Reproductive skew: disentangling concessions from control
Authors: Stephen T Emlen, H.Kern Reeve, Laurent Keller
Journal: Trends in Ecology & Evolution (1998)

The question of allocation of reproduction among individuals in social groups—and the emergence of optimal skew theory as a robust framework for providing its answer—has aroused considerable interest and controversy. Optimal skew models (OSMs) are based on the idea of a social contract. When a dominant individual benefits from the activities of a same-sex subordinate, it may concede reproduction as an incentive for the latter to remain peacefully in the group. Optimal skew models assume that the dominant controls reproduction, and incorporate ecological, social and genetic relatedness factors to predict when reproduction will be shared and by how much[1Vehrencamp, S.L. (1979) in Handbook of Behavioral Neurobiology (Vol. 3) (Marler, P. and Vandenbergh, J., eds), pp. 351–394, Plenum PressGoogle Scholar, 2Emlen S.T. Am. Nat. 1982; 119: 40-53Crossref Google Scholar, 3Vehrencamp S.L. Anim. Behav. 1983; 31: 667-682Crossref Scopus (526) Google Scholar, 4Reeve, H.K. and Ratnieks, F.L.W. (1993) in Queen Number and Sociality in Insects (Keller, L., ed.), pp. 45–85, Oxford University PressGoogle Scholar, 5Keller L. Reeve H.K. Trends Ecol. Evol. 1994; 9: 98-103Abstract Full Text PDF PubMed Scopus (405) Google Scholar]. Clutton-Brock[6Clutton-Brock T.H. Trends Ecol. Evol. 1998; 13: 288-292Abstract Full Text Full Text PDF PubMed Scopus (244) Google Scholar]offers a critique of OSMs, challenging the generality of their assumptions and suggesting that many of the data cited in their support may be explained by the mutually exclusive alternative that dominants are simply unable to prevent breeding by subordinates (the incomplete control model, ICM). We agree that not all social groups meet the conditions of OSMs (especially that dominants benefit from the activities of subordinates) and that empirically disentangling ICMs from OSMs will sometimes be difficult. However, it is important to correct two misunderstandings about OSMs and describe three predictions from recent incomplete control models that promise to ease the task of differentiating between the alternatives. First, observations of overt conflict over reproduction do not constitute evidence differentially supporting either model. Accurate assessment of resource holding power is central to both OSMs and ICMs. In OSMs, aggression is part of the establishment and maintenance of reproductive control and is predicted to occur as long as group stability is not threatened. Indeed, concession models can be used to predict the maximum amount of aggression allowable within a stable group[7Reeve H.K. Keller L. Am. Nat. 1997; 150: S42-S58Crossref PubMed Scopus (50) Google Scholar]. Second, although the avoidance of close inbreeding by many vertebrates is an additional factor potentially influencing skew[8Emlen S.T. Am. Nat. 1996; 148: 756-763Crossref Scopus (37) Google Scholar], it does not (by itself) constitute an alternative to optimal skew models, because (1) the costs of incestuous mating can be incorporated into both the ICM and OSMs, and (2) a subordinate in a group with relatives is not necessarily constrained from mating with nonrelatives outside the group and rearing noninbred offspring within the group[9Reeve H.K. Keller L. Am. Nat. 1996; 148: 764-769Crossref Scopus (27) Google Scholar]. We recently published two ICMs (Ref. [10Reeve H.K. Emlen S.T. Keller L. Behav. Ecol. 1998; 9: 267-278Crossref Scopus (289) Google Scholar]) based on three assumptions:•The dominant has only limited control over the subordinate's reproduction.•Dominant and subordinate compete directly to increase their respective fractions of the total reproduction.•Such competition carries a cost by decreasing total group reproductive output. In these models, it is predicted that the subordinate's share of reproduction is largely unaffected by ecological constraints, whereas it varies inversely with the severity of such constraints in OSMs. Additionally, the subordinate's share of reproduction in these ICMs is largely insensitive to, or increases with, the subordinate's genetic relatedness to the dominant, whereas it varies inversely with such relatedness in OSMs. A third prediction distinguishes between ICMs and OSMs even when vertebrate familial groups consist of parent(s) and mature offspring. In simple parent-offspring associations (e.g. two dominant parents and a single subordinate helper), neither model predicts subordinate reproduction because of the genetic equivalence between a subordinate's full siblings and its own offspring. However, the OSM but not the ICM predicts that subordinate offspring can reproduce when there are multiple subordinate offspring and ecological constraints are weak[10Reeve H.K. Emlen S.T. Keller L. Behav. Ecol. 1998; 9: 267-278Crossref Scopus (289) Google Scholar]. We agree with Clutton-Brock that there is an obvious need for additional theoretical and empirical work on both ICMs and OSMs. Future research, aimed at testing the predictions discussed here, will determine the importance of concessions versus incomplete control in the allocation of reproduction within animal societies.