Beyond promiscuity: mate-choice commitments in social breeding

Abstract

Obligate eusociality with distinct caste phenotypes has evolved from strictly monogamous sub-social ancestors in ants, some bees, some wasps and some termites. This implies that no lineage reached the most advanced form of social breeding, unless helpers at the nest gained indirect fitness values via siblings that were identical to direct fitness via offspring. The complete lack of re-mating promiscuity equalizes sex-specific variances in reproductive success. Later, evolutionary developments towards multiple queen-mating retained lifetime commitment between sexual partners, but reduced male variance in reproductive success relative to female's, similar to the most advanced vertebrate cooperative breeders. Here, I (i) discuss some of the unique and highly peculiar mating system adaptations of eusocial insects; (ii) address ambiguities that remained after earlier reviews and extend the monogamy logic to the evolution of soldier castes; (iii) evaluate the evidence for indirect fitness benefits driving the dynamics of (in)vertebrate cooperative breeding, while emphasizing the fundamental differences between obligate eusociality and cooperative breeding; (iv) infer that lifetime commitment is a major driver towards higher levels of organization in bodies, colonies and mutualisms. I argue that evolutionary informative definitions of social systems that separate direct and indirect fitness benefits facilitate transparency when testing inclusive fitness theory.

Leucoagaricus gongylophorus uses leaf-cutting ants to vector proteolytic enzymes towards new plant substrate

“…Such interactions normally show only minor remnants of the potential reproductive conflicts that needed to be overcome when these partnerships evolved, allowing them to ultimately become single adaptive units with organismal properties (Queller and Strassmann, 2009;Boomsma, 2013). Such high levels of interdependency are most characteristic for endosymbioses where the symbiont lives in cells or tissues of the host, but may also occur in ectosymbioses like the eusocial fungus-farming mutualisms of ants and termites where the fungus gardens are ectosymbionts for the individual ants but endosymbionts for the colony (Poulsen and Boomsma, 2005;Aanen et al, 2009).…”

Sexual Conflict Arising from Extrapair Matings in Birds

“…Selection experiments with Drosophila support this theory-selection lines with experimentally imposed lifetime monogamy showed dramatic reductions in measures of sexual conflict relative to lines with the normal polyandrous pattern of mating (Holland and Rice 1999). Theory and comparative studies also suggest that lifetime sexual monogamy is crucial for the evolution of some strong forms of altruism, such as the helping behavior observed in social insects and some birds (Hughes et al 2008;Cornwallis et al 2010;Boomsma 2013).…”

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

“…Being in the light-grey triangle makes the pursuit of indirect fitness more favourable than direct fitness and the opposite is true when being in the white triangle. Obligatorily eusocial Hymenoptera (ants, corbiculate bees, vespine wasps) have strict lifetime monogamous ancestors [13,18] so that r n /r o equalled one when workers became physically differentiated (the black triangle in the top-left), but this condition is not fulfilled in cooperative and facultatively eusocial breeders where individuals may change roles from helper to breeder later in life. In terms of lifetime inclusive fitness, individuals in such populations will always hover around the diagonal as helping never becomes fixed in the obligatorily eusocial sense.…”

“…Eusociality therefore entails a transition from reproductive skew among cooperative and facultatively eusocial breeders to sterility for most colony members. Such a transition to obligate eusociality is irreversible and this is significant when evaluating the likelihood of nepotism on either side of the transition [13]. Increasing unmatedness implies that selection for matechoice targets a decreasing proportion of individuals as reproductive division of labour increases.…”