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Sepil, I.

Publications and source records attributed to Sepil, I..

At least 19 recordsLinked to original sources

Strength of developmental carry-over varies continuously with environmental conditions in a wild bird population

Early-life phenotypes frequently predict adult phenotypes through developmental 'silver-spoon' carry-over effects, but how strongly and under what circumstances? Using 40 years of individual-based data from a great tit (Parus major) population, we used covariance reaction norms to understand how the natal-to-adult body mass association shifts across temperature, rainfall, and population density gradients during both life stages. We show that the natal-adult mass correlation is substantial (r {approx} 0.7) but strongly environment-dependent. Reaction norm shapes across climatic and density axes point to distinct mechanisms, including compensatory growth under benign adult conditions and density-dependent modulation of early-life differences. We further show that the conditions experienced in adulthood largely drive these patterns and determine whether early-life advantages are retained, even when explicitly tested within an environmental-matching paradigm. Decomposing the correlation using 38 generations of pedigree data revealed no evidence of gene-by-environment interactions. Instead, the observed phenotypic correlation reaction norms could be attributed almost entirely to environmentally-sensitive non-genetic individual differences. Overall, our findings show that climatic and demographic shifts can substantially reshape developmental carry-over without altering the genetic architecture tying body mass across life stages, with implications for how reliably early-life mass can predict individual quality and adult traits in wild animal populations.

ecology↗

Developmental stage-specific responses to extreme climatic events and environmental variability in great tit nestlings

Climate change poses a pervasive threat to many aspects of natural systems, and while impacts of changes in average conditions have been extensively studied, the effects of increased climate variability, and extreme events, on natural populations are less understood due to the challenges of studying these rare occurrences. Using 60 years of life-history data from over 83,000 individuals, and historical daily climate records, we show that developmental stages in wild great tits (Parus major) differ in their sensitivity to extreme climatic events (ECEs). Exposure to extreme cold events during the first week of development is particularly detrimental to fledging mass, while extreme rain events have a stronger negative impact as chicks grow older and their energetic requirements increase. Synergistic effects of ECEs and average climatic conditions can be particularly severe, exacerbating the challenges faced by these birds. Our findings indicate that combined exposure to extreme heat and heavy rainfall during early development is associated with a predicted reduction in fledging mass by up to 27%. Additionally, birth timing may further modulate these effects, since late-season broods exposed to frequent hot ECEs during early development are predicted to fledge nestlings up to 4.27 standard deviations (35%) lighter than broods laid earlier in the season. Moreover, phenotypic plasticity has enabled many similar populations to shift towards an overall earlier laying date, which may have increased susceptibility to cold extremes during development. However, our analyses suggest that the benefits of being part of an early-laid clutch within a season may, to some extent, offset the negative effects of extreme climate on fledging mass and apparent survival. In climate scenarios where ECEs are predicted to increase in frequency, duration, and severity, these developmental stage-specific insights are crucial for understanding how climate change may be influencing wild avian populations.

ecology↗

Chilling out or heating up? Thermal plasticity of seminal fluid proteins in Drosophila melanogaster

Seminal fluid proteins (SFPs) play crucial roles in reproduction by shaping female post-mating physiology and behaviour, male sperm competition, and sexual conflict between the sexes. However, we mostly ignore how abiotic ecological factors regulate SFP expression and transfer. Here, we use quantitative proteomics in adult flies from a wild Drosophila melanogaster population to test how exposure to natural temperature variation (20{degrees}C, 24{degrees}C and 28{degrees}C) across two-time scales (48h and 13d), and under either no or high sperm competition risk, interact to shape SFP production and transfer. We show that both production and transfer of SFPs was reduced after long-term (13d) exposure to low (20{degrees}C) and high (28{degrees}C) temperatures, including in key proteins (sex peptide and ovulin networks) mediating female post-copulatory responses, sperm competition and sexual conflict. Our results show that natural temperature fluctuations can have a strong effect on SFP production and transfer, and thus on post-copulatory sexual selection dynamics.

evolutionary biology↗

Mechanisms of phenotypic trade-offs in the resource acquisition-allocation Y-model

Phenotypic trade-offs, predicted to occur due to resource constraints, are not commonly observed. This discrepancy is often explained by the Y-model, which shows that greater variation in resource acquisition (CVA) than variation in allocation strategy (CVX) masks among-individual phenotypic trade-offs. However, the Y-model is a heuristic rather than a quantitative tool with testable predictions. Additionally, the mechanisms modulating trade-offs in the model remain unclear. Here, we simulate different parameters of the Y-model to understand their influence. We find that CVA/(CVA + CVX) accurately predicts the direction and strength of phenotypic correlations. Contrary to common assumptions, the mean resource acquired by a population does not influence trade-offs; instead, the mean allocation strategy of a population does. Importantly, within-individual dependence of allocation on acquisition exacerbates the influence of mean allocation. This causes greater sensitivity of phenotypic correlations to changes in CVA or CVX, compared to independent resource acquisition and allocation strategies. We generate novel, testable hypotheses about trade-offs in the context of dietary restriction, plasticity, polymorphism, and pace-of-life, and validate our model with empirical data to demonstrate its robustness. By systematically partitioning the influence of means, variances, and covariance, in the acquisition-allocation Y-model, we provide a simple, generalisable, quantitative synthesis for understanding phenotypic trade-offs.

evolutionary biology↗

Sperm storage reduces sperm and embryo quality in animals

In many animals, sperm are stored for extended periods either in the reproductive tracts of males before ejaculation, or of females after copulation. Sperm storage reduces the risk of sperm limitation in both sexes and avoids the costs of female re-mating. However, sperm storage can lead to post-meiotic sperm senescence, i.e. within-sperm-age-dependent deterioration, potentially impacting conceived offspring and lowering male and female fitness. Yet, the extent and magnitude of such deterioration and the variables modulating it during sperm storage are not well understood. Using a meta-analysis across humans (115 studies) and non-human animals (56 studies from 30 species), we investigate how in-vivo sperm storage affects sperm quality, fertilisation success, and offspring quality. In humans, sperm storage leads to greater sperm oxidative stress and DNA damage, and reduces sperm viability and motility. In other animals, sperm performance and embryo quality decline. We identify the duration of sperm storage, the design used for sampling individuals, and the sex of the individual storing sperm as potentially important moderators of the effects of sperm storage. These findings have key biomedical implications, including optimising the timing of ejaculation and fertilisation in fertility clinics or captive breeding programs. Overall, our results reveal the mechanisms that cause post-meiotic sperm senescence, the fitness consequences of sperm storage, and provide evolutionary insights into sex-specific adaptations that potentially mitigate the detrimental effects of sperm storage.

evolutionary biology↗

The developmental environment mediates adult seminal proteome allocation in male Drosophila melanogaster

Early life conditions can have long-lasting fitness effects on organisms. In insects, crowding during larval stages impose a significant constraint on adult phenotypes due to increased intraspecific competition for resources, which can modulate males success in pre- and post-mating competition in adulthood. Evidence for larval crowding effects on male seminal fluid allocation exists but is limited to a small subset of well-known seminal fluid proteins (Sfps), and often overlooks the interactions between male and female phenotypes. We currently lack a comprehensive understanding of how male and female larval crowding interact to affect production, composition, and transfer of the wider seminal proteome. Here, we manipulated Drosophila melanogaster larval crowding (low versus high) of males and females to generate individuals with large and small body size, respectively. We mated individuals in a fully factorial design, and measured the abundance, composition, and transfer of Sfps. Large males produced Sfps in significantly higher abundances, yet this difference was marginal and not detected when Sfps were analysed individually. Conversely, small males transferred greater quantities of much of their seminal proteome to females than did large males. When analysing proteins individually, 10 Sfps were transferred in significantly higher abundances by small males than large males. Our results suggest that small males invest more on each mating opportunity, potentially as a response of overall fewer mating opportunities due to their reduced size, or due to the larval cues of high population density. This work provides an insight into early life effects on ejaculate allocation in D. melanogaster and sheds light on the physiological and behavioural responses to developmental conditions in insects.

evolutionary biology↗

Simulations provide a mechanistic interpretation of Bateman gradients

The Bateman gradient (BG or ) is a fundamental metric of sexual selection, and is often interpreted as the fitness advantage individuals can gain by increasing their number of mates. However, researchers commonly misconceive the relationship between mating success (MS) and reproductive success (RS) as always being causal, leading to a misinterpretation of the BG. The BG is phenomenological and therefore uninformative about the mechanisms leading to correlations between MS and RS. Here, we simulate sequential matings in males from biological systems with varying levels of anisogamy and sperm competition, to better understand the underlying processes that modulate male BGs. We show that the BG does not solely reflect the causal influence of MS on RS as is typically interpreted, but is also a consequence of covariances between male MS and male ejaculate traits, female fecundity, or female post-mating decisions. For example, we show that the BG is substantially shallower when the ejaculate size of males negatively co-varies with their MS, such as in species with alternative male reproductive tactics. Such covariances can lead to a misinterpretation of the measured BG, because here, it does not merely represent the strength of selection on intra-sexual competition for mates. We suggest how such covariances can be visually assessed, and accounted for using partial Bateman gradients, to better interpret the influence of MS on RS, thus the strength of pre-copulatory sexual selection. Among other simplifications, our simulations have a male-only focus, but they provide insights into the mechanisms driving inter- and intra-specific variation in the BG, clarify its meaning, and improve our understand of sexual selection.

evolutionary biology↗

No evidence for paternal age effects on sons or daughters, when accounting for paternal sperm storage

O_LIThe age at which a father reproduces is predicted to affect not only his own fertility but also the fitness of his offspring. Specifically, offspring born to old fathers are assumed to be of a lower quality than those conceived by young fathers. However, when fathers have low mating rates, paternal age might be confounded with the duration for which mature sperm are stored in fathers prior to ejaculation. C_LIO_LIStudies that disentangle the confounding effects of paternal sperm storage duration from those of paternal age, on offspring, are lacking. We use Drosophila melanogaster to test the separate and interactive effects of paternal age and sperm storage duration (sexual rest) on the survival and lifetime reproduction of offspring. C_LIO_LIAs expected, old fathers produce fewer offspring than young fathers. But surprisingly, paternal age does not influence the survival or lifetime reproductive success of either sons or daughters. Instead, sons conceived by fathers with long durations of sexual rest have lower reproductive success than sons conceived by fathers with short durations of sexual rest. C_LIO_LIWe further discover that daughters of low reproductive quality selectively disappear with age, but sons do not, highlighting that demographic processes need to be accounted for when studying paternal age effects. C_LIO_LIOverall, our study suggests that paternal age effects might not be as pervasive as previously assumed. We emphasize that a more nuanced understanding of the mechanisms causing paternal age effects is required, so that studies do not misattribute effects of paternal sperm storage to age. C_LI

evolutionary biology↗

Genetic, natal, and spatial drivers of social phenotypes in wild great tits

In social animals, group dynamics profoundly influence collective behaviours, vital in processes like information sharing and predator vigilance. Disentangling the causes of individual-level variation in social behaviours is crucial for understanding the evolution of sociality. This requires unravelling the genetic and environmental basis of these behaviours, which is challenging in uncontrolled wild populations. In this study, we partitioned genetic, developmental and spatial environmental variation in repeatable social network traits derived from foraging events using a multigenerational pedigree and extensive observational social data from a long-term monitored great tit population. Animal models indicated minimal narrow-sense heritability (2-3%) in group size choice, further reduced when spatial location was considered, which itself explains a substantial 30% of the observed variation. Individual gregariousness also had a small genetic component, with a low heritability estimate for degree (<5%). Centrality showed heritability up to 10% in one of three years sampled, whereas betweenness showed none, indicating modest genetic variation in individual sociability, but not group-switching tendencies. These findings suggest a small, albeit detectable, genetic influence on individual sociality, but pronounced spatial effects. Furthermore, our study highlights the importance of common environment effects (natal origin and brood identity), which essentially negated genetic effects when explicitly accounted for. In addition, we demonstrate that phenotypic resemblance can be a result of similarities beyond shared genes; spatial proximity at birth and natal environmental similarity explained up to 8% of individual sociability. Our results thus emphasise the role of non-genetic factors, particularly developmental and spatial variation, in shaping individual social behavioural tendencies.

ecology↗

Reproductive output of old polygynous males is limited by seminal fluid, not sperm number

Advancing male age can lead to reproductive senescence, which in males is thought to be largely driven by declines in the numbers of sperm transferred by old males. This decline is predicted to be particularly pronounced in polygynous species, where males become sperm limited over a mating sequence. However, males also transfer seminal fluid to females, and little is known about the contribution of seminal fluid to constrain the reproductive output of old, multiply-mating males. Using Drosophila melanogaster, we investigated whether age-related variation in male reproductive output is driven by differential limitation of sperm or seminal fluid, over a series of experimental matings. Consistent with reproductive senescence, old males produced fewer offspring than young males. However, this pattern was not driven by sperm limitation, with old males having more sperm and transferring similar numbers of sperm to a female, compared to young males. Yet surprisingly, females stored fewer sperm when mated to old than young males. Notably, females mated to old multiply-mating males produced more offspring when supplemented with seminal fluid, suggesting that fertility of old males over successive matings was limited by seminal fluid availability. Generally, our study indicates that germline maintenance might be prioritised over somatic maintenance as hypothesized by the disposable soma theory of ageing, and that seminal fluid senescence is a key contributor of reproductive decline with age. While other factors such as differential sperm viability and female post-mating responses could have also influenced our results, our study highlights the under-appreciated role of seminal fluid in mediating male reproductive senescence in polygynous species. Significance statementA key assumption in ageing research is that old males are less fertile than young males, and that this reduced fertility is partly driven by old males producing fewer sperm. However, senescence in male fertility can be caused via other ejaculate-mediated pathways, which we investigate using fruit flies. Contrary to expectations, we reveal that senescence in male fertility is not because of declines in male sperm reserves, but is instead due to age-related changes in seminal fluid and differences in female sperm storage with male age. These declines in the reproductive output of old, multiply-mating males are alleviated by supplementing females with "extra" seminal fluid. Our study demonstrates that male reproductive senescence is reversible, highlighting the underappreciated role of seminal fluid in modulating senescence in polygynous species. These results have potential for improving animal fertility and our understanding of sexual selection.

evolutionary biology↗

What doesn't kill you makes you stronger? Effects of paternal age at conception on fathers and sons

Advancing male age is often hypothesised to reduce both male fertility and offspring quality through reproductive senescence. However, the effects of advancing male age on reproductive output and offspring quality need not always be deleterious. For example, older fathers might compensate for reproductive senescence by terminally investing in reproduction. Similarly, males that survive to reproduce at an old age, might carry alleles that confer high viability (viability selection) which are then inherited by offspring, or might have high reproductive potential (selective disappearance). Differentiating these mechanisms requires an integrated experimental study of paternal survival and reproductive performance, as well as offspring quality, which is currently lacking. Using Drosophila melanogaster, we test the effects of paternal age at conception (PAC) on paternal survival and reproductive success, and the lifespans of sons. We discover that mating at an old age is temporarily linked with decreased future male survival, suggesting that mating-induced mortality is possibly due to old fathers being frail. We also find a quadratic reproductive ageing pattern, with an onset of senescence in late-life. We discover no evidence for terminal investment, and instead discover positive covariances between a fathers lifespan and his probability of siring offspring, for older PAC groups. Lastly, we show that sons born to older fathers live longer than those born to younger fathers, due to viability selection. Collectively, our results suggest that effects of advancing PAC need not be deleterious for fathers or offspring, and can increase fitness if older fathers produce more viable offspring. Lay summaryIts often assumed that old fathers have fewer or lower-quality offspring than young fathers. However, old fathers have on average, usually survived to and reproduced at an older age than young fathers, which might be signals of high quality of old fathers, and benefit offspring. These opposing predictions have rarely been tested, and its unclear what their combined influence is, in determining the fathers and offsprings fitness. Using fruit flies, we explored how old paternal age affects a fathers reproduction and his sons lifespans. We find evidence for age-related reproductive decline in fathers. However, we also discover that fathers who mate at an older age live longer than fathers who mate at a younger age, and subsequently, the sons of older fathers live longer than sons of younger fathers. We suggest that the relationship between paternal age, paternal reproduction and lifespan, and offspring quality, is more complex than previously assumed, and that old fathers might provide benefits to their offspring that future studies need to consider. Teaser textIs an old dad really that bad? While old fathers might in some cases produce fewer offspring or offspring of worse quality than young fathers, they have also survived to an older age, thus might be of higher quality. We test how reproducing at an old age affects a father and his sons fitness. We show that old fathers show evidence of reproductive senescence, but, surprisingly, produce sons that are longer lived than the sons of young fathers. This effect is driven largely by old fathers themselves living longer than young fathers, thus possibly passing alleles conferring higher viability to their sons. Our research is important because it reveals specific mechanisms that drive multifaceted effects of age on fitness.

evolutionary biology↗

Structured demographic buffering: A framework to explore the environment drivers and demographic mechanisms underlying demographic buffering

Environmental stochasticity is a key determinant of population viability. Decades of work exploring how environmental stochasticity influences population dynamics have highlighted the ability of some natural populations to limit the negative effects of environmental stochasticity, one of these strategies being demographic buffering. Whilst various methods exist to quantify demographic buffering, we still do not know which environment factors and demographic characteristics are most responsible for the demographic buffering observed in natural populations. Here, we introduce a framework to quantify the relative effects of three key drivers of demographic buffering: environment components (e.g., temporal autocorrelation and variance), population structure, and demographic rates (e.g., progression and fertility). Using Integral Projection Models, we explore how these drivers impact the demographic buffering abilities of three plant species with different life histories and demonstrate how our approach successfully characterises a populations capacity to demographically buffer against environmental stochasticity in a changing world.

ecology↗

No general effects of advancing male age on ejaculates: a meta-analysis across the animal kingdom

Senescence, the deterioration of organismal function with advancing age, is a puzzling biological phenomenon. While actuarial senescence (i.e., age-dependent increases in mortality rates) is well described across some taxa, reproductive senescence (i.e. age- dependent declines in reproduction) is less understood, especially in males, with mixed patterns reported across studies. To examine the evidence for male reproductive senescence, we investigated how advancing male age affects ejaculate traits across non-human animals via a meta-analysis yielding 1814 effect sizes from 379 studies. We found no evidence for a general pattern of reproductive senescence. Instead, we found high heterogeneity for how reproduction changes with male age across animals. Some of this heterogeneity (>10%) was associated with biological factors. For example, there were taxonomical differences for some ejaculate traits -- sperm motility declined with male age in lab rodents and fish, whereas ejaculate size improved with male age in bulls, fish, and insects. Some methodological factors were also important in explaining this heterogeneity: studies sampling a larger proportion of a species lifespan were more likely to detect senescence in ejaculate traits, emphasising the need to examine the full life cycle of species to document senescence. Contrary to predictions, we reveal that the evidence for senescence in ejaculate traits is sporadic. Our findings will help generate novel hypotheses and identify more effective methodological approaches for studying male reproductive senescence.

evolutionary biology↗

Experimental evolution under varying sex ratio and nutrient availability modulates male mating success in Drosophila melanogaster

Biased population sex ratios can alter optimal male mating strategies, and allocation to reproductive traits depends on nutrient availability. However, there is little information on how nutrition interacts with sex ratio to influence the evolution of pre-copulatory and post-copulatory traits separately. To address this omission, here we test how male mating success and reproductive investment evolve under varying sex ratios and adult diet in Drosophila melanogaster using an experimental evolution approach. We found that sex ratio and nutrient availability interacted to determine male pre-copulatory performance. Males from female-biased populations were slow to mate when they evolved on a protein-restricted diet. On the other hand, we found direct and non-interacting effects of sex ratio and nutrient availability on post-copulatory success, without interactions between them. Males that evolved on a protein-restricted diet were poor at suppressing female remating. Males that evolved under equal sex ratios fathered more offspring and were better at supressing female remating, relative to males from male-biased or female-biased populations. These results support the idea that sex ratios and nutrition interact to determine the evolution of pre-copulatory mating traits, but independently influence the evolution of post-copulatory traits.

evolutionary biology↗

Influences of male age, mating history and starvation on female post mating aggression and feeding in Drosophila

O_LIMating changes female behaviour and physiology across a wide range of taxa, with important effects for male and female fitness. These changes are often induced by components of the male ejaculate, such as sperm and seminal fluid proteins. C_LIO_LIHowever, males can vary significantly in their ejaculates, due to factors such as age, mating history, or nutritional status. This male variation may therefore lead to variation in the strength of responses males can stimulate in females, with alterations in fitness outcomes for both sexes. C_LIO_LIUsing the fruit fly, Drosophila melanogaster, we tested whether three aspects of male condition shape an important, but understudied, post-mating response - increased female-female aggression. C_LIO_LIWe found that females mated to old males fought less than females mated to young males. This effect was exacerbated in mates of old, sexually active males, but there was no effect of male starvation status on mating-induced female aggression. There was also a significant effect of age and mating history on female post-mating feeding duration. C_LIO_LIOur results add to a growing body of literature that variation in male condition can shape sexual selection through post-mating responses in females, including female-female interactions. Studying such variation may therefore be useful for understanding how the condition of sex affects the behaviour of the other. C_LI

animal behavior and cognition↗

Structural variation in Drosophila melanogaster spermathecal ducts and its association with sperm competition dynamics

The ability of female insects to retain and use sperm for days, months, or even years after mating requires specialised storage organs in the reproductive tract. In most orders these organs include a pair of sclerotised capsules known as spermathecae. Here, we report that some Drosophila melanogaster females exhibit previously uncharacterised structures within the distal portion of the muscular duct that links a spermatheca to the uterus. We find that these spermathecal duct presences (SDPs) may form in either or both ducts and can extend from the duct into the sperm-storing capsule itself. We further find that the incidence of SDPs varies significantly between genotypes, but does not change significantly with the age or mating status of females, the latter indicating that SDPs are not composed of or stimulated by sperm or male seminal proteins. We show that SDPs affect neither the number of first male sperm held in a spermatheca nor the number of offspring produced after a single mating. However, we find evidence that SDPs are associated with a lack of second male sperm in the spermathecae after females remate. This raises the possibility that SDPs provide a mechanism for variation in sperm competition outcome among females.

evolutionary biology↗

BMP-signalling inhibition in Drosophila secondary cells remodels the seminal proteome, and self and rival ejaculate functions

Seminal fluid proteins (SFPs) exert potent effects on male and female fitness. Rapidly evolving and molecularly diverse, they derive from multiple male secretory cells and tissues. In Drosophila melanogaster, most SFPs are produced in the accessory glands, which are composed of [~]1000 fertility-enhancing main cells and [~]40, more functionally cryptic, secondary cells. Inhibition of BMP-signalling in secondary cells suppresses secretion, leading to a unique uncoupling of normal female post-mating responses to the ejaculate: refractoriness stimulation is impaired, but offspring production is not. Secondary cell secretions might therefore make a highly specific contribution to the seminal proteome and ejaculate function; alternatively, they might regulate more global - but hitherto-undiscovered - SFP functions and proteome composition. Here, we present data that supports the latter model. We show that in addition to previously reported phenotypes, secondary cell-specific BMP-signalling inhibition compromises sperm storage and increases female sperm use efficiency. It also impacts second male sperm, tending to slow entry into storage and delay ejection. First male paternity is enhanced, which suggests a novel constraint on ejaculate evolution whereby high female refractoriness and sperm competitiveness are mutually exclusive. Using quantitative proteomics, we reveal a mix of specific and widespread changes to the seminal proteome that surprisingly encompass alterations to main cell-derived proteins, indicating important cross-talk between classes of SFP-secreting cells. Our results demonstrate that ejaculate composition and function emerge from the integrated action of multiple secretory cell-types suggesting that modification to the cellular make-up of seminal fluid-producing tissues is an important factor in ejaculate evolution.

evolutionary biology↗

An exposition of ejaculate senescence and its inhibition in Drosophila

Declining ejaculate performance with male age is taxonomically widespread and has broad ramifications for fertility and fitness. However, we have a poor understanding of age-related changes to specific ejaculate components, how they cause reduced performance, and whether the decline is ameliorable. Here, we show that, in Drosophila, sperm production chronologically declines with age, invariant to mating activity, while repeated mating causes infertility via reduced sperm stores and viability. However, changes to sperm do not fully explain ejaculate deterioration: impacts on seminal fluid contribute to aspects of reduced ejaculate performance, associated with shifts in proteome abundance and quality. We show that ablation of insulin-like peptide-producing cells in males ameliorates aspects of ejaculate performance loss, suggesting that anti-ageing interventions can be coopted to benefit male reproductive health.\n\nOne Sentence SummaryEjaculate performance declines with male age via mating-dependent sperm and seminal protein deterioration, but it can be ameliorated.

evolutionary biology↗