pseudomonasentomophila. Given previous work manipulating adult dietary P:C, we predicted that adults from larvae raised on higher P:C diets would have increased reproduction, but shorter lifespans and an increased rate of ageing, and that the lowest larval P:C diets would be particularly detrimental for adult survival in infected individuals. For larval development, we predicted that low P:C would lead to a longer development time and lower viability. We found that early-life and lifetime egg production were highest at intermediate to high larval P:C diets, but this was independent of injury and infection. There was no effect of larval P:C on adult survival. Larval development was quickest on intermediate P:C and egg-to-pupae and egg-to-adult viability were slightly higher on higher P:C. Overall, despite larval P:C affecting several measured traits, we saw no evidence that larval P:C altered the consequence of infection or injury for adult survival or early-life and lifetime reproduction. Taken together, these data suggest that larval diets appear to have a limited impact on the adult life history consequences of infection.

Vector control: agents of selection on malaria parasites?

Insect vectors are responsible for spreading many infectious diseases, yet interactions between pathogens/parasites and insect vectors remain poorly understood. Filling this knowledge gap matters because vectors are evolving in response to the deployment of vector control tools (VCTs). Yet, whilst the evolutionary responses of vectors to VCTs are being carefully monitored, the knock-on consequences for parasite evolution have been overlooked. By examining how mosquito responses to VCTs impact upon malaria parasite ecology, we derive a framework for predicting parasite responses. Understanding how VCTs affect the selection pressures imposed on parasites could help to mitigate against parasite evolution that leads to unfavourable epidemiological outcomes. Furthermore, anticipating parasite evolution will inform monitoring strategies for VCT programmes as well as uncovering novel VCT strategies.

The role of maternally transferred antibodies in maternal performance in red deer.

Maternal effects are ubiquitous. Yet, the pathways through which maternal effects occur in wild mammals remain largely unknown. We hypothesise that maternal immune transfer is a key mechanism by which mothers can affect their offspring fitness, and that individual variation in maternally derived antibodies mainly depends on a mother's characteristics and the environmental conditions she experiences. To test this, we assayed six colostrum-derived antibodies in the plasma of 1447 neonates in a wild red deer population. Neonatal antibody levels were mainly affected by maternal genes, environmental variation and costs of prior reproductive investment. We found consistent heterogeneity in maternal performance across traits, with mothers producing the heaviest calves also having calves with more antibodies. Unexpectedly, antibody levels were not associated with calf survival. We provide a unique example of how evolutionary theory on maternal effects can be used to gain insight into the causes of maternal effects in wild populations.

Lifespan Extension Via Dietary Restriction: Time to Reconsider the Evolutionary Mechanisms?

Dietary restriction (DR) is the most consistent environmental manipulation to extend lifespan. Originally thought to be caused by a reduction in caloric intake, recent evidence suggests that macronutrient intake underpins the effect of DR. The prevailing evolutionary explanations for the DR response are conceptualized under the caloric restriction paradigm, necessitating reconsideration of how or whether these evolutionary explanations fit this macronutrient perspective. In the authors' opinion, none of the current evolutionary explanations of DR adequately explain the intricacies of observed results; instead a context-dependent combination of these theories is suggested which is likely to reflect reality. In reviewing the field, it is proposed that the ability to track the destination of different macronutrients within the body will be key to establishing the relative roles of the competing theories. Understanding the evolution of the DR response and its ecological relevance is critical to understanding variation in DR responses and their relevance outside laboratory environments.

The genetic architecture of maternal effects across ontogeny in the red deer.

Maternal effects, either environmental or genetic in origin, are an underappreciated source of phenotypic variance in natural populations. Maternal genetic effects have the potential to constrain or enhance the evolution of offspring traits depending on their magnitude and their genetic correlation with direct genetic effects. We estimated the maternal effect variance and its genetic component for 12 traits expressed over the life history in a pedigreed population of wild red deer (morphology, survival/longevity, breeding success). We only found support for maternal genetic effect variance in the two neonatal morphological traits: birth weight ( hMg2 = 0.31) and birth leg length ( hMg2 = 0.17). For these two traits, the genetic correlation between maternal and direct additive effects was not significantly different from zero, indicating no constraint to evolution from genetic architecture. In contrast, variance in maternal genetic effects enhanced the additive genetic variance available to respond to natural selection. Maternal effect variance was negligible for late-life traits. We found no evidence for sex differences in either the direct or maternal genetic architecture of offspring traits. Our results suggest that maternal genetic effect variance declines over the lifetime, but also that this additional heritable genetic variation may facilitate evolutionary responses of early-life traits.

Reconciling nutritional geometry with classical dietary restriction: Effects of nutrient intake, not calories, on survival and reproduction.

Dietary restriction (DR) is one of the main experimental paradigms to investigate the mechanisms that determine lifespan and aging. Yet, the exact nutritional parameters responsible for DR remain unclear. Recently, the advent of the geometric framework of nutrition (GF) has refocussed interest from calories to dietary macronutrients. However, GF experiments focus on invertebrates, with the importance of macronutrients in vertebrates still widely debated. This has led to the suggestion of a fundamental difference in the mode of action of DR between vertebrates and invertebrates, questioning the suggestion of an evolutionarily conserved mechanism. The use of dietary dilution rather than restriction in GF studies makes comparison with traditional DR studies difficult. Here, using a novel nonmodel vertebrate system (the stickleback fish, Gasterosteus aculeatus), we test the effect of macronutrient versus calorie intake on key fitness-related traits, both using the GF and avoiding dietary dilution. We find that the intake of macronutrients rather than calories determines both mortality risk and reproduction. Male mortality risk was lowest on intermediate lipid intakes, and female risk was generally reduced by low protein intakes. The effect of macronutrient intake on reproduction was similar between the sexes, with high protein intakes maximizing reproduction. Our results provide, to our knowledge, the first evidence that macronutrient, not caloric, intake predicts changes in mortality and reproduction in the absence of dietary dilution. This supports the suggestion of evolutionary conservation in the effect of diet on lifespan, but via variation in macronutrient intake rather than calories.

Estimating selection on the act of inbreeding in a population with strong inbreeding depression.

Inbreeding depression is widely regarded as a driving force in the evolution of dispersal, mate choice and sperm selection. However, due to likely costs of inbreeding avoidance, which are poorly understood, it is unclear to what extent selection to avoid inbreeding is expected in nature. Moreover, there are currently very few empirical estimates of the strength of selection against the act of inbreeding (mating with a relative), as opposed to the fitness costs of being inbred. Here, we use data from the individual-based study of red deer on the Scottish island of Rum, a strongly polygynous system which harbours a large inbreeding load, to estimate selection against the act of inbreeding for each sex. We use pedigree and genomic estimates of relatedness between individuals and measure fitness using both lifetime breeding success (number of calves born) and lifetime reproductive success (number of calves surviving to independence), with the latter incorporating inbreeding depression in calf survival. We find for both sexes that the repeatability of the act of inbreeding was low (< 0.1), suggesting little among-individual variation for this trait on which selection can act. Using the genomic measures, there was significant selection against the act of inbreeding in males, but not in females, and there was considerable uncertainty in the estimate in both sexes. We discuss possible explanations for these patterns and their implications for understanding the evolution of inbreeding avoidance in natural populations.

Inbreeding, inbreeding depression, and infidelity in a cooperatively breeding bird.

Inbreeding depression plays a major role in shaping mating systems: in particular, inbreeding avoidance is often proposed as a mechanism explaining extra-pair reproduction in socially monogamous species. This suggestion relies on assumptions that are rarely comprehensively tested: that inbreeding depression is present, that higher kinship between social partners increases infidelity, and that infidelity reduces the frequency of inbreeding. Here, we test these assumptions using 26 years of data for a cooperatively breeding, socially monogamous bird with high female infidelity, the superb fairy-wren (Malurus cyaneus). Although inbred individuals were rare (∼6% of offspring), we found evidence of inbreeding depression in nestling mass (but not in fledgling survival). Mother-son social pairings resulted in 100% infidelity, but kinship between a social pair did not otherwise predict female infidelity. Nevertheless, extra-pair offspring were less likely to be inbred than within-pair offspring. Finally, the social environment (the number of helpers in a group) did not affect offspring inbreeding coefficients or inbreeding depression levels. In conclusion, despite some agreement with the assumptions that are necessary for inbreeding avoidance to drive infidelity, the apparent scarcity of inbreeding events and the observed levels of inbreeding depression seem insufficient to explain the ubiquitous infidelity in this system, beyond the mother-son mating avoidance.

The relationship between telomere length and mortality risk in non-model vertebrate systems: a meta-analysis.

Telomere length (TL) has become a biomarker of increasing interest within ecology and evolutionary biology, and has been found to predict subsequent survival in some recent avian studies but not others. Here, we undertake the first formal meta-analysis to test whether there is an overall association between TL and subsequent mortality risk in vertebrates other than humans and model laboratory rodents. We identified 27 suitable studies and obtained standardized estimates of the hazard ratio associated with TL from each. We performed a meta-analysis on these estimates and found an overall significant negative association implying that short telomeres are associated with increased mortality risk, which was robust to evident publication bias. While we found that heterogeneity in the hazard ratios was not explained by sex, follow-up period, maximum lifespan or the age group of the study animals, the TL-mortality risk association was stronger in studies using qPCR compared to terminal restriction fragment methodologies. Our results provide support for a consistent association between short telomeres and increased mortality risk in birds, but also highlight the need for more research into non-avian vertebrates and the reasons why different telomere measurement methods may yield different results.This article is part of the theme issue 'Understanding diversity in telomere dynamics'.

Phenotypic and genetic integration of personality and growth under competition in the sheepshead swordtail, Xiphophorus birchmanni.

Competition for resources including food, physical space, and potential mates is a fundamental ecological process shaping variation in individual phenotype and fitness. The evolution of competitive ability, in particular social dominance, depends on genetic (co)variation among traits causal (e.g., behavior) or consequent (e.g., growth) to competitive outcomes. If dominance is heritable, it will generate both direct and indirect genetic effects (IGE) on resource-dependent traits. The latter are expected to impose evolutionary constraint because winners necessarily gain resources at the expense of losers. We varied competition in a population of sheepshead swordtails, Xiphophorus birchmanni, to investigate effects on behavior, size, growth, and survival. We then applied quantitative genetic analyses to determine (i) whether competition leads to phenotypic and/or genetic integration of behavior with life history and (ii) the potential for IGE to constrain life history evolution. Size, growth, and survival were reduced at high competition. Male dominance was repeatable and dominant individuals show higher growth and survival. Additive genetic contributions to phenotypic covariance were significant, with the G matrix largely recapitulating phenotypic relationships. Social dominance has a low but significant heritability and is strongly genetically correlated with size and growth. Assuming causal dependence of growth on dominance, hidden IGE will therefore reduce evolutionary potential.

Body macronutrient composition is predicted by lipid and not protein content of the diet.

Diet is an important determinant of fitness-related traits including growth, reproduction, and survival. Recent work has suggested that variation in protein:lipid ratio and particularly the amount of protein in the diet is a key nutritional parameter. However, the traits that mediate the link between dietary macronutrient ratio and fitness-related traits are less well understood. An obvious candidate is body composition, given its well-known link to health. Here, we investigate the relationship between dietary and body macronutrient composition using a first-generation laboratory population of a freshwater fish, the three-spine stickleback (Gasterosteus aculeatus). Carbohydrate is relatively unimportant in the diet of predatory fish, facilitating the exploration of how dietary protein-to-lipid ratio affects their relative deposition in the body. We find a significant effect of lipid intake, rather than protein, on body protein:lipid ratio. Importantly, this was not a result of absorbing macronutrients in relation to their relative abundance in the diet, as the carcass protein:lipid ratios differed from those of the diets, with ratios usually lower in the body than in the diet. This indicates that individuals can moderate their utilization, or uptake, of ingested macronutrients to reach a target balance within the body. We found no effect of diet on swimming endurance, activity, or testes size. However, there was an effect of weight on testes size, with larger males having larger testes. Our results provide evidence for the adjustment of body protein:lipid ratio away from that of the diet. As dietary lipid intake was the key determinant of body composition, we suggest this occurs via metabolism of excess protein, which conflicts with the predictions of the protein leverage hypothesis. These results could imply that the conversion and excretion of protein is one of the causes of the survival costs associated with high-protein diets.

Measuring selection for genes that promote long life in a historical human population.

The unusually long lifespans of humans and the persistence of post-reproductive lifespans in women represent evolutionary puzzles because natural selection cannot directly favour continued living in post-menopausal women or elderly men. Suggested sources of indirect selection require genetic correlations between fitness and survival or reproduction at younger ages, reproduction in the opposite sex, or late-life contributions to offspring or grandoffspring fitness. Here we apply quantitative genetic analyses to data from a historical human population to explicitly test these evolutionary genetic hypotheses. Total genetic selection increased the male post-50 lifespans by 0.138 years per generation; 94% of this arose from indirect selection acting to favour early-life fitness in both sexes. These results argue strongly against life-history models of ageing that depend on trade-offs between reproduction and late-life survival. No source of indirect selection for female post-50 lifespan was detected, deepening the mystery of why female post-reproductive survival persists. This result is probably due to recent changes in the genetic architecture of female lifespan, and it highlights the need for similar quantitative genetic analyses of human populations at other points along demographic transitions.

The effect of dietary restriction on reproduction: a meta-analytic perspective.

BACKGROUND: Dietary restriction (DR), a reduction in the amount of food or particular nutrients eaten, is the most consistent environmental manipulation to extend lifespan and protect against age related diseases. Current evolutionary theory explains this effect as a shift in the resolution of the trade-off between lifespan and reproduction. However, recent studies have questioned the role of reproduction in mediating the effect of DR on longevity and no study has quantitatively investigated the effect of DR on reproduction across species. RESULTS: Here we report a comprehensive comparative meta-analysis of the effect of DR on reproduction. In general, DR reduced reproduction across taxa, but several factors moderated this effect. The effect of DR on reproduction was greater in well-studied model species (yeast, nematode worms, fruit flies and rodents) than non-model species. This mirrors recent results for longevity and, for reproduction, seems to result from a faster rate of decline with decreasing resources in model species. Our results also suggested that not all reproductive traits are affected equally by DR. High and moderate cost reproductive traits suffered a significant reduction with DR, but low cost traits, such as ejaculate production, did not. Although the effect of DR on reproduction was stronger in females than males, this sex difference reduced to near zero when accounting for other co-factors such as the costliness of the reproductive trait. Thus, sex differences in the effect of DR on longevity may be due to a failure to expose males to as complete a range of the costs of reproduction as females. CONCLUSIONS: We suggest that to better understand the generality of the effect of DR, future studies should attempt to address the cause of the apparent model species bias and ensure that individuals are exposed to as many of the costs of reproduction as possible. Furthermore, our meta-analytic approach reveals a general shortage of DR studies that record reproduction, particularly in males, as well as a lack of direct side-by-side comparisons of the effect of DR on males and females.

Relative costs of offspring sex and offspring survival in a polygynous mammal.

Costs of reproduction are expected to be ubiquitous in wild animal populations and understanding the drivers of variation in these costs is an important aspect of life-history evolution theory. We use a 43 year dataset from a wild population of red deer to examine the relative importance of two factors that influence the costs of reproduction to mothers, and to test whether these costs vary with changing ecological conditions. Like previous studies, our analyses indicate fitness costs of lactation: mothers whose calves survived the summer subsequently showed lower survival and fecundity than those whose calves died soon after birth, accounting for 5% and 14% of the variation in mothers' survival and fecundity, respectively. The production of a male calf depressed maternal survival and fecundity more than production of a female, but accounted for less than 1% of the variation in either fitness component. There was no evidence for any change in the effect of calf survival or sex with increasing population density.

Testosterone and cortisol concentrations vary with reproductive status in wild female red deer.

Although hormones are key regulators of many fitness and life history traits, the causes of individual level variation in hormones, particularly in wild systems, remain understudied. Whilst we know that androgen and glucocorticoid levels vary within and among individuals in mammalian populations, how this relates to key reproductive processes such as gestation and lactation, and their effects on a female's measurable hormone levels are poorly understood in wild systems. Using fecal samples collected from females in a wild red deer population between 2001 and 2013, we explore how fecal androgen (FAM) and cortisol (FCM) metabolite concentrations change with age and season, and how individual differences relate to variation in reproductive state. Both FAM and FCM levels increase toward parturition, although this only affects FCM levels in older females. FCM levels are also higher when females suckle a male rather than a female calf, possibly due to the higher energetic costs of raising a son. This illustrates the importance of accounting for a female's life history and current reproductive status, as well as temporal variation, when examining individual differences in hormone levels. We discuss these findings in relation to other studies of mammalian systems and in particular to the relatively scarce information on variation in natural levels of hormones in wild populations.

Transcriptomes of parents identify parenting strategies and sexual conflict in a subsocial beetle.

Parenting in the burying beetle Nicrophorus vespilloides is complex and, unusually, the sex and number of parents that can be present is flexible. Such flexibility is expected to involve specialized behaviour by the two sexes under biparental conditions. Here, we show that offspring fare equally well regardless of the sex or number of parents present. Comparing transcriptomes, we find a largely overlapping set of differentially expressed genes in both uniparental and biparental females and in uniparental males including vitellogenin, associated with reproduction, and takeout, influencing sex-specific mating and feeding behaviour. Gene expression in biparental males is similar to that in non-caring states. Thus, being 'biparental' in N. vespilloides describes the family social organization rather than the number of directly parenting individuals. There was no specialization; instead, in biparental families, direct male parental care appears to be limited with female behaviour unchanged. This should lead to strong sexual conflict.

Cortisol but not testosterone is repeatable and varies with reproductive effort in wild red deer stags.

Although it is known that hormone concentrations vary considerably between individuals within a population, how they change across time and how they relate to an individual's reproductive effort remains poorly quantified in wild animals. Using faecal samples collected from wild red deer stags, we examined sources of variation in faecal cortisol and androgen metabolites, and the potential relationship that these might have with an index of reproductive effort. We also biologically validated an assay for measuring androgen metabolites in red deer faeces. We show that variation in hormone concentrations between samples can be accounted for by the age of the individual and the season when the sample was collected. Faecal cortisol (but not androgen) metabolites also showed significant among-individual variation across the 10-year sampling time period, which accounted for 20% of the trait's phenotypic variance after correcting for the age and season effects. Finally, we show that an index of male reproductive effort (cumulative harem size) during the mating season (rut) was positively correlated with male cortisol concentrations, both among and within individuals. We suggest that the highest ranking males have the largest cumulative harem sizes (i.e. invest the greatest reproductive effort), and that this social dominance may have associated behaviours such as increased frequency of agonistic interactions which are associated with corresponding high levels of faecal cortisol metabolites (FCM).