Heritabilities, social environment effects and genetic correlations of social behaviours in a cooperatively breeding vertebrate

Abstract

Social animals interact frequently with conspecifics, and their behaviour is influenced by social context, environmental cues and the behaviours of interaction partners, allowing for adaptive, flexible adjustments to social encounters. This flexibility can be limited by part of the behavioural variation being genetically determined. Furthermore, behaviours can be genetically correlated, potentially constraining independent evolution. Understanding social behaviour thus requires carefully disentangling genetic, environmental, maternal and social sources of variations as well as the correlation structure between behaviours. Here, we assessed heritability, maternal, common environment and social effects of eight social behaviours in Neolamprologus pulcher, a cooperatively breeding cichlid. We bred wild‐caught fish in a paternal half‐sibling design and scored ability to defend a resource against conspecifics, to integrate into a group and the propensity to help defending the group territory (“helping behaviour”). We assessed genetic, social and phenotypic correlations within clusters of behaviours predicted to be functionally related, namely “competition,” “aggression,” “aggression‐sociability,” “integration” and “integration‐help.” Helping behaviour and two affiliative behaviours were heritable, whereas there was little evidence for a genetic basis in all other traits. Phenotypic social effects explained part of the variation in a sociable and a submissive behaviour, but there were no maternal or common environment effects. Genetic and phenotypic correlation within clusters was mostly positive. A group's social environment influenced covariances of social behaviours. Genetic correlations were similar in magnitude but usually exceeding the phenotypic ones, indicating that conclusions about the evolution of social behaviours in this species could be provisionally drawn from phenotypic data in cases where data for genetic analyses are unobtainable.

Contributions of genetic and nongenetic sources to variation in cooperative behavior in a cooperative mammal

“…A recent study of banded mongooses (M. mungo) used a double pedigree approach with the "natural cross fostering" occurring in this species to tease apart genetic and social inheritance in the propensity and amount of babysitting and pup escorting performed by each sex, finding additive genetic variance in male propensities only (Nichols et al 2021). Laboratory studies of cooperatively breeding cichlids (N. pulcher) have also used careful breeding designs, standardized environments, and controlled behavioral tests to separate genetic from nongenetic sources of (co)variation in helping and other social behaviors, finding that helping behavior is partly heritable in this speciesalthough differences among individuals are driven primarily by non-genetic factors, including maternal effects and effects of the 'permanent environment' of individuals rather than by additive genetic effects (Kasper et al 2017a(Kasper et al , 2019.…”

“…Laboratory studies of cooperatively breeding cichlids ( N. pulcher ) have also used careful breeding designs, standardized environments, and controlled behavioral tests to separate genetic from nongenetic sources of (co)variation in helping and other social behaviors, finding that helping behavior is partly heritable in this species—although differences among individuals are driven primarily by non‐genetic factors, including maternal effects and effects of the ‘permanent environment’ of individuals rather than by additive genetic effects (Kasper et al. 2017a, 2019).…”

A positive feedback loop between sociality and social competence

“…For instance, there was moderate to low heritability for aggression in western bluebirds (Sialia mexicana, Duckworth & Kruuk, 2009), greylag geese (Anser anser, Weiss & Foerster, 2013) and spiders (Nuctenea umbratica, Kralj-Fiser et al, 2019), and very weak, but significant, heritability for aggression in crickets (Santostefano et al, 2017). In contrast, there was no evidence for any genetic heritability in four aggressive behaviours and in submissive behaviour in N. pulcher (Kasper et al, 2017b(Kasper et al, , 2019.…”

“…Quantitative genetics studies did not only show that behaviours are genetically heritable to a quite varying degree, but they also identified non-genetic variance components explaining social behaviour, including non-genetic parental effects. For instance, a weak but significant effect of maternal identity on affiliative behaviour was shown in N. pulcher (Kasper et al, 2019). Through parental effects, social behaviour tendencies in parents, such as the quality of parental care behaviour, may be transmitted to offspring (e.g.…”

“…For instance, a weak but significant effect of maternal identity on affiliative behaviour was shown in N . pulcher (Kasper et al, 2019). Through parental effects, social behaviour tendencies in parents, such as the quality of parental care behaviour, may be transmitted to offspring (e.g.…”