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Group Dynamics and Social Control of Reproduction in African Mole-Rats

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Group Dynamics and Social Control of Reproduction in African Mole-Rats 184 Review TRENDS in Ecology & Evolution Vol.16 No.4 April 2001 Family values: group dynamics and social control of reproduction in African mole-rats Chris G. Faulkes and Nigel C. Bennett To exploit ecological niches where constraints have favoured selection for increasingly enable elucidation of the detailed kin group living and cooperation, both vertebrates and invertebrates have evolved structure of social groups, the relative roles of different elaborate social systems. In mammals, numerous divergent taxa have proximate mechanisms that control reproductive skew converged at similar solutions to these ecological challenges (such as food can be properly understood. When does ‘SELF RESTRAINT’ distribution and predator avoidance), culminating in the social insect-like in the form of incest avoidance give way to the more behaviour of the naked mole-rat. Characteristically, breeding is partitioned extreme DOMINANT CONTROL that could be manifest as unequally in such groups, resulting in a ‘reproductive skew’.New research the suppression of reproductive physiology in linking studies of physiology, behaviour and molecular ecology in African nonbreeders, or even infanticide of their offspring mole-rats is helping us to elucidate why different proximate mechanisms that should they breed? Are there common mechanisms control groups of cooperative breeders might have evolved. mediating physiological suppression among divergent taxa, such as rodents, viverrids, canids and primates6 (Table 1), and how might ecological factors influence A characteristic of COOPERATIVELY BREEDING mammals the proximate control of reproductive skew? (see Glossary), where individuals other than the parents help care for offspring, is that reproduction is Monopoly of reproduction in African mole-rats partitioned unequally among members of the social The African mole-rats of the family Bathyergidae are group (REPRODUCTIVE SKEW), with socially dominant an ideal taxonomic group with which to tackle individuals monopolizing breeding opportunities. An questions about both ultimate factors and proximate increasing body of work is now revealing that the mechanisms that control reproduction in a social PROXIMATE MECHANISMS underlying this reproductive species, because they have a range of cooperative division of labour might differ between even closely breeding strategies and differing degrees of related species, and debate continues about the exact reproductive skew. Mating preferences encompass role the breeding female plays in maintaining levels of both facultative INBREEDING and obligate outbreeding, reproductive skew. Theoretical models of ‘incomplete and result in clear differences between mole-rat species control by dominants’1 and ‘concession’ theory in the way their social systems are maintained. involving ‘peace’ and ‘staying’ incentives2,3 (Box 1), have been proposed to explain inter- and intraspecific Sociality in African mole-rats differences in reproductive skew. The idea, however, Of the 18 or more species of African mole-rats, four are that the dominant breeder exerts, or attempts to exert, solitary. The other species in the genera Cryptomys some kind of reproductive control over subordinate and Heterocephalus exhibit varying degrees of sociality nonbreeders in the group is implicit in both models. and cooperative breeding. A characteristic feature of This control could manifest itself in different ways, the social species is a reproductive division of labour, ranging from, for example, infanticide of the offspring resulting in high reproductive skew and, consequently, of a subordinate, or interference by dominants with large variation in the lifetime reproductive success of subordinate mating attempts, to actual suppression of individuals. Two species, the naked mole-rat subordinate reproductive physiology4. As most (Heterocephalus glaber) and the Damaraland mole-rat Chris Faulkes* cooperatively breeding mammals live in extended (Cryptomys damarensis), fit the classic definition of School of Biological family groups, in many cases, INCEST AVOIDANCE alone EUSOCIALITY derived from social insects7,8. Other Sciences, Queen Mary, could be argued to be sufficient to maintain mole-rats and cooperatively breeding vertebrates University of London, 9,10 Mile End Road, London, reproductive skew, if the only unrelated individuals in might also fit this definition . Unlike other species, UK E1 4NS. the group are the founding parents. both Damaraland and naked mole-rats exhibit a *e-mail: Almost all animals have evolved mechanisms that behavioural division of labour among the nonbreeding [email protected] prevent them from breeding with close relatives. This helpers. In the Damaraland mole-rats, smaller Nigel Bennett protects them against the fitness costs of harmful individuals form a ‘frequent worker’ group, and in Dept of Zoology and recessive traits and decreased heterozygosity that naked mole-rats, the frequency of ‘work’ in the form of Entomology, University of Pretoria, Pretoria 0002, might be manifest in offspring arising from such ‘colony maintenance’ behaviour shows a negative South Africa. matings5. As molecular genetic techniques correlation with increasing body mass11,12. In addition, http://tree.trends.com 0169–5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(01)02116-4 Review TRENDS in Ecology & Evolution Vol.16 No.4 April 2001 185 be rare9. The social mole-rats studied to date in the Box 1. Reproduction in cooperative breeders – hegemony versus anarchy genus Cryptomys all have a mating system that In vertebrates, groups of cooperative breeders are characterized by a involves obligate outbreeding, whereas naked mole-rats reproductive division of labour in which a small number or, in the extreme, are unusual within the Bathyergidae and among a single member of each sex, breed. The remaining group members, of mammals in general because they can inbreed to a high both sexes, fulfil a ‘helper’ role, the nature of which varies between species. degree. These incestuous tendencies were originally Although they are nonbreeding, these individuals might accrue indirect or proposed as an important factor in explaining their inclusive fitness benefits because they are usually close relatives of the eusociality18, and it was argued that inbreeding breeders. Ecological constraints are ultimately thought to provide the produced a within kin-group genetic structure selective pressure for these reproductive and behavioural divisions of analogous to haplodiploidy in the Hymenoptera. labour. Theories of optimal reproductive skew consider such societies as a Indeed, naked mole-rats can inbreed to such an extent continuum of social systems, which differ in the way that lifetime that intra-colony relatedness has been estimated in reproductive success is distributed among group members on a scale from some groups at 0.8 (Ref. 18), greater than the maximum zero to one, the so-called ‘eusociality continuum’. This assumes that three-quarter relatedness possible in haplodiploid dominant members of the society control reproduction among the organisms where the queen is singly mated19. subordinatesa–d. In ‘low skew’ societies, all individuals have a more or less Although the inclusive fitness benefits of high equal chance of reproduction, whereas, in ‘high skew’ societies, relatedness to nonbreeding colony members are reproduction is limited to one or a small number of individuals of each sex. readily apparent, the puzzle remains that field data Although few would dispute that maintaining the optimal degree of from other cooperatively breeding mammals, skew (how many and which particular individuals breed) in a cooperatively including other social mole-rat species and the breeding society is adaptive, there are conflicting ideas about how such eusocial Damaraland mole-rat, follow the typical reproductive division of labour is established and maintained. pattern of incest avoidance. Thus, it has been proposed ‘Concession’ models argue that in certain circumstances it might pay the that inbreeding might be a derived trait, peculiar to dominant individual to allow some subordinates to breed, as an the naked mole-rat, which might have evolved as an inducement to stay in the group and cooperate peacefully (‘staying adaptive response to the high costs of dispersal. Once incentives’) or to prevent subordinates fighting for reproductive control deleterious recessive traits were purged from a (‘peace incentives’)b,d. Conversely, ‘incomplete control’ models suggest population, inbreeders would have had an advantage that subordinates breed simply because the dominant is unable to over obligate outbreeders, who could potentially suffer effectively suppress their reproductione, and ‘threat of eviction’ models fitness costs if opportunities for finding unrelated argue that skew arises from subordinate restraint, to avoid ejection from mates were rare. Indeed, without incestuous mating, the social groupf. colonies in which a breeder dies could face extinction References before sufficient (unpredictable) rainfall facilitates a Keller, L. and Reeve, H.K. (1994) Partitioning of reproduction in animal societies. emigration. Although the propensity for naked mole- Trends Ecol. Evol. 9, 98–102 rats to inbreed, together with genetic studies of wild- b Reeve, H.K. et al. (1998) Reproductive sharing in animal societies: reproductive caught colonies, indicate that dispersal is rare18,20, incentives or incomplete control by dominant breeders? Behav.
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