Abstract
Within socially monogamous breeding systems, levels of extra-pair paternity can vary not only between species, populations, and individuals, but also across time. Uncovering how different extrinsic conditions (ecological, demographic, and social) influence this behavior will help shed light on the factors driving its evolution. Here, we simultaneously address multiple socio-ecological conditions potentially influencing female infidelity in a natural population of the cooperatively breeding Seychelles warbler, Acrocephalus sechellensis. Our contained study population has been monitored for more than 25 years, enabling us to capture variation in socio-ecological conditions between individuals and across time and to accurately assign parentage. We test hypotheses predicting the influence of territory quality, breeding density and synchrony, group size and composition (number and sex of subordinates), and inbreeding avoidance on female infidelity. We find that a larger group size promotes the likelihood of extra-pair paternity in offspring from both dominant and subordinate females, but this paternity is almost always gained by dominant males from outside the group (not by subordinate males within the group). Higher relatedness between a mother and the dominant male in her group also results in more extra-pair paternity—but only for subordinate females—and this does not prevent inbreeding occurring in this population. Our findings highlight the role of social conditions favoring infidelity and contribute toward understanding the evolution of this enigmatic behavior.
Highlights
The occurrence of extra-pair paternity (EPP: genetic promiscuity) within socially monogamous breeding systems is widespread, but its evolution remains enigmatic, despite decades of research (Griffith et al 2002; Forstmeier et al 2014; Taylor et al 2014)
There was a tendency for subordinate mothers to have a higher proportion of offspring with extra-group paternity (EGP), 51% (53/104), than dominant mothers, 40% (341/861), but this did not reach statistical significance (GLMM: βMother status = 0.46 ± 0.26, P = 0.07; Supplementary Table S2)
The genetic relatedness (R) between a female and the dominant male in her territory did not differ with respect to female status (LM: βMother status = 0.02 ± 0.03, P = 0.64)
Summary
The occurrence of extra-pair paternity (EPP: genetic promiscuity) within socially monogamous breeding systems is widespread (birds: e.g., Richardson and Burke 1999; Foerster et al 2003; mammals: e.g., Schulke et al 2004; Kitchen et al 2006; Munshi-South 2007; fish: e.g., Lee-Jenkins et al 2015; Lee et al 2016; Bose et al 2018; reptiles: e.g., Bull et al 1998; While et al 2009; insects: e.g., Dillard 2017), but its evolution remains enigmatic, despite decades of research (Griffith et al 2002; Forstmeier et al 2014; Taylor et al 2014). Levels of EPP are highly variable, between different individuals, populations, and species, and across time (Petrie and Kempenaers 1998; Griffith 2000; Dietrich et al 2004; Schroeder et al 2016). This variation may be partly responsible for the ongoing lack of clarity surrounding the evolution of this phenomenon.
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