Haplodiploidy, eusociality and absence of male parental and alloparental care in Hymenoptera: a unifying genetic hypothesis distinct from kin selection theory

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Beginning with Hamilton ( J. theor. Biol. 7, 1-52 (1964)), evolutionary biologists have attempted to explain the apparent predisposition for the haplodiploid Hymenoptera to evolve both eusociality and female workers. As an alternative to kin selective, pre-adaptational, or ecological explanations for this association, I propose a new genetic hypothesis, the protected invasion hypothesis : dominant alleles for maternal care in finite haplodiploid populations are more resistant to loss from genetic drift than are paternal-care alleles in haplodiploid populations or than are either maternal or paternal-care alleles in diploid populations. Similarly, dominant alleles for female alloparental care in finite haplodiploid populations are more resistant to loss from genetic drift than are male alloparental alleles in haplodiploid populations or than are (male or female) alloparental alleles in diploid populations. A Markov model of phenotypic evolution describing the step-wise progress of a population toward one of two adaptive peaks demonstrates that even small differences in fixation probabilities among these alleles can translate into large differences in the long-run probabilities of observing the corresponding parental or alloparental strategies. Thus the protected invasion hypothesis immediately explains all of the peculiar social features of the haplodiploid Hymenoptera, namely: (i) the overwhelmingly greater tendency for maternal care than paternal care in Hymenoptera; (ii) the greater propensity for eusociality (alloparental sibling care) in Hymenoptera than in diploid insects; and (iii) the greater likelihood for females than males to become alloparents (workers) in the Hymenoptera. The hypothesis also correctly predicts (iv) the apparently higher frequency of paternal care in diploid species than in haplodiploid species, and (v) the lack of a sex-bias among workers of eusocial diploid species. The protected invasion hypothesis is distinct from relatedness-based explanations and provides a more comprehensive explanation for the repeated appearance of the distinctive social structures of the Hymenoptera than does the kin selection model. I show that the bias toward eusociality in Hymenoptera is produced by protected invasion effects even when there is no female-biased sex ratio and no asymmetry between a female’s relatedness to its siblings and to its own offspring. In addition, protected invasion effects create a bias for female versus male workers within the Hymenoptera even when there is no asymmetry between a female’s and male’s relatedness to its siblings. Furthermore, protected invasion effects create a bias toward eusociality in haplodiploid versus diploid populations even when the queen mates an indefinite number of times and there is no difference between haplodiploid and diploid colonies in the relatednesses of workers to their tended brood. Finally, the protected invasion hypothesis explains a phenomenon that cannot be explained by kin selection theory: the surprising overwhelming preponderance of maternal over paternal care in the Hymenoptera (because male and female parents have the same mean relatedness to their offspring when the female mates singly). An important implication of the protected invasion hypothesis is that synergistic co-operation among siblings is more likely to evolve in haplodiploid than in diploid species.