Ecological and molecular basis of differential resource use in populations of burying beetles Nicrophorus vespilloides

A fundamental prediction of ecological theory is that competition for resources can drive the evolution of specialised resource use. One way in which costly competition can be avoided is via individual specialisation, i.e., the persistence of specialised individuals within a generalist population that utilise a smaller subset of the entire population’s resource base. This could occur through the evolution of genetic morphs that specialise on different resources. Although correlational evidence exists that is consistent with this prediction, there is surprisingly little evidence that competition causes resource specialisation. Burying beetles are an ideal species for testing this prediction. They require the carcass of a small vertebrate such as a mouse or a songbird for reproduction, but carcasses can be unpredictably distributed and competition to secure ownership is correspondingly intense. For my PhD project in Prof. Rebecca Kilner’s lab, I tested whether this fierce competition for a carcass breeding resource has driven the evolution of beetles that specialise in breeding on dead mammals or dead birds. With field experiments at three different woodlands, I tested for evidence of a bias in the type of carcass favoured by Nicrophorus vespilloides and if this bias changed across the burying beetle season (from April to October each year). I found spatial and seasonal variation within each of the three populations in the preference for dead mice over dead birds. In two populations, beetles were more likely to be trapped upon dead mice overall, but were occasionally trapped with greater frequencies on dead birds. This trend was completely reversed for the third population, where beetles were more likely to be found in traps baited with dead birds than dead mice. The patterns of resource use I observed in the field could be due to adaptive partitioning of resource type within populations. To test this hypothesis, I measured the reproductive success of wild beetles induced to breed on different types of carrion. Although I found seasonal variation in beetle reproductive success on different types of carrion, I found no evidence that this resulted from variation in carrion preferences at the individual or population level. Instead, it is more likely to be explained by variation in individual quality. In collaboration with Dr Michael Sheehan at Cornell University, we sequenced females trapped on each type of carrion within all three woodlands, to test whether carrion specialisation was associated with genetic differences. Consistent with this possibility, we found divergence at ~ 50 loci in each of the three populations. Several of these loci were associated with olfaction and sensory-system development. In the lab, I set up replicate experimentally evolving populations of N. vespilloides which were bred either on mice or chicks for ~ 20 generations. I used these populations to test whether, in principle, beetles within a natural population could become divergently adapted to specialise on different types of carrion. I found no evidence to support this possibility, perhaps because there was insufficient standing genetic variation in the founding populations to select upon. However, there was some indication that the experimental populations might have diverged in cryptic ways that I did not measure directly. To understand the chemical basis for differential resource use, I carried out several analyses in collaboration with Prof. Patrizia d'Ettorre at Université Paris, using mass spectrometric techniques. We found little evidence that the volatiles emitted from carrion differ substantially between birds and mice. We also found little evidence that a beetle’s cuticular hydrocarbons predict the carrion it will be attracted to in nature. However, we did find seasonal variation in the cuticular hydrocarbon profiles of wild-caught beetles that could be related to beetle quality or breeding status. In short, although we found some evidence for differential carrion use within wild burying beetle populations and some indication that this is associated with genetic differences among individuals, some of this variation is also due to phenotypic variation in individual quality. While it is possible that carrion specialists could evolve within natural populations, we found no strong evidence to suggest that this happens routinely.I received financial support from St. John’s College, the Cambridge Philosophical Society, the Santander International Mobility Grant, the Gilchrist Educational Trust, the Leche Trust, the Department of Zoology as well as the University of Cambridge for my studies, research collaborations and during periods of hardshi

Carrion type and extent of breeding success together influence subsequent carrion choice by adult burying beetles

Publication status: PublishedFunder: St. John's College, CambridgeFunder: University of Cambridge; doi: http://dx.doi.org/10.13039/501100000735Insects 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 Nicrophorus vespilloides modulate their choice of carrion type in relation to the outcome of their past breeding experience. Burying beetles require the carcass of a small vertebrate, such as a mouse or a chick, to reproduce. Beetle parents convert this carrion into an edible nursery for their larvae, whom they typically care for throughout larval development. We tested whether a beetle's past breeding experience influenced its subsequent choice of carrion when presented simultaneously with either a dead mouse or a dead chick. We found that beetles that bred on a mouse and produced many larvae in their first breeding attempt subsequently favoured mice over chicks for their second breeding attempt. 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

Selection on the joint actions of pairs leads to divergent adaptation and coadaptation of care-giving parents during pre-hatching 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 female’s line of origin. We discuss how social coadaptations within pairs or groups could act as a post-mating barrier to gene flow

Selection on the joint actions of pairs leads to divergent adaptation and coadaptation of care-giving parents during pre-hatching care.

Peer reviewed: TruePublication status: PublishedFunder: European Research Council; FundRef: http://dx.doi.org/10.13039/501100000781Funder: Royal Society; FundRef: http://dx.doi.org/10.13039/501100000288Funder: Human Frontiers Science ProgramThe 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: NC lines) than with post-hatching care (Full Care: FC lines). Here, we investigate how this joint activity evolved. After 15 generations of experimental evolution, we created heterotypic pairs (NC females with FC males and NC males with FC females) and compared their carrion nest making with homotypic NC and FC pairs. We found that pairs with NC males prepared the nest more rapidly than pairs with FC males, regardless of the female's line of origin. We discuss how social coadaptations within pairs or groups could act as a post-mating barrier to gene flow

Data from: Female density-dependent chemical warfare underlies fitness effects of group sex ratio in flour beetles

In animals, skewed sex ratios can affect individual fitness either via sexual (e.g. intersexual conflict or intrasexual mate competition) or non-sexual interactions (e.g. sex-specific resource competition). Because most analyses of sex ratio focus on sexual interactions, the relative importance of sexual vs. non-sexual mechanisms remains unclear. We tested both mechanisms in the flour beetle Tribolium castaneum, where male-biased sex ratios increase female fitness relative to unbiased or female-biased groups. Although flour beetles show both sexual and non-sexual (resource) competition, we found that sexual interactions did not explain female fitness. Instead, female fecundity was dramatically reduced even after a brief exposure to flour conditioned by other females. Earlier studies suggested that secreted toxins might mediate density-dependent population growth in flour beetles. We identified ethyl- and methyl- benzoquinone (EBQ and MBQ; “quinones”), as components of adult stink glands that regulate female fecundity. In female-biased groups (i.e. at high female density), females upregulated quinones and suppressed each other’s reproduction. In male-biased groups, low female density and associated low quinone levels maximized fecundity. Thus, females appear to use quinones as weapons for female-specific, density-dependent interference competition. Our results underscore the importance of non-sexual interference competition that may often underlie the fitness consequences of skewed sex ratios

Selection on the joint actions of pairs leads to divergent adaptation and coadaptation of care-giving parents during pre-hatching care

Peer reviewed: TruePublication status: PublishedFunder: European Research Council; FundRef: http://dx.doi.org/10.13039/501100000781Funder: Royal Society; FundRef: http://dx.doi.org/10.13039/501100000288Funder: Human Frontiers Science ProgramThe 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: NC lines) than with post-hatching care (Full Care: FC lines). Here, we investigate how this joint activity evolved. After 15 generations of experimental evolution, we created heterotypic pairs (NC females with FC males and NC males with FC females) and compared their carrion nest making with homotypic NC and FC pairs. We found that pairs with NC males prepared the nest more rapidly than pairs with FC males, regardless of the female’s line of origin. We discuss how social coadaptations within pairs or groups could act as a post-mating barrier to gene flow

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