Biology subjects

Bretman, A.

Publications and source records attributed to Bretman, A..

8 recordsLinked to original sources

bioRxiv2024

Female fruit flies use social cues to make egg clustering decisions

BackgroundThe 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, 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 over-exploitation 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. ResultsOur 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. ConclusionsCollectively, the results reveal that females actively 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 public goods-related benefits.

animal behavior and cognition↗

bioRxiv2024

Female oviposition decisions are influenced by the microbial environment

In ovipositing animals, egg placement decisions can be key determinants of offspring survival. One oviposition strategy reported across taxa is egg clustering, whereby a female lays multiple eggs next to one another or next to the eggs of other females. The fitness benefits of egg clustering, especially in mixed maternity clusters, are unknown. 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 D. melanogaster females; (ii) D. melanogaster eggs exhibit antimicrobial activity. The results partially supported the first hypothesis. Females exposed to environmental microbes that naturally colonised the oviposition substrates in the absence of antimicrobial preservatives reduced their levels of fecundity but did not significantly alter egg clustering. In contrast, the presence of commensal (fly-associated) microbes did not affect oviposition. The second hypothesis was not supported. There was no evidence of antimicrobial activity, either in whole eggs or in soluble surface material extracted from them. In conclusion, while there was no evidence that oviposition decisions are shaped by the opportunity to share antimicrobials, there is evidence that the microbial environment provides cues that females use to make sophisticated decisions on fecundity and egg placement.

evolutionary biology↗

bioRxiv2022

Held out wings RNA binding activity in the cytoplasm during early spermatogenesis

Held out wings (HOW) is an RNA-binding protein essential for spermatogenesis in Drosophila melanogaster. HOW is a signal transduction and activation of RNA (STAR) protein, regulating post-transcriptional gene expression. The characteristics of RNA-binding by the conserved short cytoplasmic isoform, HOW(S), are unknown. In vivo RIP-seq identified 121 novel transcripts bound by HOW(S) in germ stem cells and spermatogonia, many with signal transduction functions. (A/G/U)CUAAC motifs were enriched in 3-UTRs and GCG(A/U)G in 5-UTRs. HOW binds with high-affinity to sites containing CUAAC motifs from lola and hipk mRNAs. This study provides new insight into STAR protein-RNA interactions and functions in spermatogenesis.

molecular biology↗

bioRxiv2021

Female fruit flies cannot protect stored sperm from high temperature damage

Recently, it has been demonstrated that heat-induced male sterility is likely to shape population persistence as climate change progresses. However, an under-explored possibility is that females may be able to successfully store and preserve sperm at temperatures that sterilise males, which could ameliorate the impact of male infertility on populations. Here, we test whether females from two fruit fly species can protect stored sperm from a high temperature stress. We find that sperm carried by female Drosophila virilis are almost completely sterilised by high temperatures, whereas sperm carried by female Zaprionus indianus show only slightly reduced fertility. Heat-shocked D. virilis females can recover fertility when allowed to remate, suggesting that the delivered heat-shock is destroying stored sperm and not directly damaging females in this species. The temperatures required to reduce fertility of mated females are substantially lower than the temperatures required to destroy mature sperm in males, suggesting that females are worse than males at protecting mature sperm. This suggests that female sperm storage is unlikely to ameliorate the impacts of high temperature fertility losses in males, and instead exacerbates fertility costs of high temperatures, representing an important determinant of population persistence during climate change.

physiology↗

bioRxiv2021

Female fruitflies use gustatory cues to exhibit reproductive plasticity in response to the social environment

Animals can exhibit remarkable reproductive plasticity in response to their social surroundings, with profound fitness consequences. The study of such plasticity in females, particularly in same-sex interactions, has been severely neglected. Here we measured the impact of variation in the pre-mating social environment on reproductive success in females and tested the underlying mechanisms involved. We used the Drosophila melanogaster model system to test the effect of varying female group size prior to mating and deployed physical and genetic methods to manipulate the perception of different social cues and sensory pathways. We found that socially isolated females were significantly more likely to retain unfertilised eggs before mating, but to show the opposite pattern and lay significantly more fertilised eggs in the 24h after mating, in comparison to grouped females. More than 48h of exposure to other females was necessary for this socially-induced plasticity to be expressed. Neither olfactory nor visual cues were involved in mediating these responses. Instead, we found that females detected other females through direct contact with the deposits they leave behind, even in the absence of eggs. The results demonstrate that females show striking reproductive plasticity in response to their social surroundings and that the nature of their plastic reproductive responses, and the cues they use, differ markedly from those of males. The results emphasise the stark contrasts in how each sex realises reproductive success.

evolutionary biology↗

bioRxiv2021

Reproductive plasticity in both sexes interacts to determine mating behaviour and fecundity

Organisms alter their phenotype in response to variation in their environment by expressing phenotypic plasticity. Both sexes exhibit such plasticity in response to contrasting environmental and social cues, and this can reflect the influence of sexual conflict. However, theory predicts that plasticity expressed by both sexes may either maximise the sex-specific fitness of both, or of one sex at the expense of the other. Hence empirical tests of the predictions are sorely needed. Here we conducted novel tests of the fitness effects of interacting reproductive plasticity in Drosophila melanogaster. First, prior to mating, males were kept alone, or with same sex rivals, and females were kept alone, in same sex, or mixed sex groups. Second, we conducted matings between individuals from all these social treatments under choice and no choice scenarios. The results showed that males and females can both plastically respond to these socio-sexual environments to influence the expression of mating duration, mating latency, and fecundity. These plastic responses interacted significantly to determine mating latency and fecundity. Effects on mating latency were also observed under both choice and no-choice conditions, but in opposing directions. Variation in the outcome of interacting plasticity pivoted around the outcomes observed with focal females that had been maintained in same-sex environments prior to mating. However, not all fitness-related traits examined responded in the same way. Mating duration was determined largely by the social environment of the male. Our results show that the expression of some, but not all fitness-related reproductive traits can be determined by the outcome of interacting behavioural plasticity expressed by both sexes. This highlights the need for new predictive theory informed by these empirically-derived parameters. Overall, we conclude that variation in the expression of shared traits due to interacting plasticity represents an important and novel facet of sexual interactions. Impact SummaryAnimals and plants are able to respond to variation in their environment by expressing phenotypic plasticity. In sexual organisms, both males and females can exhibit such plasticity but the cues they respond to and the fitness consequences of these actions may be different between the sexes, and even conflicting. For example, males may respond to the presence of competitors by altering their mating behaviour or ejaculate transfer to increase their own, but not necessarily their mates reproductive output. However, females may also express phenotypic plasticity in response to their social and sexual environment to maximise their own fitness. Theory suggests that plasticity expressed by both sexes may either maximise the sex-specific fitness of both, or of one sex at the expense of the other. So far, little experimental work has been conducted to explore such interacting plasticity. Here we conducted novel tests of the fitness effects of interacting plasticity in the fruit fly Drosophila melanogaster. In doing so, we provide novel experimental evidence for interacting behavioural plasticity. We show that males and females can plastically respond to their socio-sexual environment to influence the expression of mating duration, mating latency, and fecundity. These plastic responses, while induced to increase the fitness interests of each sex, interact in the case of mating latency and fecundity and may reflect the outcome of sexual conflict. Our findings suggest that studies of reproductive behaviour should carefully consider the socio-sexual environment of both males and females and highlight the need for new predictive theory informed by empirically-derived parameters. Overall, we show that interacting plasticity between sexes represents an important and novel facet of sexual interactions.

evolutionary biology↗

bioRxiv2020

Temperatures that sterilise males better predict global distributions of species than lethal temperatures

Predicting how biodiversity will respond to increased temperatures caused by climate change is vital. However, our understanding of the traits that determine species response to thermal stress remains incomplete. Laboratory measurements of lethal temperatures have successfully been used to predict global species distributions and the vulnerability of species to future climate change. However, although it has long been known that fertility is sensitive to heat stress, temperatures that cause sterility have not been incorporated into predictions about how climate change will affect biodiversity. Here we show that male sterility temperatures predict the global distributions of 43 species of Drosophila substantially better than their lethal temperatures. This strongly suggests that thermal limits to reproduction can underpin how temperature affects species distributions. High temperatures impair male fertility across a broad range of animals and plants, so many organisms may be more vulnerable to high temperatures than currently expected.

ecology↗

bioRxiv2020

Social environment drives sex and age-specific variation in Drosophila melanogaster microbiome composition and predicted function.

Social environments influence multiple traits of individuals including immunity, stress and ageing, often in sex-specific ways. The composition of the microbiome (the assemblage of symbiotic microorganisms within a host) is determined by environmental factors and the hosts immune, endocrine and neural systems. The social environment could alter host microbiomes extrinsically by affecting transmission between individuals, likely promoting homogeneity in the microbiome of social partners. Alternatively, intrinsic effects arising from interactions between the microbiome and host physiology (the microbiota-gut-brain axis) could translate social stress into dysbiotic microbiomes, with consequences for host health. We investigated how manipulating social environments during larval and adult life-stages altered the microbiome composition of Drosophila melanogaster fruit flies. We used social contexts that particularly alter the development and lifespan of males, predicting that any intrinsic social effects on the microbiome would therefore be sex-specific. The presence of adult males during the larval stage significantly altered the microbiome of pupae of both sexes. In adults, same-sex grouping increased bacterial diversity in both sexes. Importantly, the microbiome community structure of males was more sensitive to social contact at older ages, an effect partially mitigated by housing focal males with young rather than co-aged groups. Functional analyses suggest that these microbiome changes impact ageing and immune responses. This is consistent with the hypothesis that the substantial effects of the social environment on individual health are mediated through intrinsic effects on the microbiome, and provides a model for understanding the mechanistic basis of the microbiota-gut-brain axis. Significance statementThe social environment has pervasive, multifaceted effects on individual health and fitness. If a hosts microbiome is sensitive to the social environment then it could be an important mediator of social effects, as the reciprocal relationships between hosts and their microbiomes have substantial implications for host health. Using a Drosophila melanogaster fruit fly model we show that the fly microbiome is sensitive to the social environment in a sex, age and life-stage dependent manner. In particular, older adult male microbiome communities are altered by same-sex social contact, but this depends on the age of the social partners. These changes have functional effects on fly immunity and lifespan, evidence that indeed this is an influential mediator of social effects on health.

ecology↗