Genetic relatedness in social groups of the emerald coral goby Paragobiodon xanthosoma creates potential for weak kin selection

Abstract

Animals forming social groups that include breeders and nonbreeders present evolutionary paradoxes; why do breeders tolerate nonbreeders? And why do nonbreeders tolerate their situation? Both paradoxes are often explained with kin selection. Kin selection is, however, assumed to play little or no role in social group formation of marine organisms with dispersive larval phases. Yet, in some marine organisms, recent evidence suggests small‐scale patterns of relatedness, meaning that this assumption must always be tested. Here, we investigated the genetic relatedness of social groups of the emerald coral goby, Paragobiodon xanthosoma. We genotyped 73 individuals from 16 groups in Kimbe Bay, Papua New Guinea, at 20 microsatellite loci and estimated pairwise relatedness among all individuals. We found that estimated pairwise relatedness among individuals within groups was significantly higher than the pairwise relatedness among individuals from the same reef, and pairwise relatedness among individuals from the same reef was significantly higher than the pairwise relatedness among individuals from different reefs. This spatial signature suggests that there may be very limited dispersal in this species. The slightly positive relatedness within groups creates the potential for weak kin selection, which may help to resolve the paradox of why breeders tolerate subordinates in P. xanthosoma. The other paradox, why nonbreeders tolerate their situation, is better explained by alternative hypotheses such as territory inheritance, and ecological and social constraints. We show that even in marine animals with dispersive larval phases, kin selection needs to be considered to explain the evolution of complex social groups.

Optimization of an amplicon sequencing‐based microsatellite panel and protocol for stock identification and kinship inference of lake trout (Salvelinus namaycush)

“…We demultiplexed loci and called individual genotypes using a python script (amplicon.py, https://bitbu cket.org/corne ll_bioin forma tics/ampli con/src/maste r/) that has been employed for other microsatellite genotyping projects (Rueger et al, 2021) In brief, the script separates paired reads by locus using Cutadapt (Martin, 2011) and then merges each pair using BBMerge (Bushnell et al, 2017). Identical reads are then counted and collapsed, with the ratio of resulting counts used to call haplotypes for each locus and individual.…”

“…We demultiplexed loci and called individual genotypes using a python script (amplicon.py, https://bitbucket.org/cornell_bioinformatics/amplicon/src/master/ ) that has been employed for other microsatellite genotyping projects (Rueger et al, 2021 ) and itself represents a refinement of the earlier Perl script used by similar studies (D'Aloia et al, 2013 ; Karn et al, 2021 ; Marcy‐Quay et al, 2020 ). In brief, the script separates paired reads by locus using Cutadapt (Martin, 2011 ) and then merges each pair using BBMerge (Bushnell et al, 2017 ).…”

Evolution, Development and Ecology of Anemonefishes

“…That study suggested that non-breeders were not closely related to the breeders ). However, more recent evidence suggests that non-breeders can sometimes be related to the breeders in A. percula (e.g., rare occurrences of full-sibs, uncles/aunts, nieces/nephews; , creating the potential for weak kin selection that might favour breeders tolerating rather than evicting non-breeders as seen in other reef fishes (Rueger et al , 2021b. This weak kin selection hypothesis is yet to be rigorously tested in A. percula or any other anemonefish, but dominants might accrue a 1-2% increase in relative fitness (rY i > rY j , Inequality 14.2) tipping the balance in favour of tolerating rather than evicting subordinates.…”

Larval ecology, dispersal, and the evolution of sociality in the sea

“…Thus, although the predominance of a larval stage in marine species is often seen as a barrier to the evolution of cooperative group living driven by kin selection, it might actually be an advantage in the evolution of peaceful cooperation. Furthermore, recent evidence suggests that low but positive relatedness might have a small role in explaining peaceful cooperation in P. xanthosomus (Rueger et al, 2021), which highlights the importance of measuring genetic relatedness in marine social groups for betting understanding their grouping benefits. Ultimately, the dual benefit framework may prove useful for not only testing the grouping benefits hypotheses in the few social marine species studied thus far, but also predicting which types of species might form social groups and therefore warrant further study.…”

“…Although the evolution of sociality with indiscriminate altruism is more likely in species that have completely lost a planktonic larval phase (e.g., Synalpheus shrimps), targeted cooperative behavior could still evolve partly by kin selection in species that show low within‐group relatedness, but that can recognize, associate, and interact frequently with relatives (Buston et al, 2009). For example, in the emerald coral goby Paragobiodon xanthosoma , low but positive relatedness within groups has been suggested to explain why breeders tolerate subordinates (Rueger et al, 2021), while a combination of future selection and ecological/social constraints may explain why nonbreeders wait peacefully in a queue for breeding positions (Wong et al, 2007; Wong, 2010).…”