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

Abstract

BackgroundPhylogenetic analyses strongly associate nonsocial ancestors of cooperatively-breeding or eusocial species with monogamy. Because monogamy creates high-relatedness family groups, kin selection has been concluded to drive the evolution of cooperative breeding (i.e., the monogamy hypothesis). Although kin selection is criticized as inappropriate for modeling and predicting the evolution of cooperation, there are no examples where specific inclusive fitness-based predictions are intrinsically wrong. The monogamy hypothesis may be the first case of such a flawed calculation.ResultsA simulation model mutated helping alleles into non-cooperative populations where females mated either once or multiply. Although multiple mating produces sibling broods of lower relatedness, it also increases the likelihood that one offspring will adopt a helper role. Examining this tradeoff showed that under a wide range of conditions polygamy, rather than monogamy, allowed helping to spread more rapidly through populations. Further simulations with mating strategies as heritable traits confirmed that multiple-mating is selectively advantageous. Although cooperation evolves similarly regardless of whether dependent young are close or more distant kin, it does not evolve if they are unrelated.ConclusionsThe solitary ancestral species to cooperative breeders may have been predominantly monogamous, but it cannot be concluded that monogamy is a predisposing state for the evolution of helping behavior. Monogamy may simply be coincidental to other more important life history characteristics such as nest defense or sequential provisioning of offspring. The differing predictive outcome from a gene-based model also supports arguments that inclusive fitness formulations poorly model some evolutionary questions. Nevertheless, cooperation only evolves when benefits are provided for kin: helping alleles did not increase in frequency in the absence of potential gains in indirect fitness. The key question, therefore, is not whether kin selection occurs, but how best to elucidate the differing evolutionary advantages of genetic relatedness versus genetic diversity.

Monogamy and haplodiploidy act in synergy to promote the evolution of eusociality

“…A negative relationship between promiscuity and the evolution of cooperative breeding in birds 8 likewise supports a role of monogamy in favouring the evolution of helping behaviour, although no birds are classified as eusocial. The present work strengthens the theoretical foundation of these empirical results, which has recently been questioned based on an individualbased simulation model that has compared invasion speed of a social allele under monandry versus biandry, instead of comparing the parameter space where evolution of sociality is predicted or not 17 . …”

“…Given the recent debate about the merits of kin selection 10,[15][16][17][18][19][20][21] , it is worth emphasizing that models that are not explicitly phrased in terms of 'inclusive fitness' , including ours, nevertheless allow kin selection to operate. Social interactions between relatives have a crucial role for the total selection experienced by an allele.…”

Kinship, greenbeards, and runaway social selection in the evolution of social insect cooperation

“…Controversies about kin selection often concern the best methods to model the effects of genetic relatedness (4)(5)(6)(7)(8)(9). This tends to obscure the more salient point of how important the level of relatedness is for favoring cooperation (15). The dynamics of social groups can be dominated by either their genetic relatedness or their genetic diversity, because both bring evolutionarily selective advantages.…”

“…The second example is the "monogamy hypothesis," where cooperative breeding is predicted to be more likely to evolve in species where family groups are full siblings because of monog-amy (14). However, a gene-based model for the evolution of cooperation found that helping actually often tended to spread more rapidly through populations with polygamy (15). This may be an instance where the underlying kin selection model actually produces erroneous predictions [as postulated by Nowak et al (4)].…”

An adaptive view of caste differentiation in the neotropical wasp Polybia (Trichothorax) sericea Olivier (Hymenoptera: Vespidae)

“…An opposite situation occurs when levels of polygyny are low and queens are closely related (Hamilton 1972, Queller et al 1993, Strassmann et al 1998, Nascimento et al 2004. Additionally, a recent study showed through gene-based simulations, that cooperative behavior would be favored by multiple matings (Nonacs 2011). This enigmatic scenario involving the Epiponini draws sociobiologists' attention to the real social status of this group (for further discussion see Bourke 1999 andWenzel 2008).…”