Influence of Genetic Variation in the Biotic Environment on Phenotypic Variation in a Plant-feeding Insect

While many species spend much of their lives in close association with other organisms, only recently have biologists started to explore the implications of the biotic nature of environments for their role as causes of variation in phenotypes. This means that the genotypes of individuals that constitute the biotic environment may influence the phenotypes of individuals that live in that environment. These are called indirect genetic effects (IGEs) when they occur between conspecifics, and interspecific indirect genetic effects (IIGEs) when they occur between heterospecifics. However, the impact of genetic variation in biotic environments remains largely unknown. I used a member of the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae) to assess how male mating signals and female mate preferences are influenced by genetic variation in biotic environments. I used novel implementations of classic quantitative genetics designs, with samples of full-sibling families of treehoppers (IGEs) and clone lines of a sample of host plant genotypes (IIGEs) constituting the background biotic environment. To measure IGEs, I used full-sibling split-families as treatment social environments, and reared a random sample of focal females alongside each treatment family, describing the mate preferences of these focal females. With this I detected substantial genetic variation in social influence on mate preferences: the mate preferences of focal females varied according to the treatment families along with which they grew up. To measure IIGEs, I reared a random sample of treehoppers on potted replicates of a sample of host plant clones, describing the male signals and female mate preferences of these individuals. I found that male signals and female mate preferences varied according to the clone line on which they developed, demonstrating that genetic variation in host plants has cross-trophic consequences on sexually-selected traits at the level of the insect. I discuss the evolutionary implications of the presence of such genetic variation in biotic environments on male signals and female mate preferences. I focus on how IGEs and IIGEs may influence the way in which selection may act within and across environments, including potential contributions to the maintenance of genetic variation and the promotion of evolutionary divergence

An evolutionary switch from sibling rivalry to sibling cooperation, caused by a sustained loss of parental care.

Sibling rivalry is commonplace within animal families, yet offspring can also work together to promote each other's fitness. Here we show that the extent of parental care can determine whether siblings evolve to compete or to cooperate. Our experiments focus on the burying beetle Nicrophorus vespilloides, which naturally provides variable levels of care to its larvae. We evolved replicate populations of burying beetles under two different regimes of parental care: Some populations were allowed to supply posthatching care to their young (Full Care), while others were not (No Care). After 22 generations of experimental evolution, we found that No Care larvae had evolved to be more cooperative, whereas Full Care larvae were more competitive. Greater levels of cooperation among larvae compensated for the fitness costs caused by parental absence, whereas parental care fully compensated for the fitness costs of sibling rivalry. We dissected the evolutionary mechanisms underlying these responses by measuring indirect genetic effects (IGEs) that occur when different sibling social environments induce the expression of more cooperative (or more competitive) behavior in focal larvae. We found that indirect genetic effects create a tipping point in the evolution of larval social behavior. Once the majority of offspring in a brood start to express cooperative (or competitive) behavior, they induce greater levels of cooperation (or competition) in their siblings. The resulting positive feedback loops rapidly lock larvae into evolving greater levels of cooperation in the absence of parental care and greater levels of rivalry when parents provide care

Adaptive evolution of synchronous egg-hatching in compensation for the loss of parental care.

Interactions among siblings are finely balanced between rivalry and cooperation, but the factors that tip the balance towards cooperation are incompletely understood. Previous observations of insect species suggest that (i) sibling cooperation is more likely when siblings hatch at the same time, and (ii) this is more common when parents provide little to no care. In this paper, we tested these ideas experimentally with the burying beetle, Nicrophorus vespilloides Burying beetles convert the body of a small dead vertebrate into an edible nest for their larvae, and provision and guard their young after hatching. In our first experiment, we simulated synchronous or asynchronous hatching by adding larvae at different intervals to the carrion-breeding resource. We found that 'synchronously' hatched broods survived better than 'asynchronously' hatched broods, probably because 'synchronous hatching' generated larger teams of larvae, that together worked more effectively to penetrate the carrion nest and feed upon it. In our second experiment, we measured the synchronicity of hatching in experimental populations that had evolved for 22 generations without any post-hatching care, and control populations that had evolved in parallel with post-hatching care. We found that larvae were more likely to hatch earlier, and at the same time as their broodmates, in the experimental populations that evolved without post-hatching care. We suggest that synchronous hatching enables offspring to help each other when parents are not present to provide care. However, we also suggest that greater levels of cooperation among siblings cannot compensate fully for the loss of parental care

Adaptation to a novel family environment involves both apparent and cryptic phenotypic changes

Cryptic evolution occurs when evolutionary change is masked by concurrent environmental change. In most cases, evolutionary changes in the phenotype are masked by changing abiotic factors. However, evolutionary change in one trait might also be masked by evolutionary change in another trait, a phenomenon referred to as evolutionary environmental deterioration. Nevertheless, detecting this second type of cryptic evolution is challenging and there are few compelling examples. Here, we describe a likely case of evolutionary environmental deterioration occurring in experimental burying beetle (Nicrophorus vespilloides) populations that are adapting to a novel social environment that lacks post-hatching parental care. We found that populations rapidly adapted to the removal of post-hatching parental care. This adaptation involved clear increases in breeding success and larval density (number of dispersing larvae produced per gram of breeding carcass), which in turn masked a concurrent increase in the mean larval mass across generations. This cryptic increase in larval mass was accomplished through a change in the reaction norm that relates mean larval mass to larval density. Our results suggest that cryptic evolution might be commonplace in animal families, because evolving trophic and social interactions can potentially mask evolutionary change in other traits, like body size.The authors were supported by a Consolidator's Grant from the European Research Council (310785 Baldwinian Beetles) to R.M.K. R.M.K. had additional support from a Wolfson Merit Award from the Royal Society. The research was also funded by the Natural Environment Research Council, UK (NE/H019731/1), the European Research Council and the Department of Zoology at the University of Cambridge

Evolutionary change in the construction of the nursery environment when parents are prevented from caring for their young directly.

Funder: EC | FP7 | FP7 Ideas: European Research Council (FP7 Ideas); Id: 100011199; Grant(s): 310785Parental care can be partitioned into traits that involve direct engagement with offspring and traits that are expressed as an extended phenotype and influence the developmental environment, such as constructing a nursery. Here, we use experimental evolution to test whether parents can evolve modifications in nursery construction when they are experimentally prevented from supplying care directly to offspring. We exposed replicate experimental populations of burying beetles (Nicrophorus vespilloides) to different regimes of posthatching care by allowing larvae to develop in the presence (Full Care) or absence of parents (No Care). After only 13 generations of experimental evolution, we found an adaptive evolutionary increase in the pace at which parents in the No Care populations converted a dead body into a carrion nest for larvae. Cross-fostering experiments further revealed that No Care larvae performed better on a carrion nest prepared by No Care parents than did Full Care larvae. We conclude that parents construct the nursery environment in relation to their effectiveness at supplying care directly, after offspring are born. When direct care is prevented entirely, they evolve to make compensatory adjustments to the nursery in which their young will develop. The rapid evolutionary change observed in our experiments suggests there is considerable standing genetic variation for parental care traits in natural burying beetle populations-for reasons that remain unclear

Variation in Enchenopa male signal traits

Measurements of 7 Enchenopa male signal traits from two separate experiments. Each row corresponds to an individual male, and the first column denotes from which experiment each male belongs. Each signal trait is in its own column

Data from: Genetic variation in host plants influences the mate preferences of a plant-feeding insect

Many species spend their lives in close association with other organisms, and the environments provided by those organisms can play an important role as causes of variation in phenotypes. When this is the case, the genotypes of the individuals constituting the environment may influence the phenotypes of individuals living in that environment. When these effects are between heterospecifics, interspecific indirect genetic effects (IIGEs) occur. Several studies have detected IIGEs, but whether IIGEs contribute to variation in sexually selected traits remains virtually unexplored. We assessed how mate preferences in a plant-feeding insect are influenced by the genotype of their host plant. We established clone lines of a sample of host plant genotypes constituting the background biotic environment for a random sample of insects that we reared on them. We found that the insects’ mate preferences varied according to the clone line on which they developed. These results demonstrate that genetic variation in host plants has cross-trophic consequences on a trait that has strong effects on fitness and interpopulation dynamics such as diversification in communication systems. We discuss how IIGEs on mate preferences may influence the way in which selection acts, including the maintenance of variation and the promotion of evolutionary divergence