Biology subjects

Kilner, R. M.

Publications and source records attributed to Kilner, R. M..

17 recordsLinked to original sources

bioRxiv2026

Parental care is a genetic capacitor

Parental care is widespread across the animal kingdom and plays a critical role in offspring development. Yet, its broader genetic and evolutionary impacts remain underexplored. Here, using the biparental burying beetle Nicrophorus vespilloides as a model, we show that parental care acts as a genetic capacitor: it allows genetic variation to accumulate while care is present and releases it when care is disrupted. By experimentally manipulating care, we demonstrate that parental care suppresses genetic variation associated with offspring body size, which is released when care is lost. To investigate the underlying molecular mechanisms, we generate a chromosome-scale genome assembly for N. vespilloides, alongside a single-nucleus gene expression atlas and epigenomic datasets from larvae reared with and without parental care. We find that the loss of parental care induces molecular stress, disrupting the expression of the protein chaperone Hsp83, which is a well-known molecular capacitor, alongside other putative mRNA chaperones. Moreover, our results suggest that parental care buffers development by maintaining an open, responsive chromatin landscape and redundant gene regulatory interactions. Overall, our work reveals that parental care shapes the storage, expression and release of genetic variation with broad implications for adaptation and evolution.

animal behavior and cognition↗

bioRxiv2025

The form and function of a multi-functional weapon system in male and female burying beetles (Nicrophorus vespilloides)

Animal weapon systems are used for attack and defence during competition for resources including, though not confined to, competition for mates. They comprise the weapon itself and associated morphological structures - or weapon-supportive traits - that are essential for the deployment of the weapon in combat. We investigate the form and function of a weapon system in burying beetles Nicrophorus vespilloides, to better understand why it differs between the sexes. Both males and females engage in contests with members of their own sex to monopolise a scarce carrion breeding resource. We show that mandibles (weapon during biting) and head width (weapon-supportive trait) are larger in males, and that males exhibit a disproportionately larger increase in bite force with head width than females. However, in staged contests with size-matched rivals of the same sex, the weapon system functioned in the same way for males and females: for each sex, the combined effects of head width and maximum bite force best predicted contest outcome. We suggest that the component parts of the weapon system each serve multiple additional functions, including tasks associated with parental care, which contribute differently to fitness in each sex. The resulting divergent selection pressures may explain why sexual dimorphism persists.

evolutionary biology↗

bioRxiv2024

Plasticity and evolution of metabolic division of labour within families

Fluids produced by parents for dependent young, such as milk or regurgitate, carry molecules that assist offspring with growth, immunity and digestion, allowing the metabolic burden of development to be shared between parents and offspring. We tested whether this division of metabolic labour changes plastically and evolves when offspring are experimentally deprived of their parents metabolic assistance. In the burying beetle Nicrophorus vespilloides parents deposit oral fluids on their carrion nest during pre-hatching care, and facultatively transfer fluids to larvae through oral trophallaxis as post-hatching care. We analysed the oral fluid proteomes of replicate experimental populations that had been evolving for 50 generations with or without post-hatching care, and which were then allowed to raise larvae with or without post-hatching care for one experimental generation. We found that parents and larvae plastically and evolutionarily adjusted the proteins in their oral fluids when we prevented post-hatching care. When reared in the absence of post-hatching care, larvae that evolved without post-hatching care were also more capable of consuming carrion proteins than larvae that had evolved with post-hatching care, and had higher survival. Our results suggest that metabolic division of labour within families is plastically modulated, and that the extent of socially modulated plasticity can evolve rapidly when social conditions change.

evolutionary biology↗

bioRxiv2024

Nest construction and its effect on post-hatching family life in the burying beetle Nicrophorus vespilloides

Through the effort required to construct them, the microenvironmental conditions they impose on the family and their indirect influence on post-hatching care, nests play a key role in influencing family life. We combined experimental evolution with cross-fostering experiments on laboratory populations of Nicrophorus vespilloides to investigate three ways in which the nest can contribute more broadly to parental investment. We used replicate populations of N. vespilloides that had evolved for 42 generations under contrasting regimes of care. Populations were either able to supply post-hatching care ("Full Care") or prevented from supplying any post-hatching care ("No Care"). Research on these populations has previously shown that the No Care populations evolved to build rounder nests, more rapidly, by Generation 14. Here we found: 1) larvae raised by Full Care parents on nests prepared by parents from the No Care population did not attain a higher mass by the end of larval development than larvae in other treatments. However, we did discover that: 2) cross-fostering nests between families consistently reduced larval mass - and to a similar extent whether nests were cross-fostered between or within the populations. We suggest that cross-fostering disrupted the chemical environment on and around the nest since we found no evidence that 3) nests mediate interactions between males and females. The duration of paternal care was consistently shorter than the duration of maternal care, and even shorter for males from the No Care populations than males from the Full Care populations. Nevertheless, the duration of male care did not predict variation in duration of female care. In short, although the nest is the substrate for burying beetle family life, we found little evidence that it had evolved divergently in our experimental populations to influence parental investment.

evolutionary biology↗

bioRxiv2023

Sexual dimorphism in head size in wild burying beetles (Nicrophorus vespilloides)

O_LIMale burying beetles (Nicrophorus vespilloides) carry an additional abdominal segment and produce pheromones but otherwise the species is thought to be sexually monomorphic. Both sexes bear bright orange bands on their black elytra, which probably function as part of a warning display rather than in mate choice. C_LIO_LIAlthough larger individuals are more likely to win contests to secure the small carrion required for reproduction, both sexes compete for this vital breeding resource. In wild populations, the sexes are alike in the mean and distribution in their body size. C_LIO_LIHere we describe a form of sexual size dimorphism in wild populations that has previously been overlooked. We show that males have wider heads than females, for any given body size, and that the scaling relationship with body size is hyperallometric in males, but isometric in females. We also show how absolute head width, and the extent of sexual dimorphism in head width differs among wild populations which are within c.10km of each other. C_LIO_LIWe suggest that head size dimorphism could be adaptive, and could be due to divergent selection arising from task specialisation during biparental care, since the duties of care favoured by males are likely to require a greater bite force. C_LI

evolutionary biology↗

bioRxiv2023

Previous breeding success and carrion substrate together influence subsequent carrion choice by adult Nicrophorus vespilloides

Insects can adjust their behaviour in relation to experience in a wide range of contexts including foraging, mate selection, and choice of oviposition site. Here we investigate whether burying beetles modulate their choice of carrion in relation to the outcome of their past breeding experience. Burying beetles require small vertebrate carrion to reproduce. Beetle parents convert carrion into an edible nursery for their larvae, whom they typically care for throughout larval development. We tested whether a beetles past breeding experience influenced its subsequent choice of carrion, when presented simultaneously with either a dead mouse or a dead chick. We found that both male and female beetles favoured the same carrion as used in their first breeding attempt - but only if they had produced many larvae and only if they had previously bred on a mouse. Beetles that had produced fewer larvae on a dead mouse switched to favouring dead chicks in their second breeding attempt. Those that had bred on a dead chick chose carrion at random subsequently, regardless of their previous breeding success. Our general conclusion is that burying beetles can integrate different sources of information about their past breeding experience with current cues when selecting carrion for reproduction.

evolutionary biology↗

bioRxiv2023

Parental care drives the evolution of molecular genetic variation

Cooperative social behaviours, such as parental care, have long been hypothesized to relax selection leading to the accumulation of genetic variation in populations. Although the idea has been discussed for decades, there has been relatively little experimental work to investigate how social behaviour contributes to genetic variation in populations. Here, we investigate how parental care can shape molecular genetic variation in the subsocial insect Nicrophorus vespilloides. Using whole genome sequencing of populations that had evolved in the presence or absence of parental care for 30 generations, we show that parental care maintains levels of standing genetic variation. In contrast, under a harsh environment without care, strong directional selection caused a reduction in genetic variation. Furthermore, we show that adaptation to the loss of care is associated with genetic divergence between populations at loci related to stress, morphological development and transcriptional regulation. These data reveal how social behaviour is linked to the genetic processes that shape and maintain genetic diversity within populations, and provides rare empirical evidence for an old hypothesis. Lay SummarySocial behaviours, such as parental care, have long been hypothesized to result in the accumulation of genetic variation in populations. Here, we investigate how parental care can shape molecular genetic variation in a species that perform biparental care, Nicrophorus vespilloides. Using genome sequencing of populations that had evolved in the presence or absence of parental care for 30 generations, we show that parental care maintains levels of standing genetic variation. In contrast, under a harsh environment without care, populations lost genetic variation. Furthermore, we show that adaptation to the loss of care is associated with genetic divergence between populations at genes related to stress, morphological development and transcriptional regulation. These data reveal how social behaviour is linked to the genetic processes that shape and maintain genetic diversity within populations.

evolutionary biology↗

bioRxiv2022

The role of recent evolutionary history in resilience to environmental change: social evolution effects versus founder effects

Principles of social evolution have long been used retrospectively to interpret social interactions, but have less commonly been applied predictively to inform conservation and animal husbandry strategies. We investigate whether differences in developmental environment, facilitated by divergent social conditions, can predict resilience to environmental change. Upon exposure to harsh novel environments, populations that previously experienced more benign social environments are predicted either to suffer fitness losses (the "mutation load hypothesis" and "selection filter hypothesis") or maintain fitness (the "beneficial mutation hypothesis"). We tested these contrasting predictions using populations of burying beetles Nicrophorus vespilloides we had evolved experimentally for 45 generations under contrasting social environments by manipulating the supply of post-hatching parental care. We exposed sexually immature adults from each population to varying heat stress and measured the effect on survival and reproduction. The greater the level of parental care previously experienced by a population, the better its survival under heat stress during sexual maturation. Although this is consistent with the "beneficial mutation hypothesis", it is also possible that populations that had evolved without post-hatching care were simply more prone to dying during maturation, regardless of their thermal environment. Overall, we suggest that stochastic genetic variation, probably due to founder effects, had a stronger influence on resilience. We discuss the implications for translocation and captive breeding programmes. Lay summaryCan we use knowledge of a populations evolutionary history to predict how individuals might cope with environmental change? We investigated whether burying beetles that had evolved for 45 generations with or without post-hatching parental care differed in their resilience to extreme temperatures as they developed to sexual maturity. We found limited evidence that experimental evolution under different regimes of parental care contributed to thermal resilience, which instead was better explained by chance historical events.

evolutionary biology↗

bioRxiv2022

Multilevel selection leads to divergent coadaptation of care-giving parents during pre-hatching parental care

The joint actions of animals in partnerships or social groups evolve under both natural selection, from the wider environment, and social selection, imposed by other members of the pair or group. We used experimental evolution to investigate how jointly expressed actions evolve upon exposure to a new environmental challenge. Our work focused on the evolution of carrion nest preparation by pairs of burying beetles Nicrophorus vespilloides, a joint activity undertaken by the pair but typically led by the male. In previous work, we found that carrion nest preparation evolved to be faster in experimental populations without post-hatching care (No Care lines) than with post-hatching care (Full Care lines). Here we investigate how this joint activity evolved. After 15 generations of experimental evolution, we created heterotypic pairs (No Care females with Full Care males, and No Care males with Full Care females) and compared their carrion nest making with homotypic No Care and Full Care pairs. We found that pairs with No Care males prepared the nest more rapidly than pairs with Full Care males, regardless of the females line of origin. This suggests that males led the way by adapting their nest preparation behaviour to the No Care environment first, with females secondarily co-adapting their behaviour to the males behaviour by reducing their nest preparation behaviour. We discuss how social coadaptations within pairs or groups could act as a post-mating barrier to gene flow.

evolutionary biology↗

bioRxiv2022

The evolutionary demise of a social interaction: social partners differ in the rate at which interacting phenotypes are lost

Phenotypic plasticity enables animals to adjust their behaviour flexibly to their social environment - sometimes through the expression of adaptive traits that have not been exhibited for several generations. We investigated how long social adaptations can usefully persist when they are not routinely expressed, by using experimental evolution to document the loss of social traits associated with the supply and demand of parental care. We allowed populations of burying beetles Nicrophorus vespilloides to evolve in two social environments for 48 generations in the lab. In Full Care populations, traits associated with the supply and demand of parental care were expressed at every generation, whereas in No Care populations we prevented expression of these traits experimentally. We then revived trait expression in the No Care populations at generations 24, 43 and 48 by allowing parents to supply post-hatching care, and compared these social traits with those expressed by the Full Care populations. We found that offspring demands for care decayed in the No Care populations more rapidly than a parents capacity to supply care. Furthermore, male care decayed before female care. We suggest that this reflects differences in the strength of selection for the expression of alternative traits in offspring, males and females, which can enhance fitness when post-hatching care is disrupted. Impact SummarySocial interactions between animals are suggested to be increasingly vulnerable to breakdown in our changing world. Our experiments offer a rare insight into what happens next, by assessing in real time the durability of social behaviours that are no longer routinely expressed. Our results also have implications for conservation captive breeding programmes where compensatory husbandry techniques prevent trait expression and so could inadvertently induce rapid, irreversible trait loss. We investigated how long it took populations to lose the ability to express appropriate social behaviour when they had been prevented from doing so for many generations. We did this by evolving replicate populations of burying beetles Nicrophorus vespilloides in the laboratory for 48 generations. The burying beetle is a common insect that is well-known for caring for its larvae, although larvae can survive in the lab without any care at all. In two populations ("Full Care"), we allowed parents and offspring to interact during the supply of post-hatching care, as usual. In two other populations ("No Care"), parents were removed before offspring hatched and so could not interact socially with their young. Over the course of 48 generations of experimental evolution, we periodically revived social interactions between parents and offspring in the No Care populations. We assessed the extent to which larval begging behaviours, and parental care behaviours, had decayed by comparing their expression with those in the Full Care populations. We found that larval begging behaviour eroded rapidly in No Care populations, and more rapidly than the supply of care by parents. Furthermore, paternal care decayed to a greater extent than maternal care (which was largely unchanged relative to its expression in the Full Care populations). We suggest that these differences could be due to differences in the strength of selection on each family member for alternative traits to enhance fitness.

evolutionary biology↗

bioRxiv2021

Evolved changes in DNA methylation in response to the sustained loss of parental care in the burying beetle

Levels of parental care critically influence the developmental environment with the capacity to impact the growth, survival, physiology, and behaviour of offspring. Plastic changes in DNA methylation have been hypothesised to modulate gene expression responses to parental environments. Moreover, these effects can be inherited and so may affect the process of adaptive evolution. In this study, using experimental evolution, we investigated how plastic changes in DNA methylation induced by the loss of parental care have evolved in a biparental insect (Nicrophorus vespilloides) using experimental evolution. We show that removal of care in a single generation is associated with changes in gene expression in stress-related pathways in 1st instar larvae. However, in larvae that have adapted to the loss of parental care after being deprived of care for 30 generations, gene expression is shifted from stress-related gene expression towards growth and brain development pathways. We found that changes in gene body methylation arose both as a direct response to the loss of parental care and stochastically as populations diverged. Overall, our results suggest that a complex interplay between transcription and DNA methylation shapes the molecular adaptation to environmental change.

evolutionary biology↗

bioRxiv2019

Cryptic host specialisation within Poecilochirus carabi mites explains population differences in the extent of co-adaptation with their burying beetle Nicrophorus vespilloides hosts

Reciprocal selection between symbiotic organisms and their hosts can generate variations in local adaptation between them. Symbionts often form species complexes with lineages partially adapted to various hosts. However, it is unclear how interactions among these lineages influences geographic variation in host-symbiont local adaptation. We addressed this shortcoming with experiments on burying beetles Nicrophorus vespilloides and their specialist phoretic mite Poecilochirus carabi in two adjacent woodlands. Burying beetles transport these mites to vertebrate carrion upon which they both reproduce. P. carabi appears to be a species complex, with distinct lineages that specialise on breeding alongside different Nicrophorus species. We found that in one wood (Gamlingay Woods), N. vespilloides carries a mixture of mite lineages, with each lineage corresponding to one of the four Nicrophorus species that inhabits this wood. However, two burying beetle species coexist in neighbouring Waresley Woods and here N. vespilloides predominantly carries the mite lineage that favours N. vespilloides. Mite lineage mixing alters the degree of local adaptation for both N. vespilloides and the P. carabi mites, affecting reproductive success variably across different woodlands. In Gamlingay, mite lineage mixing reduced N. vespilloides reproductive success, while experimentally purifying mites lineage enhanced it. The near pure lineage of vespilloides mites negligibly impacted Waresley N. vespilloides. Mite reproductive success varied with host specificity: Gamlingay mites had greatest reproductive success on Gamlingay beetles, and performed less well with Waresley beetles. By contrast, Waresley mites had consistent reproductive success, regardless of beetles woodland of origin. We conclude that there is some evidence that N. vespilloides and its specific mite lineage have co-adapted. However, neither N. vespilloides nor its mite lineage adapted to breed alongside other mite lineages. This, we suggest, causes variation between Waresley and Gaminglay Woods in the extent of local adaptation between N. vespilloides beetles and their P. carabi mites.

evolutionary biology↗

bioRxiv2019

Mutualistic interactions with phoretic mites Poecilochirus carabi expand the realised thermal niche of the burying beetle Nicrophorus vespilloides

Mutualisms are so ubiquitous, and play such a key role in major biological processes, that it is important to understand how they will function in a changing world. Here we test whether mutualisms can help populations to persist in challenging new environments, by focusing on the protective mutualism between burying beetles Nicrophorus vespilloides and their phoretic mites (Poecilochirus carabi). Our experiments identify the burying beetles fundamental thermal niche and show that it is restricted by competition with blowfly larvae at higher and lower temperatures (within the natural range). We further demonstrate that mites expand the burying beetles realised thermal niche, by reducing competition with blowflies at lower and higher temperatures, thereby enabling beetles to produce more offspring across a wider thermal range. We conclude that mutualisms can play an important role in promoting survival under novel and adverse conditions, particularly when these conditions enhance the performance of a common enemy.

ecology↗

bioRxiv2018

Competition within species determines the value of a mutualism between species

Social interactions within species, and mutualisms between species are both well characterised, but their influence on each other is poorly understood. We determined how interactions among burying beetles Nicrophorus vespilloides influence the value of their interactions with the mite Poecilochirus carabi. Beetles transport these mites to carrion, upon which both species breed. We show that mites help beetles win intraspecific contests for this scarce resource: mites raise beetle body temperature, which enhances beetle competitive prowess. However, mites confer this benefit only upon smaller beetles, which are otherwise doomed by their size to lose contests for carrion. Larger beetles need no assistance to win a carcass and lose reproductive success when breeding alongside mites. We conclude that social interactions within species explain whether interactions with another species are mutualistic or parasitic.\n\nOne Sentence SummarySocial interactions within species can explain whether interactions with a second species are mutualistic or parasitic.

ecology↗

bioRxiv2018

The evolution of a beneficial association between an animal and a microbial community

Animals are now known to be intimately associated with microbial communities, some of which enhance animal fitness. Yet relatively little is known about how these beneficial associations initially arose. We investigated this problem with an experiment on burying beetles, Nicrophorus vespilloides, which breed on the body of a small dead vertebrate. We found that burying beetles breeding on germ-free mice produced smaller larvae, with lower fitness, than those breeding on conventional germ-laden mice. Thus, burying beetles gain benefits from the microbial community associated with their carrion breeding resource, because they lose fitness when this community is removed experimentally. Our experiment suggests that a symbiosis between an animal and a microbial community might begin as an adaptation to the microbial ecosystem in which the animal lives, even when these microbes exist outside the animal, are transiently associated with it at each generation and are not directly transmitted from parents to offspring.

animal behavior and cognition↗

bioRxiv2017

Superior stimulation of female fecundity by subordinate males provides a mechanism for telegony

When females mate promiscuously, sperm compete within females to fertilise the ova. In theory, a male can increase his success at siring offspring by inducing the female to lay more eggs, as well as by producing more competitive sperm. Here we report that the evolutionary consequences of fecundity stimulation extend beyond rival males, by experimentally uncovering effects on offspring. With experiments on the burying beetle Nicrophorus vespilloides, we show that smaller subordinate males are better able to stimulate female fecundity than larger, dominant males. Furthermore dominant males also benefit from the greater fecundity induced by smaller males, and so gain from the females earlier promiscuity just as predicted by theory. By inducing females to produce more offspring on a limited resource, smaller males cause each larva to be smaller, even those they do not sire themselves. Fecundity stimulation thus promotes the non-genetic inheritance of offspring body size, and provides a mechanism for telegony.

evolutionary biology↗

bioRxiv2017

Social interactions within the family enhance the capacity for evolutionary change

Classical models of evolution seldom predict evolution in the wild. One explanation is that the social environment has important, yet overlooked, effects on how traits change in response to natural selection. We tested this idea with selection experiments on burying beetles (Nicrophorus vespilloides), sub-social insects that exhibit biparental care. Populations responded to selection for larger adults only when parents cared for their offspring, and responded to selection for smaller adults only when we prevented parents from providing care. Comparative analyses revealed a similar pattern: evolutionary increases in species size within the genus Nicrophorus are associated with the obligate provision of care. Synthesising our results with previous studies, we suggest that cooperative social environments enhance the response to selection whereas conflict can prevent further directional selection.

evolutionary biology↗