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The evolution of monogamy in response to partner scarcity.

ABSTRACT: The evolution of monogamy and paternal care in humans is often argued to have resulted from the needs of our expensive offspring. Recent research challenges this claim, however, contending that promiscuous male competitors and the risk of cuckoldry limit the scope for the evolution of male investment. So how did monogamy first evolve? Links between mating strategies and partner availability may offer resolution. While studies of sex roles commonly assume that optimal mating rates for males are higher, fitness payoffs to monogamy and the maintenance of a single partner can be greater when partners are rare. Thus, partner availability is increasingly recognized as a key variable structuring mating behavior. To apply these recent insights to human evolution, we model three male strategies - multiple mating, mate guarding and paternal care - in response to partner availability. Under assumed ancestral human conditions, we find that male mate guarding, rather than paternal care, drives the evolution of monogamy, as it secures a partner and ensures paternity certainty in the face of more promiscuous competitors. Accordingly, we argue that while paternal investment may be common across human societies, current patterns should not be confused with the reason pairing first evolved.

SUBMITTER: Schacht R

PROVIDER: S-EPMC5013280 | biostudies-literature | 2016 Sep

REPOSITORIES: biostudies-literature

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The evolution of monogamy in response to partner scarcity.

Schacht Ryan R Bell Adrian V AV

Scientific reports 20160907

The evolution of monogamy and paternal care in humans is often argued to have resulted from the needs of our expensive offspring. Recent research challenges this claim, however, contending that promiscuous male competitors and the risk of cuckoldry limit the scope for the evolution of male investment. So how did monogamy first evolve? Links between mating strategies and partner availability may offer resolution. While studies of sex roles commonly assume that optimal mating rates for males are h ...[more]

PMID: 27600189

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Project description:Small populations are susceptible to high genetic loads and random fluctuations in birth and death rates. While these selective forces can adversely affect their viability, small populations persist across taxa. Here, we investigate the resilience of small groups to demographic uncertainty, and specifically to fluctuations in adult sex ratio (ASR), partner availability and dispersal patterns. Using 25 years of demographic data for two Savannah Pumé groups of South American hunter-gatherers, we show that in small human populations: (i) ASRs fluctuate substantially from year to year, but do not consistently trend in a sex-biased direction; (ii) the primary driver of local variation in partner availability is stochasticity in the sex ratio at maturity; and (iii) dispersal outside of the group is an important behavioural means to mediate locally constrained mating options. To then simulate conditions under which dispersal outside of the local group may have evolved, we develop two mathematical models. Model results predict that if the ASR is biased, the globally rarer sex should disperse. The model's utility is then evaluated by applying our empirical data to this central prediction. The results are consistent with the observed hunter-gatherer pattern of variation in the sex that disperses. Together, these findings offer an alternative explanation to resource provisioning for the evolution of traits central to human sociality (e.g. flexible dispersal, bilocal post-marital residence and cooperation across local groups). We argue that in small populations, looking outside of one's local group is necessary to find a mate and that, motivated by ASR imbalance, the alliances formed to facilitate the movement of partners are an important foundation for the human-typical pattern of network formation across local groups.This article is part of the themed issue 'Adult sex ratios and reproductive decisions: a critical re-examination of sex differences in human and animal societies'.

Project description: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.

Project description:The neurohypophysial hormone arginine vasopressin (AVP) plays important roles in fluid regulation and vascular resistance. Differences in AVP receptor expression, particularly mediated through variation in the noncoding promoter region of the primary receptor for AVP (AVPR1a), may play a role in social phenotypes, particularly social monogamy, in rodents and humans. Among primates, social monogamy is rare, but is common among New World monkeys (NWM). AVP is a nonapeptide and generally conserved among eutherian mammals, although a recent paper demonstrated that some NWM species possess a novel form of the related neuropeptide hormone, oxytocin. We therefore characterized variation in the AVP and AVPR1a genes in 22 species representing every genus in the three major platyrrhine families (Cebidae, Atelidae and Pitheciidae). For AVP, a total of 16 synonymous substitutions were detected in 15 NWM species. No non-synonymous substitutions were noted, hence, AVP is conserved in NWM. By contrast, relative to the human AVPR1a, 66 predicted amino acids (AA) substitutions were identified in NWM. The AVPR1a N-terminus (ligand binding domain), third intracellular (G-protein binding domain), and C-terminus were variable among species. Complex evolution of AVPR1a is also apparent in NWM. A molecular phylogenetic tree inferred from AVPR1a coding sequences revealed some consensus taxonomic separation by families, but also a mixed group composed of genera from all three families. The overall dN/dS ratio of AVPR1a was 0.11, but signals of positive selection in distinct AVPR1a regions were observed, including the N-terminus, in which we identified six potential positive selection sites. AA substitutions at positions 241, 319, 399 and 409 occurred uniquely in marmosets and tamarins. Our results enhance the appreciation of genetic diversity in the mammalian AVP/AVPR1a system, and set the stage for molecular modeling of the neurohypophyseal hormones and social behavior in primates.

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The evolution of monogamy in response to partner scarcity.

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The evolution of monogamy in response to partner scarcity.

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