Behavioral dominance interactions between Nicrophorus orbicollis and N. tomentosus burying beetles (Coleoptera: Silphidae)

Asymmetric interference competition, where one species is behaviorally dominant over another, appears widespread in nature with the potential to structure ecological communities through trade-offs between competitive dominance and environmental tolerance. The details of how species interact and the factors that contribute to behavioral dominance, however, are poorly known for most species, yet such details are important for understanding when and why trade-offs occur. Here, we examine behavioral interactions between two species of burying beetles (Coleoptera: Silphidae) that compete for limited breeding resources (i.e., small vertebrate carcasses) in nature, to identify behaviors involved in interference competition and to test if large body size, species identity, or time of arrival best predict behavioral dominance among species. To test these ideas, we placed same-sex individuals of Nicrophorus orbicollis (early to mid-summer breeder) and N. tomentosus (late summer to fall breeder) into an enclosure together with a 25–30 g mouse carcass (Mus musculus). We then video-recorded all behaviors, including neutral and aggressive interactions, for 13 h per trial (N = 14 trials). For each interaction, we assigned a winner based on which beetle retained its position instead of fleeing or retained possession of the carcass; the overall behavioral dominant was determined as the individual that won the most interactions over the length of the trial. We found that large body size was the best predictor of behavioral dominance. In most interactions, N. orbicollis was larger and dominant over N. tomentosus; however, when N. tomentosus was larger they outcompeted smaller N. orbicollis, illustrating the importance of body size in aggressive contests. The order of arrival to the carcass (priority effects) did not predict behavioral dominance. The larger size and abundance of N. orbicollis in nature suggest a competitive asymmetry between the species, supporting the idea that N. orbicollis constrains the ability of N. tomentosus to breed earlier in the summer.

Estimating Population Abundance of Burying Beetles Using Photo-Identification and Mark-Recapture Methods

Successful conservation and management of protected wildlife populations require reliable population abundance data. Traditional capture-mark-recapture methods can be costly, time-consuming, and invasive. Photographic mark-recapture (PMR) is a cost-effective, minimally invasive way to study population dynamics in species with distinct markings or color patterns. We tested the feasibility and the application of PMR using the software Hotspotter to identify Nicrophorus spp. from digital images of naturally occurring spot patterns on their elytra. We conducted a laboratory study evaluating the identification success of Hotspotter on Nicrophorus americanus (Olivier, 1790) and Nicrophorus orbicollis (Say, 1825) before implementation of a mark-recapture study in situ. We compared the performance of Hotspotter using both ‘high-quality’ and ‘low-quality’ photographs. For high-quality photographs, Hotspotter had a false rejection rate of 2.7–3.0% for laboratory-reared individuals and 3.9% for wild-caught individuals. For low-quality photographs, the false rejection rate was much higher, 48.8–53.3% for laboratory-reared individuals and 28.3% for wild-caught individuals. We subsequently analyzed encounter histories of wild-caught individuals with closed population models in Program MARK to estimate population abundance. In our study, we demonstrated the utility of using PMR in estimating population abundance for Nicrophorus spp. based on elytral spot patterns.

Habitat use of co-occurring burying beetles (genus Nicrophorus) in southeastern Ontario, Canada

The coexistence of closely related species plays an important role in shaping local diversity. However, competition for shared resources can limit the ability of species to coexist. Many species avoid the costs of coexistence by diverging in habitat use, known as habitat partitioning. We examine patterns of habitat use in seven co-occurring species of burying beetles (genus Nicrophorus Fabricius, 1775), testing the hypothesis that Nicrophorus species partition resources by occupying distinct habitats. We surveyed Nicrophorus abundance and 54 habitat characteristics at 100 random sites spanning an environmentally diverse region of southeastern Ontario, Canada. We found that three species occupied distinct habitat types consistent with habitat partitioning. Specifically, Nicrophorus pustulatus Herschel, 1807, Nicrophorus hebes Kirby, 1837, and Nicrophorus marginatus Fabricius, 1801 appear to be specialists for forest canopy, wetlands, and open fields, respectively. In contrast, Nicrophorus orbicollis Say, 1825, Nicrophorus sayi Laporte, 1840, and Nicrophorus tomentosus Weber, 1801 appear to be generalists with wide breadths of habitat use. We were unable to identify the habitat associations of Nicrophorus defodiens Mannerheim, 1846. Our findings are consistent with habitat acting as an important resource axis along which some Nicrophorus species partition; however, divergence along other resource axes (e.g., temporal partitioning) also appears important for Nicrophorus coexistence.

Disrupting information alters the behavioral response to a mutual signal trait in both sexes of Nicrophorus (Coleoptera: Silphidae) burying beetles

Effective signals transfer information in a way that enhances the fitness of the sender. Signal traits are often sexually dimorphic. However, in some species, males and females display similar signals, and these mutual signals are less often studied. Competition for resources occurs in both males and females, and mate choice is likely to occur whenever mates vary in quality and reproductive investment is high. Nicrophorus burying beetles compete intrasexually over the carrion resources on which they biparentally raise their young. Nicrophorus species also often have clypeal membranes which scale hyperallometrically with body size, exaggerating the apparent body size of larger individuals. To examine the potential signaling function of clypeal membranes, we examined the behavioral responses of male and female Nicrophorus orbicollis and Nicrophorus pustulatus burying beetles to same- and opposite-sex social partners which had their membranes painted black or clear. We found evidence that blocking the information in clypeal membranes affected intrasexual aggressive interactions for both sexes of both species. Blocking a female’s signal reduced the likelihood of mating attempts for male N. pustulatus, whereas blocking a male’s signal influenced female rejection behaviors in N. orbicollis. Our results show that males and females can experience similar selection pressures, and suggest that examining mutual signals in a broader range of systems will expand our understanding of evolutionary differences and similarities between the sexes.

Ecological divergence of burying beetles into the forest canopy

Closely related species with overlapping geographic ranges encounter a significant challenge: they share many ecological traits and preferences but must partition resources to coexist. In Ontario, potentially eleven species of carrion beetles (Coleoptera: Silphidae) live together and require vertebrate carrion for reproduction. Their reliance on an ephemeral and uncommon resource that is unpredictable in space and time is thought to create intense intra- and interspecific competition. Evidence suggests that burying beetle species reduce competition by partitioning carrion for breeding across different habitats, temperatures, and seasons. Here, we test predictions of an alternative axis for partitioning carrion: vertical partitioning between the ground and forest canopy. We conducted a survey of carrion beetles from May to July 2016 at the Queen’s University Biological Station across 50 randomly generated points using baited lethal traps at zero and six metres. Ground traps yielded more species and individuals compared to those in the canopy, and the number of individuals and species caught increased through the season in both trap types. Ground and canopy traps were accurately distinguished by the presence or absence of three species: ground traps contained more Nicrophorus orbicollis and Necrophila americana, while canopy traps contained more Nicrophorus pustulatus. We trapped 253 N. pustulatus in the canopy, but only 60 on the ground. N. pustulatus is thought to be rare across its geographic range, but our results suggest it is uniquely common in canopy habitats, demonstrating a vertical partitioning of habitat and resources. Our results are consistent with N. pustulatus having diverged into canopy habitats as a strategy to coexist with closely related sympatric species when competing for similar resources. We still, however, do not know the traits that allow N. pustulatus to flourish in the canopy, exactly how N. pustulatus uses canopy resources for breeding, or the factors that restrict the expansion of other burying beetles into this habitat.

Divergent coevolutionary trajectories in parent–offspring interactions and discrimination against brood parasites revealed by interspecific cross-fostering

In animal families, parents are expected to adapt to their offspring's traits, and offspring, in turn, are expected to adapt to the environment circumscribed by their parents. However, whether such coevolutionary trajectories differ between closely related species is poorly understood. Here, we employ interspecific cross-fostering in three species of burying beetles, Nicrophorus orbicollis , Nicrophorus pustulatus and Nicrophorus vespilloides , to test for divergent co-adaptation among species with different degrees of offspring dependency on parental care, and to test whether they are able to discriminate against interspecific parasites. We found that offspring survival was always higher when offspring were reared by conspecific rather than heterospecific parents. In the case of N. orbicollis raising N. pustulatus , none of the larvae survived. Overall, these results indicate that parent and offspring traits have diverged between species, and that the differential survival of conspecific and heterospecific larvae is because of improper matching of co-adapted traits, or, in the case of N. orbicollis with larval N. pustulatus , because of selection on parents to recognize and destroy interspecific brood parasites. We suggest that burying beetles experiencing a high risk of brood parasitism have evolved direct recognition mechanisms that enable them to selectively kill larvae of potential brood parasites.

Ecological divergence of burying beetles into the forest canopy

Closely related species with overlapping geographic ranges encounter a significant challenge: they share many ecological traits and preferences but must partition resources to coexist. In Ontario, potentially eleven species of carrion beetles (Coleoptera: Silphidae) live together and require vertebrate carrion for reproduction. Their reliance on an ephemeral and uncommon resource that is unpredictable in space and time is thought to create intense intra- and interspecific competition. Evidence suggests that burying beetle species reduce competition by partitioning carrion for breeding across different habitats, temperatures, and seasons. Here, we test predictions of an alternative axis for partitioning carrion: vertical partitioning between the ground and forest canopy. We conducted a survey of carrion beetles from May to July 2016 at the Queen’s University Biological Station across 50 randomly generated points using baited lethal traps at 0m and 6m. Ground traps yielded more species and individuals compared to those in the canopy, and the number of individuals and species caught increased through the season in both trap types. Ground and canopy traps were accurately distinguished by the presence or absence of three predictor species: ground traps contained more Nicrophorus orbicollis and Necrophila americana, while canopy traps contained more Nicrophorus pustulatus. Indeed, we trapped 253 N. pustulatus in the canopy, but only 60 on the ground; N. pustulatus was the most common species in the canopy, and the only species that was more common in the 6m traps than on the ground. N. pustulatus is thought to be rare across its geographic range, but our results suggest instead that N. pustulatus is uniquely common in canopy habitats, demonstrating a vertical partitioning of habitat and resources between N. pustulatus and other co-occurring burying beetles. Our results are consistent with N. pustulatus having diverged into canopy habitats as a strategy to coexist with closely related sympatric species when competing for similar resources. We still, however, do not know the traits that allow N. pustulatus to flourish in the canopy, exactly how N. pustulatus uses canopy resources for breeding, or the factors that restrict the expansion of other burying beetles into this habitat.

Ecological divergence of burying beetles into the forest canopy

Closely related species with overlapping geographic ranges encounter a significant challenge: they share many ecological traits and preferences but must partition resources to coexist. In Ontario, potentially eleven species of carrion beetles (Coleoptera: Silphidae) live together and require vertebrate carrion for reproduction. Their reliance on an ephemeral and uncommon resource that is unpredictable in space and time is thought to create intense intra- and interspecific competition. Evidence suggests that burying beetle species reduce competition by partitioning carrion for breeding across different habitats, temperatures, and seasons. Here, we test predictions of an alternative axis for partitioning carrion: vertical partitioning between the ground and forest canopy. We conducted a survey of carrion beetles from May to July 2016 at the Queen’s University Biological Station across 50 randomly generated points using baited lethal traps at 0m and 6m. Ground traps yielded more species and individuals compared to those in the canopy, and the number of individuals and species caught increased through the season in both trap types. Ground and canopy traps were accurately distinguished by the presence or absence of three predictor species: ground traps contained more Nicrophorus orbicollis and Necrophila americana, while canopy traps contained more Nicrophorus pustulatus. Indeed, we trapped 253 N. pustulatus in the canopy, but only 60 on the ground; N. pustulatus was the most common species in the canopy, and the only species that was more common in the 6m traps than on the ground. N. pustulatus is thought to be rare across its geographic range, but our results suggest instead that N. pustulatus is uniquely common in canopy habitats, demonstrating a vertical partitioning of habitat and resources between N. pustulatus and other co-occurring burying beetles. Our results are consistent with N. pustulatus having diverged into canopy habitats as a strategy to coexist with closely related sympatric species when competing for similar resources. We still, however, do not know the traits that allow N. pustulatus to flourish in the canopy, exactly how N. pustulatus uses canopy resources for breeding, or the factors that restrict the expansion of other burying beetles into this habitat.

The transcriptional basis of quantitative behavioral variation

What causes individuals to produce quantitatively different phenotypes? While substantial research has focused on the allelic changes that affect phenotype, we know less about how gene expression accompanies variable phenotypes. Here, we investigate the transcriptional basis of variation in parental provisioning using two species of burying beetle, Nicrophorus orbicollis and Nicrophorus vespilloides. Specifically, we used RNA-seq to compare the transcriptomes of parents that provided high amounts of provisioning behavior versus low amounts in males and females of each species. We found that there were no overarching transcriptional patterns that distinguish high from low caring parents, and no informative transcripts that displayed particularly large expression differences in females or males. However, we did find more subtle gene expression changes between high and low provisioning parents that are consistent across sexes as well as between the two species. Furthermore, we show that transcripts previously implicated in transitioning into parental care in N. vespilloides had high variance in the levels of transcription and were unusually likely to display differential expression between high and low provisioning parents. Thus, quantitative behavioral variation appears to reflect many transcriptional differences of small effect. We show that nuanced regulation of the same gene products that are required for the transition of one behavioral state to another are also those influencing variation within a behavioral state.Author SummaryBurying beetles in the genus Nicrophorus breed on vertebrate carcasses and provide advanced parental care to their offspring by regurgitating partially digested flesh. However, all adult beetles do not uniformly express this trait. Some provide a large amount of parenting to their offspring, and some only a little. Here, we investigate the genetic causes of why some Nicrophorus beetles feed their offspring more than others. We demonstrate that this difference is likely caused by many small changes in gene expression, rather than a few genes that have major effects. We also find that some of the same genes that help to turn on parental care behavior in burying beetles also seem to play a role in determining how much care a beetle gives. These results provide new angles on longstanding questions about the complexity of the mechanisms that underlie quantitative variation in populations.