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.

It takes two: Heritable male effects on reproductive timing but not clutch size in a wild bird population*

“…Clearly, incorporating the impact of the social environment into empirical description of evolutionary dynamics under natural settings is a considerable challenge, and it is perhaps unsurprising that published estimates of direct-indirect genetic correlations for free-living populations are exceedingly few (Fisher and Pruitt 2019;Hunt et al 2019), despite the increasing application of quantitative genetic analyses to long-term study populations more generally (Postma 2014). Nonetheless, while the extent to which indirect genetic determination applies to behavioral traits remains unclear, recent results from laboratory studies suggest it is potentially widespread (Carter et al 2019;Dewan et al 2019). Of course, expression of a host of behaviors is sensitive to the phenotype of unrelated social partners, as testified by studies of mate choice (Bateson 1983), resource competition (Hardy and Briffa 2013), and social structure (Krause et al 2015).…”

“…Nonetheless, while the extent to which indirect genetic determination applies to behavioral traits remains unclear, recent results from laboratory studies suggest it is potentially widespread (Carter et al. 2019; Dewan et al. 2019).…”

“…However, social interactions between non-relatives can also give rise to IGEs (Wade et al 2010;Costa e Silva et al 2013), although published estimates for populations in natural settings are scant (Hunt et al 2019). In this context, sexual partnerships have clear potential to facilitate indirect genetic effects, particularly in species where pairs form an association that persists beyond fertilization (Carter et al 2019;Chakrabarty et al 2019). In many animal taxa, for example, both sexes exhibit parental care, such that raising offspring is a shared task.…”

“…In this context, sexual partnerships have clear potential to facilitate indirect genetic effects, particularly in species where pairs form an association that persists beyond fertilization (Carter et al. 2019; Chakrabarty et al. 2019).…”

Honey bee colony aggression and indirect genetic effects

“…Social experiences can affect different levels of biological organization (e.g., neural transmission, gene expression, and development) acting on different timescales (10). IGEs are found in many species of insects including beetles (11) and the fruit fly (12,13), fire ant (7), and honey bee (6,14); however, a link to group allele frequencies has not been established, and mechanistic studies of IGEs are lacking.…”