The role of indirect genetic effects in the evolution of interacting reproductive behaviors in the burying beetle, Nicrophorus vespilloides

Abstract

Social interactions can give rise to indirect genetic effects (IGEs), which occur when genes expressed in one individual affect the phenotype of another individual. The evolutionary dynamics of traits can be altered when there are IGEs. Sex often involves indirect effects arising from first-order (current) or second-order (prior) social interactions, yet IGEs are infrequently quantified for reproductive behaviors. Here, we use experimental populations of burying beetles that have experienced bidirectional selection on mating rate to test for social plasticity and IGEs associated with focal males mating with a female either without (first-order effect) or with (second-order effect) prior exposure to a competitor, and resource defense behavior (first-order effect). Additive IGEs were detected for mating rate arising from (first-order) interactions with females. For resource defense behavior, a standard variance partitioning analysis provided no evidence of additive genetic variance-either direct or indirect. However, behavior was predicted by focal size relative to that of the competitor, and size is also heritable. Assuming that behavior is causally dependent on relative size, this implies that both DGEs and IGEs do occur (and may potentially interact). The relative contribution of IGEs may differ among social behaviors related to mating which has consequences for the evolutionary trajectories of multivariate traits.

Keywords: indirect genetic effect; mating; mating system; resource defense; social plasticity.

Figure 1

Nicrophorus vespilloides on carcass of common shrew Sorex araneus in the wild with interspecific competitors in attendance (blowflies, Calliphoridae). Photograph by Nick Royle

Figure 2

Potential responses of beetles from regimes selected for high (unbroken line) or low (dotted line) repeated mating rate to a change in social environment (absence (No‐comp) or presence (Comp) of male–male competition) for response variables (Z). (a) Illustrates the scenario where there is a difference in the mean values of traits between individuals from different selection regimes but no plasticity across social environments. (b) the selection regimes differ in mean values and there is plasticity but no G × E (selection regime × environment interaction). In contrast, (c) shows a significant G × E

Figure 3

Variance and covariance components estimated in our experimental design. Mating rate (MR) and resource defense (CA) behaviors of focal males maybe influenced by direct genetic effects (a_i) and/or indirect genetic effects as a result of social interactions with both rival, competitor males (m_j with first‐order effects indicated by the solid arrow and second‐order effects indicated by the dashed‐line arrow) and females (f_k—a first‐order effect). Covariance relationships estimated in our models are indicated by the dotted‐line arrows. See main text for more details. Photographs by Paul Hopwood, Jena Johnson, and Nick Royle

Figure 4

Predicted mean (± 1SE) male mating rate (MR) and resource defense (CA; amount of time spent active on the carcass) in relation to selection regime (Red circles = high line, Blue triangles = low line) and social environments experienced. The social environment (presence or absence of a rival, competitor male during resource defense prior to mating) is a second‐order effect for MR and a first‐order effect for CA; see main text for further details, including sample sizes