Reproductive concessions between related and unrelated members promote eusociality in bees

Abstract

Animal societies exhibit remarkable variation in their breeding strategies. Individuals can maximize their fitness by either reproducing or by helping relatives. Social hymenopterans have been key taxa for the study of Hamilton’s inclusive fitness theory because the haplodiploid sex-determination system results in asymmetric relatedness among breeders producing conflict over the partitioning of reproduction. In small cooperative groups of insects, totipotent individuals may maximize their inclusive fitness by controlling reproduction despotically rather than helping their relatives. Here, we demonstrate that the dominant females of the primitively eusocial bee Euglossa melanotricha (Apidae: Euglossini) control reproduction, but concede part of the reproductive output with their related and unrelated subordinates. As expected, a dominant female capitalizes on the direct reproduction of related subordinates, according to her interests. We found that reproductive skew was positively correlated with relatedness. The concessions were highly reduced in mother-daughter and sibling nests (relatedness r ± s.d. = 0.54 ± 0.02 and 0.79 ± 0.02, respectively) but much more egalitarian in unrelated associations ( r = −0.10 ± 0.01). We concluded that reproductive skew in these primitively eusocial bees is strongly related to the genetic structure of associations, and also that females are able to assess pairwise relatedness, either directly or indirectly, and use this information to mediate social contracts.