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Open Access Highly Accessed Research article

Monogamy and high relatedness do not preferentially favor the evolution of cooperation

Peter Nonacs

BMC Evolutionary Biology 2011, 11:58  doi:10.1186/1471-2148-11-58

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Resolving differences with Fromhage & Kokko model.

Peter Nonacs   (2011-08-19 12:06)  University of California Los Angeles email

Recently Fromhage and Kokko (FK: 2011, Nature Communications 2:397) modeled the same issue as the Nonacs (N) paper. The two papers differ with FK finding cooperation becomes more likely with monogamy and haplodiploidy, which is the opposite to the outcomes reported here. Nevertheless, there are several similarities across the two papers. Helping evolves only if the cost of allelic ‘free-riders’ can be overcome. As shown in both papers, alleles for helping behavior are at higher frequencies in helpers than in those being helped with certain mating combinations. This assortment cost creates within-group selection favoring non-helping alleles. Monogamy and haplodiploidy minimize such costs, hence producing the FK outcomes. In the N outcomes, this assortment cost creates limited sets of conditions where cooperation evolves only with monogamy.

It is worth noting that allele assortment differs substantially from the original basis of the ‘monogamy hypothesis’ which emphasized the two-fold difference in relatedness between helping full or half sibs (references #13 & 14 in N). This is easily seen in the FK model by making one mathematical change: I.e., when an individual becomes a helper, an identical clone is added to the disperser pool. Although biologically impossible, this change nullifies all assortment costs and allows a direct examination of whether eusociality evolves more readily if only full sibs are aided. When I numerically simulated with this change and using HK model parameters, I found that neither monogamy nor haplodiploidy creates any advantage for evolving cooperation. Therefore, any differential likelihood for evolving eusociality is driven only by allele assortment probabilities.

This emphasizes that the differing outcomes across the two models are due to a difference in assumptions of what happens if helpers survive past their mother’s death. In FK, all surviving helpers become dispersers and therefore have no differential advantage relative to non-helpers that disperse upon maturation. In contrast, surviving helpers inherit the existing nest and have opportunities to continue rearing kin or their own offspring in the N model. They might also recruit their own related helper. This creates a second allele assortment issue as only individuals having helping alleles can inherit nests. This assortment benefit is more likely to accrue with polyandry, and is why under a wide range of conditions monogamy is less conducive for eusocial evolution.

Monogamy or reduced promiscuity is suggested to be the most likely ancestral states for the initial evolution of cooperative breeding in Hymenoptera and birds (15,16). Whether this is strong evidence for the preadaptive benefit of haplodiploidy and monogamy or just evidence for a coincidental happenstance, depends on whether helper dispersal (FK model) or helper inheritance (N model) after the death of parents is the more likely scenario. The abundant evidence in bees, wasps and birds that helpers are likely to remain at natal sites upon the death of dominant reproductives, favors the Nonacs model as the most biologically realistic. If indeed it is, the more robust conclusion must be that neither monogamy nor haplodiploidy have a special relationship for the proffered examples of eusocial evolution.

Competing interests



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