Inclusive fitness benefits mitigate costs of cuckoldry to socially paired males

Abstract

BackgroundIn socially monogamous species, reproduction is not always confined to paired males and females. Extra-pair males commonly also reproduce with paired females, which is traditionally thought to be costly to the females’ social partners. However, we suggest that when the relatedness between reproducing individuals is considered, cuckolded males can suffer lower fitness losses than otherwise expected, especially when the rate of cuckoldry is high. We combine theoretical modeling with a detailed genetic study on a socially monogamous wild fish, Variabilichromis moorii, which displays biparental care despite exceptionally high rates of extra-pair paternity.ResultsWe measured the relatedness between all parties involved in V. moorii spawning events (i.e. between males and females in social pairs, females and their extra-pair partners, and paired males and their cuckolders), and we reveal that males are on average more related to their cuckolders than expected by chance. Queller–Goodnight estimates of relatedness between males and their cuckolders are on average r = 0.038 but can range up to r = 0.64. This also increases the relatedness between males and the extra-pair offspring under their care. These intriguing results are consistent with the predictions of our mathematical model, which shows that elevated relatedness between paired males and their cuckolders can be adaptive for both parties when competition for fertilizations is strong.ConclusionsOur results show how cuckoldry by relatives can offset males’ direct fitness losses with inclusive fitness gains, which can be substantial in systems where males face almost certain paternity losses.Electronic supplementary materialThe online version of this article (10.1186/s12915-018-0620-6) contains supplementary material, which is available to authorized users.

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

“…Small increases in fitness can be profitable as long as the ecological cost does not become too great and therefore selection could favour evolution of behaviours based on small elevations in relatedness, as long as they are above the population average (West‐Eberhard, 1975). In the cichlid Variabilichromis moori , inclusive fitness benefits conferred by an average relatedness of 0.034 between male breeders and cuckolding males helps to mitigate the cost of cuckoldry (Bose et al, 2019). Even in some mammals performing alloparental care, mean within‐group relatedness was found to be low; the mean relatedness ± SE of females in groups of wild boar, Sus srofa , was 0.08 ± 0.1 (Briga et al, 2012; Poteaux et al, 2009), and in spear‐nosed bats, Phyllostomus hastatus , was only 0.01 ± 0.01 (Briga et al, 2012; McCracken & Bradbury, 1981).…”

Nest defense in the face of cuckoldry: evolutionary rather than facultative adaptation to chronic paternity loss

“…Indeed, in our current study, sire number was strongly correlated with paternity of the paired male (Spearman correlation coefficient r = − 0.834). However, the number of rivals present during a spawning becomes an increasingly unreliable measure as the number of unsuccessful cuckolders in the group increases and becomes more variable [48]. Direct observations of V. moorii spawning events will be valuable for assessing the utility of this paternity cue.…”

“…Solitary individuals and mated pairs of the small (< 10 cm), dark-colored cichlid defend their territories against other members of the species-rich littoral fish community that compete with them for food and space. Additionally, non-territorial V. moorii cruise the rocky littoral, snatch up food and on occasion participate in the spawning of the mated pairs [47, 48]. Spawning females attach their clutches of up to > 100 eggs onto vertical rock surfaces.…”

Freshwater hydrozoan blooms alter activity and behaviour of territorial cichlids in Lake Tanganyika

“…Jellyfish blooms may also affect cuckoldry, which is a common component of many Tanganyikan cichlid mating systems (e.g. [17,43,44]). In general, cuckolder males seek to intrude on mating events and steal fertilizations from spawning males, but if their movement is restricted, they could suffer in terms of missed reproductive opportunities.…”