Lifetime monogamy and the evolution of eusociality

Abstract

All evidence currently available indicates that obligatory sterile eusocial castes only arose via the association of lifetime monogamous parents and offspring. This is consistent with Hamilton's rule (br s . r o c), but implies that relatedness cancels out of the equation because average relatedness to siblings (r s ) and offspring (r o ) are both predictably 0.5. This equality implies that any infinitesimally small benefit of helping at the maternal nest (b), relative to the cost in personal reproduction (c) that persists throughout the lifespan of entire cohorts of helpers suffices to establish permanent eusociality, so that group benefits can increase gradually during, but mostly after the transition. The monogamy window can be conceptualized as a singularity comparable with the single zygote commitment of gametes in eukaryotes. The increase of colony size in ants, bees, wasps and termites is thus analogous to the evolution of multicellularity. Focusing on lifetime monogamy as a universal precondition for the evolution of obligate eusociality simplifies the theory and may help to resolve controversies about levels of selection and targets of adaptation. The monogamy window underlines that cooperative breeding and eusociality are different domains of social evolution, characterized by different sectors of parameter space for Hamilton's rule.

A halictid bee with sympatric solitary and eusocial nests offers evidence for Hamilton's rule

“…The F0 females of halictid bees maintain their nests without helpers during the first reproductive period 12,13,16,19 . It has been suggested that the lack of lifetime monogamy may prevent the halictid bees from lifetime eusociality 26 . A fraction of F0 females mated twice.…”

Nice to kin and nasty to non-kin: revisiting Hamilton's early insights on eusociality

“…It now seems more likely that there is a gradient of nepotism, which is negatively correlated with reproductive division of labour, so that nepotism is most easily maintained in advanced primate (including human) groups, less so but still frequent in other vertebrate societies [4,10], but absent in the more organismal [27] insect societies. When high levels of organismality are reached [13,27,28], nepotism likely becomes an aberration rather than a kinselected norm, analogous to cancer in metazoan bodies [29].…”

Recruitment-dance signals draw larger audiences when honey bee colonies have multiple patrilines

“…That extreme polyandry is so pervasive in Apis suggests that it is favoured strongly by selection once workers are locked into a non-reproductive role (Boomsma, 2009;Brown, 2003;Crozier and Fjerdingstad, 2001;Crozier and Page, 1985;Hughes et al, 2008a, b;Oldroyd and Fewell, 2008). Indeed, a growing body of evidence shows that honey bee colonies reap numerous fitness benefits from the genetic diversity that is introduced into their population by the polyandrous behaviour of their queens.…”