Conditional indirect genetic effects of caregivers on brood in the clonal raider ant

Abstract

Caregivers shape the rearing environment of their young. Consequently, offspring traits are influenced by the genes of their caregivers via indirect genetic effects (IGEs). However, the extent to which IGEs are modulated by environmental factors, other than the genotype of social partners (i.e., intergenomic epistasis), remains an open question. Here we investigate how brood are influenced by the genotype of their caregivers in the clonal raider ant, Ooceraea biroi, a species in which the genotype, age and number of both caregivers and brood can be experimentally controlled. First, we used four clonal lines to establish colonies that differed only in the genotype of caregivers and measured effects on foraging activity, as well as IGEs on brood phenotypes. In a second experiment, we tested whether these IGEs are conditional on the age and number of caregivers. We found that caregiver genotype affected the feeding and foraging activity of colonies, and influenced the rate of development, survival, body size, and caste fate of brood. Caregiver genotype interacted with other factors to influence the rate of development and survival of brood, demonstrating that IGEs can be conditional. Thus, we provide an empirical example of phenotypes being influenced by IGE-by-environment interactions beyond intergenomic epistasis, highlighting that IGEs of caregivers/parents are alterable by factors other than their brood’s/offspring’s genotype.

Intergenerational genotypic interactions drive collective behavioural cycles in a social insect

“…This is supported by Piekarski et al . [29], who report reduced foraging activity in workers of line A. The finding that both larvae and workers of the same line (A) were sufficient to prolong cycle length suggests a genetic effect acting on both larval growth and worker foraging activity.…”

“…Some of these findings are corroborated by Piekarski et al . [29] who report higher motility in line D workers and larger body size in brood reared by workers of line A using different metrics. More surprisingly, we detect several instances of indirect genetic effects of the brood on worker behaviour, with larval genotype affecting the amount of time workers spend in the nest as well as their walking speed.…”

“…More surprisingly, we detect several instances of indirect genetic effects of the brood on worker behaviour, with larval genotype affecting the amount of time workers spend in the nest as well as their walking speed. While effects of the rearing environment on brood development, and particularly on sex and caste allocation, have been extensively studied in social insects [29–33], whether and how the brood can affect worker behaviour has received comparatively little attention. Previous work in other systems has shown that the brood of social insects can produce chemical [34], behavioural [35] and acoustic [36] cues, some of which influence worker behaviour [37,38].…”

Studying the genetic basis of ecological interactions with intergenomic epistasis

“…Intergenomic epistasis within an individual has been used to describe interactions between mitochondrial and nuclear DNA (e.g., Dowling et al, 2007;Immonen et al, 2020) and hybrid incompatibilities (e.g., Woods et al, 2009). Intergenomic epistasis between individuals has been described in socially interacting individuals of the same species, such as ants, where the interactions between genotypes can affect brood development (e.g., Linksvayer, 2007;Piekarski et al, 2023;Teseo et al, 2014), or in ecologically interacting individuals of different species, as discussed in this paper.…”