Sinervo, Chaine, and Miles (2020, The American Naturalist 195:247–274) proposed a genic theory of mammalian mating-system evolution: frequency-dependent competition among three genetically determined alternative strategies — monogamous, polygynous, and sneak — played through payoffs for male competition, neighborhood choice, and paternal care, which predicts transitions among promiscuity, polygyny, and monogamy and higher speciation rates in monogamous rodent lineages, without invoking resource distribution. The authors themselves identified what remains undone. The model cannot regenerate a strategy once a lineage has lost it, yet stochastic character mapping of the rodent phylogeny shows reversals back to promiscuity (5.6% of monogamy transitions, 26% of polygyny transitions); the single additive-locus and allele-sharing-based paternal-care assumptions are untested; and the theory's discriminating empirical predictions — newly evolved genomic imprints in the 23 inferred independent transitions from ancient monogamy back to promiscuity or polygyny (the imprint transition set: 'ancient monogamy' is the source, or ancestral, state at the transition node, so the set is exactly the transitions whose source state is monogamy and whose destination is promiscuity or polygyny; this set shares the monogamy-to-promiscuity reversals with the loss-reversals counted above and additionally contains the monogamy-to-polygyny transitions), and the relative explanatory power of genic versus fine-scale resource-ecological mechanisms — await evaluation.

Background

A mating system is the way mating access is organized in a population — promiscuity (multiple mates for both sexes), polygyny (one male mates with several females), or social monogamy (persistent pair bonds). The dominant framework since the 1970s is resource-defense theory: mating systems follow the spatial and temporal distribution of defendable resources and mates, so mating-system shifts should track ecological change. This framework struggles to explain stable mating systems across contrasting environments and shifts that occur without any ecological change.

Sinervo, Chaine, and Miles (2020) offered an alternative, genic account. They modeled three genetically determined alternative reproductive strategies — monogamous, polygynous, and sneak (the last being non-territorial males that exploit others' pair bonds) — whose carriers compete in a frequency-dependent social game: each strategy's payoff depends on the relative abundance of the others. Such games can show rock–paper–scissors (RPS) intransitivity, where each strategy beats one and loses to another, so no single strategy wins and all are maintained in cyclic equilibrium. 'Genic' selection here means selection acting on alleles with distinguishable effects on social behavior (competition, discrimination of social partners, paternal care), rather than on ecological traits. The payoffs were organized into matrices for male competition, neighborhood choice (discrimination among neighboring territories in proportion to genetic similarity), and paternal care allocated in proportion to the alleles a sire shares with offspring. Iterating the resulting selection equations predicted four evolutionarily stable strategy (ESS) outcomes — stable states that no mutant strategy can invade — promiscuity maintained by RPS cycling (with two or three strategies), fixation of polygyny, and fixation of monogamy.

A comparative test used the rodent phylogeny: mating systems were scored from the literature for 288 taxa with sufficient data (276 of the roughly 2,277 known rodent species sampled, spanning all major clades), and ancestral states and transition counts were inferred by stochastic character mapping, a method that samples plausible histories of discrete-character change along the phylogeny. Promiscuity was recovered as ancestral; monogamy and polygyny arose repeatedly from it and co-occur in sister taxa more often than chance; and state-dependent diversification models (BiSSE/HiSSE — binary and hidden-state state-speciation-and-extinction models, which estimate speciation and extinction rates conditional on a trait, optionally with unmeasured 'hidden' factors) indicated roughly 4.8-fold higher speciation rates in monogamous lineages.

Two gaps motivate the open problem. First, irreversibility: in the model an eliminated strategy can never return, yet the inferred rodent history contains reversals — monogamy to promiscuity (5.6% of monogamy transitions) and polygyny to promiscuity (26% of polygyny transitions) — so the model cannot, even in principle, generate an important class of observed transitions. Second, untested assumptions: the behaviors are driven by a single locus with additive (codominant) effects, and paternal care requires genic recognition of offspring. The paper proposes concrete extensions — reintroduction of lost strategies through mutation or gene flow, other genetic architectures such as phenotypic plasticity (one genotype expressing different strategies), dominance, heterozygote advantage, or multiple linked loci (a supergene: a chromosomal block, often an inversion, that inherits as a unit and holds together several strategy-determining genes), and equal allocation of paternal care regardless of allele sharing — and two discriminating empirical programs: adding fine-scale resource and environmental data to the rodent dataset to compare genic and resource-ecological explanations, and testing a distinctive genic prediction involving genomic imprinting. Genomic imprinting is parent-of-origin-specific epigenetic silencing, so that only the maternal or paternal allele of a gene is expressed; earlier work on muroid rodents found imprinting patterns differing between monogamous and promiscuous sister taxa, and the genic-recognition mechanism of the model predicts that newly evolved imprints should mark the 23 inferred independent transitions from ancient monogamy back to promiscuity or polygyny. A suggestive but unconfirmed corollary links segregating coat-color polymorphism (a possible 'badge' marking alternative strategies, as in the side-blotched lizard RPS system) with promiscuous but never monogamous or polygynous rodents.

Problem Statement

As posed by the source and left unresolved by subsequent literature, the problem is to complete and validate the genic game theory of rodent mating-system evolution, in three parts directed at a reversible, genetically general, and empirically validated theory of mating-system transitions:

  1. Reversibility. Determine how the three-strategy (monogamy, polygyny, sneak) frequency-dependent genic game can account for the empirically inferred reversals, transitions from monogamy back to promiscuity (5.6% of monogamy transitions) and from polygyny back to promiscuity (26% of polygyny transitions), and characterize the conditions — in the payoff structure for male competition, neighborhood choice and paternal care, and in the reintroduction terms — under which the model produces them, distinguishing reversals generated by the frequency-dependent game from reversals imposed by the reintroduction terms alone, and hence whether the model recovers cyclical transitions among mating systems at phylogenetic scale, driven by the intransitive (rock–paper–scissors) competition among strategies.

  2. Genetic and behavioral generality. Determine how the predicted transition structure and stable outcomes change when the single additive (codominant) locus is replaced by each of the following genetic mechanisms — phenotypic plasticity, dominance, heterozygote advantage, and multiple linked loci such as a supergene — and when paternal care, currently allocated in proportion to sire–offspring allele sharing, is instead provided equally to all offspring.

  3. Discriminating tests. Evaluate the relative explanatory power of the genic mechanism versus fine-scale resource ecology, and their interaction, in rodent mating-system evolution, using the rodent mating-system dataset (276 of 2,277 species sampled; 288 taxa in the phylogenetic analysis); test the genic prediction that newly evolved genomic imprints exist in the 23 independent transitions from ancient monogamy back to promiscuity or polygyny inferred by the source's stochastic character mapping of the rodent phylogeny; and examine the suggested association between coat-color polymorphism and alternative strategies in rodents, which the source presents as a suggestive but unconfirmed corollary.

The three parts are each independently refutable strands: resolving any one part settles the question it poses while leaving the other two open. Part 1 supplies the missing dynamics (the current model cannot generate observed reversals even in principle); part 2 establishes whether the model's published predictions are artifacts of its single-locus and allele-sharing-care assumptions; part 3 supplies the empirical discrimination, including the imprint prediction that follows specifically from genic recognition.

References

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