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

Abstract

The evolution of cooperative behavior is a major area of research among evolutionary biologists and behavioral ecologists, yet there are few estimates of its heritability or its evolutionary potential, and long-term studies of identifiable individuals are required to disentangle genetic and nongenetic components of cooperative behavior. Here, we use long-term data on over 1800 individually recognizable wild meerkats (Suricata suricatta) collected over 30 years and a multigenerational genetic pedigree to partition phenotypic variation in three cooperative behaviors (babysitting, pup feeding, and sentinel behavior) into individual, additive genetic, and other sources, and to assess their repeatability and heritability. In addition to strong effects of sex, age, and dominance status, we found significant repeatability in individual contributions to all three types of cooperative behavior both within and across breeding seasons. Like most other studies of the heritability of social behavior, we found that the heritability of cooperative behavior was low. However, our analysis suggests that a substantial component of the repeatable individual differences in cooperative behavior that we observed was a consequence of additive genetic variation. Our results consequently indicate that cooperative behavior can respond to selection, and suggest scope for further exploration of the genetic basis of social behavior.

Genetic variance and indirect genetic effects for affiliative social behavior in a wild primate

“…The highest heritability we detected was 0.26 for total grooming, consistent with heritability estimates reported for life history and behavioral traits in wild populations, but lower than generally reported for morphological traits (Visscher et al 2008, Houslay et al 2021). This value may indicate that the quantitative genetics of grooming is more like that of life history traits than morphological traits, and that selection has effectively reduced genetic variation for grooming behavior, resulting in a relatively small numerator (V A ) in the calculation of heritability.…”

“…However, in wild, non-human vertebrate populations, few studies have directly investigated the heritability of affiliative social behaviors (but see Blomquist and Brent, 2014). Instead, studies to date have focused on social network metrics (e.g., Fowler et al 2009; Lea et al 2010; Brent et al 2012) or cooperative behaviors (e.g., Bleakley and Brodie 2009, Kasper et al 2017, Houslay et al 2021). Measurable heritability values for both types of traits suggest possible pathways through which social integration could affect fitness (e.g., cooperation can emerge from social bonds: Berghänel et al 2011).…”

Early life adversity and adult social relationships have independent effects on survival in a wild animal model of aging

“…Our results suggest that adult social behaviors that maintain social bonds should be under strong selection. Further, because social behavior is almost always partially heritable (e.g., (62)(63)(64), these behaviors have the potential to evolve via natural selection. Further, they suggest that indirect genetic effects, in which the genotypes of social partners affect behavior, could play an important role in social selection and evolution (65,66).…”

Genetic, maternal, and environmental influences on sociality in a pedigreed primate population

“…The relative contributions of additive genetic and maternal effects to individual repeatability in behavior have been a topic of much research (Moore et al 2019 )—maternal effects in particular because they can bias estimates of heritability when not adequately controlled for (Rausher 1992 ), and because they can influence evolutionary responses to selection on traits (Mousseau and Fox 1998 ; Räsänen and Kruuk 2007 ). Recent reviews and meta-analyses of animal models show that narrow-sense heritability tends to be low for behavioral traits (at least in comparison to morphological traits) (95% confidence range: 0.092–0.232 (Moore et al 2019 ); 95% credible interval: 0.200, 0.271 (Dochtermann et al 2019 )), particularly for social behavior in wild populations (95% credible interval: 0.029, 0.204 (Houslay et al 2021 )). Estimates for maternal effects are even lower (95% confidence range: 0.030–0.098) (Moore et al 2019 ).…”

“…Studies addressing long-term repeatability of social behavior in wild or free-ranging vertebrates across the lifespan are rare (e.g., Aplin et al 2015 ; Menz et al 2017 ; Houslay et al 2021 ; Evans et al 2021 Strickland et al 2021 ), including studies on long-lived primates (Brent et al 2017 ; Tkaczynski et al 2020 ; Thompson González et al 2021 ). In a longitudinal study on free-ranging rhesus macaques, Brent and colleagues ( 2017 ) used repeat sampling spanning up to 6 years on individuals to look at repeatability in multiple social network-derived measures of social isolation.…”