Rapid local adaptation linked with phenotypic plasticity.
ABSTRACT: Models of "plasticity-first" evolution are attractive because they explain the rapid evolution of new complex adaptations. Nevertheless, it is unclear whether plasticity can facilitate rapid microevolutionary change between diverging populations. Here, we show how plasticity may have generated adaptive differences in fecundity between neighboring wild populations of burying beetles Nicrophorus vespilloides. These populations occupy distinct Cambridgeshire woodlands that are just 2.5 km apart and that probably originated from a common ancestral population about 1000-4000 years ago. We find that populations are divergently adapted to breed on differently sized carrion. Adaptive differences in clutch size and egg size are associated with divergence at loci connected with oogenesis. The populations differ specifically in the elevation of the reaction norm linking clutch size to carrion size (i.e., genetic accommodation), and in the likelihood that surplus offspring will be lost after hatching. We suggest that these two processes may have facilitated rapid local adaptation on a fine-grained spatial scale.
Project description:Classical models of evolution seldom predict the rate at which populations evolve in the wild. One explanation is that the social environment affects how traits change in response to natural selection. Here, we determine how social interactions between parents and offspring, and among larvae, influence the response to experimental selection on adult size. Our experiments focus on burying beetles (Nicrophorus vespilloides), whose larvae develop within a carrion nest. Some broods exclusively self-feed on the carrion while others are also fed by their parents. We found populations responded to selection for larger adults but only when parents cared for their offspring. We also found populations responded to selection for smaller adults too, but only by removing parents and causing larval interactions to exert more influence on eventual adult size. 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 excessive conflict can prevent further directional selection.
Project description:Although cooperative social interactions within species are considered an important driver of evolutionary change, few studies have experimentally demonstrated that they cause adaptive evolution. Here we address this problem by studying the burying beetle Nicrophorus vespilloides. In this species, parents and larvae work together to obtain nourishment for larvae from the carrion breeding resource: parents feed larvae and larvae also self-feed. We established experimentally evolving populations in which we varied the assistance that parents provided for their offspring and investigated how offspring evolved in response. We show that in populations where parents predictably supplied more care, larval mandibles evolved to be smaller in relation to larval mass, and larvae were correspondingly less self-sufficient. Previous work has shown that antagonistic social interactions can generate escalating evolutionary arms races. Our study shows that cooperative interactions can yield the opposite evolutionary outcome: when one party invests more, the other evolves to invest less.
Project description:Burying beetles (genus Nicrophorus) are relatively rare among insects in providing sophisticated parental care. Consequently, they have become model species in research analysing social evolution, the evolution of parental care and mating systems. We used the recently published N. vespilloides genome and transcriptome to develop microsatellite markers. Specifically, we developed 14 polymorphic markers with five to 13 alleles per locus and used them to investigate levels of genetic differentiation in four south Cambridgeshire (UK) populations of N. vespilloides, separated by 21 km at most. The markers revealed significant genetic structuring among populations (global FST = 0.023) with all but one of the pairwise comparisons among populations being significant. The single exception was the comparison between the two closest populations, which are approximately 2.5 km apart. In general, the microsatellite markers showed lower observed heterozygosity than expected. We infer that there is limited dispersal between populations and potentially also some inbreeding within them and suggest that this may be due to habitat fragmentation. We discuss these results in the context of recent laboratory experiments on inbreeding and beetle flight.
Project description:The ability to feed on a wide range of diets has enabled insects to diversify and colonize specialized niches. Carrion, for example, is highly susceptible to microbial decomposers, but is kept palatable several days after an animal's death by carrion-feeding insects. Here we show that the burying beetle Nicrophorus vespilloides preserves carrion by preventing the microbial succession associated with carrion decomposition, thus ensuring a high-quality resource for their developing larvae. Beetle-tended carcasses showed no signs of degradation and hosted a microbial community containing the beetles' gut microbiota, including the yeast Yarrowia In contrast, untended carcasses showed visual and olfactory signs of putrefaction, and their microbial community consisted of endogenous and soil-originating microbial decomposers. This regulation of the carcass' bacterial and fungal community and transcriptomic profile was associated with lower concentrations of putrescine and cadaverine (toxic polyamines associated with carcass putrefaction) and altered levels of proteases, lipases, and free amino acids. Beetle-tended carcasses develop a biofilm-like matrix housing the yeast, which, when experimentally removed, leads to reduced larval growth. Thus, tended carcasses hosted a mutualistic microbial community that promotes optimal larval development, likely through symbiont-mediated extraintestinal digestion and detoxification of carrion nutrients. The adaptive preservation of carrion coordinated by the beetles and their symbionts demonstrates a specialized resource-management strategy through which insects modify their habitats to enhance fitness.
Project description:The evolution of elaborate forms of parental care is an important topic in behavioral ecology, yet the factors shaping the evolution of complex suites of parental and offspring traits are poorly understood. Here, we use a multivariate quantitative genetic approach to study phenotypic and genetic correlations between parental and offspring traits in the burying beetle Nicrophorus vespilloides. To this end, we recorded 2 prenatal traits (clutch size and egg size), 2 postnatal parental behaviors (direct care directed toward larvae and indirect care directed toward resource maintenance), 1 offspring behavior (begging), and 2 measures of breeding success (larval dispersal mass and number of dispersing larvae). Females breeding on larger carcasses provided less direct care but produced larger larvae than females breeding on smaller carcasses. Furthermore, there were positive phenotypic correlations between clutch size, direct, and indirect care. Both egg size and direct care were positively correlated with dispersal mass, whereas clutch size was negatively correlated with dispersal mass. Clutch size and number of dispersed larvae showed genetic variance both in terms of differences between populations of origin and significant heritabilities. However, we found no evidence of genetic variance underlying other parental or offspring traits. Our results suggest that correlations between suites of parental traits are driven by variation in individual quality rather than trade-offs, that some parental traits promote offspring growth while others increase the number of offspring produced, and that parental and offspring traits might respond slowly to selection due to low levels of additive genetic variance.
Project description:The genetics of complex social behaviour can be dissected by examining the genetic influences of component pathways, which can be predicted based on expected evolutionary precursors. Here, we examine how gene expression in a pathway that influences the motivation to eat is altered during parental care that involves direct feeding of larvae. We examine the expression of neuropeptide F, and its receptor, in the burying beetle Nicrophorus vespilloides, which feeds pre-digested carrion to its begging larvae. We found that the npf receptor was greatly reduced during active care. Our research provides evidence that feeding behaviour was a likely target during the evolution of parental care in N. vespilloides Moreover, dissecting complex behaviours into ethologically distinct sub-behaviours is a productive way to begin to target the genetic mechanisms involved in the evolution of complex behaviours.
Project description:Phenotypic plasticity is important in the evolution of traits and facilitates adaptation to rapid environmental changes. However, variation in plasticity at the individual level, and the heritable basis underlying this plasticity is rarely quantified for behavioral traits. Alternative behavioral reproductive tactics are key components of mating systems but are not often considered within a phenotypic plasticity framework (i.e., as reaction norms). Here, using lines artificially selected for repeated mating rate, we test for genetic (G × E) sources of variation in reproductive behavior of male Nicrophorus vespilloides burying beetles (including signaling behavior), as well as the role of individual body size, in responsiveness to changes in social environment. The results show that body size influences the response of individuals' signaling behavior to changes in the social environment. Moreover, there was G × E underlying the responses of males to variation in the quality of social environment experienced (relative size of focal male compared to his rival). This shows that individual variation in plasticity and social sensitivity of signaling behavior can evolve in response to selection on investment in mating behavior, with males selected for high mating investment having greater social sensitivity.
Project description:Ecological conditions are known to change the expression of mutualisms though the causal agents driving such changes remain poorly understood. Here we show that temperature stress modulates the harm threatened by a common enemy, and thereby induces a phoretic mite to become a protective mutualist. Our experiments focus on the interactions between the burying beetle Nicrophorus vespilloides, an associated mite species Poecilochirus carabi and their common enemy, blowflies, when all three species reproduce on the same small vertebrate carrion. We show that mites compete with beetle larvae for food in the absence of blowflies, and reduce beetle reproductive success. However, when blowflies breed on the carrion too, mites enhance beetle reproductive success by eating blowfly eggs. High densities of mites are especially effective at promoting beetle reproductive success at higher and lower natural ranges in temperature, when blowfly larvae are more potent rivals for the limited resources on the carcass.
Project description:Carrion beetles in the genus Nicrophorus rear their offspring on decomposing carcasses where larvae are exposed to a diverse community of decomposer bacteria. Parents coat the carcass with antimicrobial secretions prior to egg hatch (defined as prehatch care) and also feed regurgitated food, and potentially bacteria, to larvae throughout development (defined as full care). Here, we partition the roles of prehatch and posthatch parental care in the transmission and persistence of culturable symbiotic bacteria to larvae. Using three treatment groups (full care, prehatch care only, and no care), we found that larvae receiving full care are predominantly colonized by bacteria resident in the maternal gut while larvae receiving no care are colonized with bacteria from the carcass. More importantly, larvae receiving only prehatch care were also predominantly colonized by maternal bacteria; this result indicates that parental treatment of the carcass, including application of bacteria to the carcass surface, is sufficient to ensure symbiont transfer even in the absence of direct larval feeding. Later in development, we found striking evidence that pupae undergo an aposymbiotic stage, after which they are recolonized at eclosion with bacteria similar to those found on the molted larval cuticle and on the wall of the pupal chamber. Our results clarify the importance of prehatch parental care for symbiont transmission in Nicrophorus vespilloides and suggest that these bacteria successfully outcompete decomposer bacteria during larval and pupal gut colonization.IMPORTANCE Here, we examine the origin and persistence of the culturable gut microbiota of larvae in the burying beetle Nicrophorus vespilloides This insect is particularly interesting for this study because larvae are reared on decomposing vertebrate carcasses, where they are exposed to high densities of carrion-decomposing microbes. Larvae also receive extensive parental care in the form of carcass preservation and direct larval feeding. We find that parents transmit their gut bacteria to larvae both directly, through regurgitation, and indirectly via their effects on the carcass. In addition, we find that larvae become aposymbiotic during pupation but are recolonized apparently from bacteria shed onto the insect cuticle before adult eclosion. Our results highlight the diverse interactions between insect behavior and development on microbiota composition. They further suggest that competitive interactions mediate the bacterial composition of Nicrophorus larvae together with or apart from the influence of beetle immunity, suggesting that the bacterial communities of these insects may be highly coevolved with those of their host species.
Project description:We report the application of Chromatraps® Solid-State Chromatin Immunoprecipitation technology for epigenetic profiling of histone modifications in insects. Here, we present the optimised protocol and conditions of Chromatrap® kits for successful ChIP and high-throughput sequencing of established model species, Drosophila melanogaster and the emerging model for behavioural plasticity Nicrophorus vespilloides. We highlight successful ChIP-seq of Drosophila melanogaster (Oregon-R) of comparable quality to modENCODE data and present successful enrichment of histone marks for Nicrophorus vespilloides. The addition of this insect-based ChIP-seq protocol provides a set of optimal guidelines to aid streamline end-users epigenetic research focus and reduce experimental time. Overall design: Optimization of ChIP-seq protocol for insect tissue of two species; Drosophila melanogaster (strain: Oregon-R) and Nicrophorus vespilloides at two different life stages; 3rd instar larvae and adult whole brains respectively. Four replicates per insect investigated using one antibody; H3K4me3 including input controls for each ChIP assay.