Tracey Chapman

Nutritional requirements vary across sexes and lifetimes and are predicted to influence dietary preferences. Here, we tested the hypothesis that diet preferences vary adaptively with sex, age and life stage. We used the fruit fly Drosophila melanogaster to take independent snapshots of choice for three protein : carbohydrate (P : C) diets in both sexes of young (5 d), mid-aged (15 d) or old (25 d) flies, while simultaneously recording oviposition site choice. We then tested, for mothers of each age, the diet preferences, development and survival on each diet of their larval offspring. Diet choice was sex- and age-specific. Males consistently preferred high carbohydrate, and females high protein (and these preferences became stronger with age). By contrast, oviposition choice was for balanced (1 : 1 P : C) and high carbohydrate diets in young and old females, respectively. Larvae of old, but not young, parents also preferred balanced diets. Young-parent larvae developed faster on balanced diets, with survival differences (highest with high carbohydrate) evident only in mid-aged-parent larvae. Unexpectedly, mid-aged-parent larvae had slower development and higher preadult mortality than young-parent larvae. Thus, diet choices may not be optimized across parents and offspring, and we identify novel effects of modest increases in parental age and offspring diets on offspring fitness.

Theory suggests sexual selection will enhance population viability by purging deleterious alleles. However, direct genomic evidence for this fundamental idea is scarce and contradictory. We combined long-term experimental evolution with whole-genome resequencing to directly test how sexual selection affects mutation load, genomic divergence, and extinction risk in small populations (maximum N _e = 40) of Tribolium castaneum . After 156 generations, populations evolving under strong sexual selection carried substantially fewer deleterious alleles than populations under weak sexual selection, based on both individual-level estimates of missense and nonsense variants and population-level R _xy analyses, indicating more efficient purging of deleterious alleles. In contrast, nucleotide diversity and runs of homozygosity were similar across treatments, indicating that purging acted most strongly on deleterious variation, and that reduced mutation load in these small populations under strong sexual selection was not explained by demographic effects. Importantly, population-level mutation load estimates best explained extinction risk under inbreeding, directly linking sexual selection to purging and population viability. Genome scans of high and low sexual selection populations revealed peaks of divergence, which included genes involved in courtship, sex discrimination, and seminal fluid proteins. Our results provide direct genomic evidence that sexual selection can reduce mutation load without eroding standing genetic diversity and thus adaptive potential, while driving adaptive divergence in reproductive traits. This beneficial purging may help explain the widespread prevalence of sexual reproduction in nature despite inherent costs and have important ramifications as to how we manage populations of conservation concern.

Natural selection might favour brightly coloured males and drab females. A male and a female might disagree about whether to mate. Such tensions are often described as ‘sexual conflict’ of two forms: intralocus and interlocus. However, this framing unites two very different evolutionary processes: genetic constraint and social conflict, in which male and female fitness are linked by shared genetics or by shared social interactions, respectively. We suggest that coupling both under the banner of ‘sexual conflict’ is not justified and impedes progress. This problem has become acute as researchers explore the mechanistic underpinnings of both phenomena and as conflation emerges in other research. We propose that a conceptual uncoupling of ‘sexual conflict’ into true sexual conflict and sexual pleiotropy is needed. Here, we (i) clarify the distinction between conflict and pleiotropy, using evolutionary theory; (ii) show how current conceptual coupling has led to faulty predictions, misdirected research efforts and missed opportunities; (iii) detail how interlocus and intralocus terms have added to confusion; and (iv) establish links with other areas of biology. We show the potential scientific advances that can emerge from disentangling conflict and pleiotropy in biodiversity, molecular genetic and ecological research.

Intergenerational and transgenerational fitness effects can shape evolutionary processes. Theoretically, however, intergenerational and transgenerational effects can trade off with each other with profound consequences for evolutionary processes. Here, we show that beneficial intergenerational effects that increase offspring fitness can result in detrimental transgenerational effects that decrease great-grand offspring fitness. We combined theoretical modeling and experimental approaches to investigate multigenerational fitness trade-offs induced by larval starvation in Caenorhabditis elegans. We demonstrate that larval starvation triggers a cascading effect: starved individuals suffered marked fitness losses, their direct offspring enjoyed fitness gains in both starvation and ad libitum environments, but great-grand offspring paid fitness costs. Demographic simulation models revealed that genotypes exploiting this short-term intergenerational advantage outcompete rival genotypes despite the deferred transgenerational debt. Our findings demonstrate that adaptive intergenerational gains can be intrinsically linked to maladaptive transgenerational outcomes, challenging the assumption that transgenerational effects are inherently beneficial and highlighting the role of multigenerational trade-offs in evolution.

We report the identification and functional validation of a 7SK RNA polymerase III promoter in the Mediterranean fruit fly, Ceratitis capitata . CRISPR/Cas9-based genetic control strategies for this global agricultural pest, including gene drives and precision guided sterile insect approaches, require efficient guide RNA expression, yet only a single U6 Pol III promoter had previously been validated for this purpose in C. capitata , and no 7SK promoter had been characterised in any Tephritid species. Using comparative genomics with Drosophila orthologues, we identified a previously unannotated 7SK gene in the C. capitata genome, confirmed its transcriptional activity by RT-PCR, and demonstrated that the cloned promoter drives functional guide RNA expression in CRISPR/Cas9-mediated knockouts of the white gene. Comparative analysis identified putative 7SK orthologues across the Tephritid fruit flies. The availability of this additional new Pol III promoter will enable multiplexed guide RNA strategies using distinct promoters, supporting more robust genetic control designs. Graphical

Females and males typically differ in lifespan, patterns of ageing, and reproduction. General explanations for variation in the magnitude of this sex-specificity remain elusive, and the role of the social environment in this context is under-explored. Sexual selection theory predicts that males should adopt a “live fast, die young” strategy, as their fitness is likely to be contingent on intense investment to achieve success in competing for potentially few matings. However, there is a growing realization that sexual selection can act on a much broader suite of “general performance” traits than only those directly related to mating competition. This, combined with frequently observed high costs of reproduction in females, makes an alternative prediction—that ageing and reproductive senescence can be high for females, and could potentially exceed what is seen in males. We tested these contrasting predictions in the fruit fly Drosophila melanogaster, using assays in which both sexes competed for reproductive opportunities over their lifetimes within varying socio-sexual environments. Females consistently exhibited “live fast, die young” life histories, whereas males had significantly longer lifespans and showed only limited declines in age-specific fitness and mating performance. We also identified new same-sex exposure effects—females housed with females exhibited faster reproductive ageing at a marginal lifespan cost, whereas corresponding males maintained higher courtship and activity with age, with no detectable effect on lifespan. The results highlight the crucial importance of social environments to the study of ageing and fitness. The possibility that rapid reproductive senescence is widespread in females is key to broadening our holistic understanding of the biology of sex differences in ageing and reproduction.

Background: The ability to respond plastically to environmental variation is a key determinant of fitness. Females may use cues to strategically place their eggs, for example adjusting the number or location of eggs according to whether other females are present and driving the dynamics of local competition or cooperation. The expression of plasticity in egg-laying patterns within individual patches (i.e. in contact clusters or not) represents an additional, under-researched, and potentially important opportunity for fitness gains. Clustered eggs might benefit from increased protection or defence, and clustering could facilitate cooperative feeding. However, increased clustering is also expected to increase the risk of overexploitation through direct competition. These potential benefits and costs likely covary with the number of individuals present; hence, egg-clustering behaviour within resource patches should be socially responsive. We investigate this new topic using the fruit fly Drosophila melanogaster. Results: Our mathematical model, parameterised by data, verified that females cluster their eggs non-randomly and increase clustering as group size increases. We also showed that as the density of adult females increased, females laid more eggs, laid them faster, and laid more eggs in clusters. Females also preferred to place eggs within existing clusters. Most egg clusters were of mixed maternity. Conclusions: Collectively, the results reveal that females express plasticity in egg clustering according to social environment cues and prefer to lay in clusters of mixed maternity, despite the potential for increased competition. These findings are consistent with egg-clustering plasticity being selected due to cooperative benefits.

Heatwaves are becoming more common and severe. Previous work has highlighted male insects as being particularly vulnerable to multi-day continuous heatwaves, yet our understanding of short duration heatwave impacts on insects is limited. Here, we assess the impacts of short, simulated heatwave exposures (2, 5 and 10 hours [h]) using ecologically relevant temperatures (42°C, 44°C, 46°C, 48°C and 50°C) on survival, reproductive output, testes volume and sperm length in Tribolium castaneum. We show that reproductive output is compromised at lower temperatures than survival, especially during the shortest heatwaves, supporting the notion that thermal fertility limits are lower than thermal viability limits. Furthermore, testes volumes were reduced by 40% after a 10 h exposure at 42°C and sperm length decreased by 2.7% after an exposure of 42°C for just 2 h. This highlights that even short heat exposure can impact male fertility and reproductive trait morphology at temperatures below viability limits.

In ovipositing animals, egg placement decisions can be key determinants of offspring survival. One oviposition strategy reported across taxa is laying eggs in clusters. In some species, mothers provision eggs with diffusible defence compounds, such as antimicrobials, raising the possibility of public good benefits arising from egg clustering. Here we report that Drosophila melanogaster females frequently lay eggs in mixed-maternity clusters. We tested two hypotheses for potential drivers of this oviposition behaviour: (i) the microbial environment affects fecundity and egg placement in groups of females; (ii) eggs exhibit antimicrobial activity. The results partially supported the first hypothesis. Females reduced egg laying but did not alter egg clustering, on non-sterile substrates that had been naturally colonized with microbes from the environment. However, oviposition remained unaffected when the substrate community consisted of commensal (fly-associated) microbes. The second hypothesis was not supported. There was no evidence of antimicrobial activity, either in whole eggs or in soluble egg-surface material. In conclusion, while we found no behavioural or physiological evidence that egg clustering decisions are shaped by the opportunity to share antimicrobials, females are sensitive to their microbial environment and can adjust egg-laying rates accordingly.

It is increasingly clear that social environments have profound impacts on the life histories of ‘non-social’ animals. However, it is not yet well known how species with varying degrees of sociality respond to different social contexts and whether such effects are sex-specific. To survey the extent to which social environments specifically affect lifespan and ageing in non-social species, we performed a systematic literature review, focusing on invertebrates but excluding eusocial insects. We found 80 studies in which lifespan or ageing parameters were measured in relation to changes in same-sex or opposite-sex exposure, group size or cues thereof. Most of the studies focused on manipulations of adults, often reporting sex differences in lifespan following exposure to the opposite sex. Some studies highlighted the impacts of developmental environments or social partner age on lifespan. Several studies explored potential underlying mechanisms, emphasizing that studies on insects could provide excellent opportunities to interrogate the basis of social effects on ageing. We discuss what these studies can tell us about the social environment as a stressor, or trade-offs in resources prompted by different social contexts. We suggest fruitful avenues for further research of social effects across a wider and more diverse range of taxa. This article is part of the discussion meeting issue ‘Understanding age and society using natural populations’.