In a landmark study of spotted hyenas (Crocuta crocuta) in Tanzania's Ngorongoro Crater, Höner et al. (2007) showed that male-biased dispersal most probably results from males adaptively responding to simple female mate-choice rules that evolved for inbreeding avoidance: females preferred sires born into or immigrated into their clan after the female's own birth (a time-based rule making male tenure shorter than the female's age), and male dispersers, by settling in clans with the most young females, achieved higher long-term reproductive success than the 11% of males that bred philopatrically. The paper left a five-part research agenda: (1) the generality of female-choice-driven male dispersal across social mammals with different life histories and kin structures; (2) the mechanistic basis and error rates of the time-based female rule; (3) whether unmeasured, context-dependent aspects of alternative drivers (male–male competition, male inbreeding avoidance, resource competition) contribute under other ecological conditions; (4) the long-term population-genetic and adaptive consequences of demography-driven male dispersal; (5) the proximate mechanisms by which prospecting males assess and compare clan demography. The five strands are not equally open: the descriptive population-genetic consequences of demography-driven male dispersal (strand 4) have since been quantified, while the generality, mechanism, alternatives and male-assessment questions remain open or in part contested, and the long-term sufficiency question is explicitly open; the problem as a whole remains unresolved.

Background

Natal dispersal — the permanent movement of an individual from its birth group or site to its breeding group or site — is often biased toward one sex, and in group-living mammals it is usually males that disperse while females remain philopatric (staying in the natal group). Since Greenwood's (1980) synthesis, the classic candidate explanations for male-biased dispersal have been competition among males for mating opportunities, avoidance of inbreeding by the dispersing sex, and competition over resources. A theoretical alternative predates Höner et al. (2007): Lehmann and Perrin (2003) showed by modeling that if females can recognize and reject kin as mates, female mate choice itself creates selection for male dispersal, because nondispersing males lose mating opportunities — inbreeding is then avoided without females having to disperse.

The spotted hyena is the system in which this prediction was convincingly demonstrated. Spotted hyenas live in fission–fusion societies called clans: stable social units of related philopatric females (who dominate males socially) plus immigrant males. Immigrant males join at the bottom of a strict 'queuing' hierarchy and rise in rank only with time in the group (East and Hofer, 2001); a male's tenure is the time elapsed since he joined his current clan. Females mate promiscuously and conception is cryptic, so mate choice must be inferred from genetically assigned paternity. Using microsatellite paternity analysis in the eight clans of the Ngorongoro Crater, Höner et al. (2007) found that (i) females preferred sires that had been born into, or immigrated into, the female's clan after the female was born — i.e., males whose clan tenure was shorter than the female's age — a simple time-based rule that avoids mating with potential fathers and other older kin; (ii) young females preferred short-tenured sires while older females preferred longer-tenured sires; (iii) males responded by initiating their reproductive careers in the clans with the most young females, so that 89% of males dispersed and 11% bred in their natal clan, and dispersers that chose clans with many young females gained substantially higher long-term reproductive success. The variables measured did not support male–male competition, male inbreeding avoidance, or resource competition as the primary driver.

Two complications frame the unresolved questions. First, Van Horn, Watts and Holekamp (2008) challenged the interpretation of the time-based rule, arguing that females might instead choose on dispersal status (preferring immigrants over natal males), which would equally reduce incest risk; Höner et al. (2008) replied that one of the two rules cannot be explained by dispersal status. The dispute has never been adjudicated by new data. Second, the result is from a single population of a single species with female philopatry, high female social dominance, and male queuing; whether the mechanism generalizes, what sensory or cognitive machinery implements it, and what it does to population genetics over generations were explicitly left open.

Problem Statement

The unresolved problem posed by Höner et al. (2007) is to establish whether, how, and with what consequences female mate choice drives male-biased dispersal in social mammals, jointly across five linked questions. (1) Generality: is the sufficiency of simple time-based female mate-choice rules (males preferred whose clan tenure is shorter than the female's age, plus the age-dependent tenure preference) specific to the spotted hyena's female-philopatric, male-queuing society, or does female choice alone drive male dispersal across social mammals with different female survival, male queuing systems, kin structures and cue reliability — and where it does not, which factor breaks the mechanism? (2) Mechanism: what is the proximate, sensory or cognitive basis of the time-based rule — in particular, whether females track male tenure per se or dispersal status/early-life familiarity, as disputed in the 2008 Nature exchange — and with what error rates (false positives, i.e. accepted likely-kin sires; false negatives, i.e. rejected unrelated sires) under natural demographic and dispersal regimes? (3) Alternatives: to what extent do unmeasured or context-dependent aspects of male–male competition, male inbreeding avoidance, or resource competition contribute to male dispersal under ecological conditions different from the Ngorongoro Crater? (4) Consequences: the descriptive population-genetic consequences of demography-driven male dispersal — effects on gene flow, local relatedness structure and inbreeding — are already documented (Watts et al. 2011; Holekamp et al. 2012), so the open question is whether dispersal and female preferences suffice to buffer the genetic risks now known to arise from the hyenas' social inheritance of reproductive privilege, and what this implies for adaptive potential over the long term? (5) Male assessment: by what proximate mechanisms do males assess and compare clan demography (number of young females, competitors) during their pre-settlement excursions — what sensory and behavioural sampling rules, what information accuracy, what assessment costs — and how do these scale with landscape connectivity and population density? The five strands form one linked objective — determining whether, how, and under what conditions female mate choice drives male-biased dispersal, and what evolutionary machinery implements it. Each of the five strands is an independently refutable question that can be advanced on its own, while the problem as a whole is jointly posed across all five.

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