Hamilton's inclusive fitness maintains heritable altruism polymorphism through rb = c

Abstract

How can altruism evolve or be maintained in a selfish world? Hamilton's rule shows that the former process will occur when rb > c-the benefits to the recipients of an altruistic act b, weighted by the relatedness between the social partners r, exceed the costs to the altruists c-drives altruistic genotypes spreading against nonaltruistic ones. From this rule, we infer that altruistic genotypes will persist in a population by forming a stable heritable polymorphism with nonaltruistic genotypes if rb = c makes inclusive fitness of the two morphs equal. We test this prediction using the data of 12 years of study on a cooperatively breeding bird, the Tibetan ground tit Pseudopodoces humilis, where helping is performed by males only and kin-directed. Individual variation in ever acting as a helper was heritable (h² = 0.47), and the resultant altruism polymorphism remained stable as indicated by low-level annual fluctuation of the percentage of helpers among all adult males (24-28%). Helpers' indirect fitness gains from increased lifetime reproductive success of related breeders statistically fully compensated for their lifetime direct fitness losses, suggesting that rb = c holds. While our work provides a fundamental support for Hamilton's idea, it highlights the equivalent inclusive fitness returns to altruists and nonaltruists mediated by rb = c as a theoretically and realistically important mechanism to maintain social polymorphism.

Keywords: Fisher's natural selection theorem; cooperative breeding; kin selection; lifetime fitness; quantitative genetics.

Fig. 1.

A sketch showing the testing system for the equivalent inclusive fitness mechanism mediated by rb = c to maintain altruism polymorphism. (A) Altruism enhances lifetime direct fitness of the recipients, where b is the direct fitness difference between recipients and nonrecipients. (B) The indirect fitness payoffs for altruists rb (where r is the genetic relatedness between altruists and recipients) perfectly compensate c—the lifetime direct fitness losses suffered by altruists relative to nonaltruists.

Fig. 2.

Yearly variation in the percentages of helpers (blue line) among all adult males and of helped nests (gray line) among all nests in the Tibetan ground tit population across the study period.

Fig. 3.

Comparisons of lifetime fitness between individual ground tits to test the prediction that equivalent inclusive fitness mediated by rb = c maintains altruism polymorphism. (A) Lifetime reproductive success of ever-receiving-help (blue columns) vs. never-receiving-help (white columns) breeders. (B) Lifetime direct reproductive success of ever-giving-help (purple columns) vs. never-giving-help (white column) males, and indirect fitness benefits of ever-giving-help males (light blue column). Values are given as mean + SE, with sample sizes above the SE bar.