Age- and sex-dependent variation in relatedness corresponds to reproductive skew, territory inheritance, and workload in cooperatively breeding cichlids.

Dario Josi,Michael Taborsky,Joachim G Frommen,Masanori Kohda,Dmitry A Konovalov,Tomohiro Takeyama,Danielle Bonfils,Dik Heg

doi:10.1111/evo.14348

Abstract

Kin selection plays a major role in the evolution of cooperative systems. However, many social species exhibit complex within‐group relatedness structures, where kin selection alone cannot explain the occurrence of cooperative behavior. Understanding such social structures is crucial to elucidate the evolution and maintenance of multi‐layered cooperative societies. In lamprologine cichlids, intragroup relatedness seems to correlate positively with reproductive skew, suggesting that in this clade dominants tend to provide reproductive concessions to unrelated subordinates to secure their participation in brood care. We investigate how patterns of within‐group relatedness covary with direct and indirect fitness benefits of cooperation in a highly social vertebrate, the cooperatively breeding, polygynous lamprologine cichlid Neolamprologus savoryi. Behavioral and genetic data from 43 groups containing 578 individuals show that groups are socially and genetically structured into subgroups. About 17% of group members were unrelated immigrants, and average relatedness between breeders and brood care helpers declined with helper age due to group membership dynamics. Hence the relative importance of direct and indirect fitness benefits of cooperation depends on helper age. Our findings highlight how both direct and indirect fitness benefits of cooperation and group membership can select for cooperative behavior in societies comprising complex social and relatedness structures.

Highlights

These helpers will not gain indirect fitness benefits but are assumed to acquire direct benefits instead, for example, through increased tolerance by dominant individuals allowing them to remain in the group (“pay-to-stay”, Gaston 1978; Kokko et al 2002; Bergmüller and Taborsky 2005; Fischer et al 2014; Kingma 2017; Naef and Taborsky 2020a,b), which reflects an exchange of different commodities (Quiñones et al 2016; Taborsky 2016)
Large helpers of N. pulcher are often unrelated to the breeders they aid (Dierkes et al 2005; Stiver et al 2005), whereas helpers of Neolamprologus obscurus are typically closely related to the breeders they assist (Tanaka et al 2015)
Cooperative behavior of subordinates in N. obscurus is probably to a larger extent driven by kin selection (Tanaka et al 2015)

Summary

Introduction

Cooperative breeding, where individuals other than breeders provide alloparental care, evolved across many different animal taxa, including insects (Boomsma 2009; Biedermann and Taborsky 2011), crustaceans (Hultgren and Duffy 2012), fishes (Heg and Bachar 2006; Taborsky 2016; Tanaka et al 2018b), birds (Koenig and Dickinson 2016), and mammals (Solomon and French 1997; Clutton-Brock 2016). Cooperative behavior of subordinates in N. obscurus is probably to a larger extent driven by kin selection (Tanaka et al 2015) This striking divergence of selection mechanisms responsible for apparently altruistic alloparental care among closely related species sharing a common ecology provides unique opportunities to elucidate the significance of relatedness and group structure for the evolution of cooperative behavior in animals. This enables the collection of large sample sizes on social structure, relatedness patterns, and behavior within manageable time

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Conclusion