Reproductive Skew Theory

Abstract

An almost universal characteristic of cooperatively breeding animal groups is the unequal sharing of reproduction within the group, referred to as reproductive skew. Reproductive skew theory has been developed to investigate the adaptive causes underlying the variation in reproduction between and within species seen in nature. From its inception in the late 1970s, skew theory has expanded over the years both conceptually and in its application. Three main types of models are distinguished: Transactional models assume that reproductive shares are offered as a reward for cooperative behaviour, tug‐of‐war; TOW (or compromise) models assume that reproductive shares are determined by competitive abilities of individuals. Both assumptions are reconciled in the third type of models, most recently developed synthetic models.

Reproductive skew theory makes predictions about the range of skew using a set of key parameters such as relatedness and competitive abilities of group members. Skew theory has been applied to a wide variety of topics in evolutionary biology such as parent–offspring conflict, sex ratio conflict or the evolution of cooperation. Key to skew theory is the question under what conditions groups remain stable and it has thus been advanced as a framework to understand the evolution of sociality.

Key Concepts:

  • Social animals living in groups must often resolve a conflict over the allocation of reproduction.

  • Unequal partitioning of reproduction is termed reproductive skew. Reproductive skew is a degree of reproductive bias in favour of one or a few breeders.

  • Skew theory provides a possible explanation for conflict resolution and adaptive causes of sociality.

  • Several indices of skew exist, suitable for different types of studies and questions.

  • There are three main types of models: transactional, tug‐of‐war (TOW) (also referred to as compromise) and synthetic models, based on different assumptions and yielding different predictions.

  • Transactional models are subdivided into two categories: concession and restraint models. Concession models assume full control of dominants over reproduction in the group, and reproductive share is offered as a reward for cooperation. Restraint models assume subordinates are free to claim reproduction and are only limited by the threat of eviction.

  • TOW models are based on the assumption that both subordinates and dominants have only a limited control over the reproduction and reproductive share is determined by the mutual competitive abilities.

  • Synthetic models combine features of transactional and TOW models. The maximal and minimal reproductive share of the subordinate for a group to remain stable is determined as in transactional models, while, within the range given by the maximal and minimal share, the exact reproductive share is determined by the competitive abilities of both subordinate and dominant in a TOW scenario.

Keywords: reproductive skew; conflict resolution; transactional models; tug‐of‐war models; compromise models; sociality; cooperative behaviour

Figure 1.

Division of reproductive skew models.

Figure 2.

Illustration of the minimal and maximal subordinate's reproductive share as a function of relatedness r and group productivity k in transactional models. Both pmin (solid line) and pmax (dotted line) are shown for different values of k, the productivity of the association: 6 (green lines), 7 (blue lines) and 8 (red lines). Productivity of lone subordinate and dominant are xs=1 and xd=4, respectively.

Figure 3.

Dominant's (a) and subordinate's (b) reproductive share as a function of relatedness r and their relative competitive abilities b, according to TOW models.

Figure 4.

Synthetic model. Maximal and minimal subordinate's reproductive shares required for a group to remain stable depend on relatedness between individuals. Restraint models give the maximum share that subordinates can gain, while its minimal share is given by concession models. Inside this range, the exact reproductive share is determined by competitive abilities of both subordinate and dominant (TOW model).

close

References

Buston PM and Zink AG (2009) Reproductive skew and the evolution of conflict resolution: a synthesis of transactional and tug‐of‐war models. Behavioral Ecology 20(3): 672–684.

Cant MA (1998) A model for the evolution of reproductive skew without reproductive suppression. Animal Behaviour 55(1): 163–169.

Cant MA (2006) Stable group size in cooperative breeders: the role of inheritance and reproductive skew. Behavioral Ecology 17(4): 560–568.

Cant MA and English S (2006) Stable group size in cooperative breeders: the role of inheritance and reproductive skew. Behavioral Ecology 17(4): 560–568.

Cant MA and Johnstone RA (2009) How threats influence the evolutionary resolution of within‐group conflict. American Naturalist 173(6): 759–771.

Clutton‐Brock TH (1998) Reproductive skew, concessions and limited control. Trends in Ecology & Evolution 13(7): 288–292.

Clutton‐Brock TH, Brotherton P, Russell A et al. (2001) Cooperation, control, and concession in meerkat groups. Science 291(5503): 478.

Creel SR and Waser PM (1991) Failures of reproductive supression in dwarf mongooses (Helogale parvula): accident or adaptation? Behavioral Ecology 2(1): 7–15.

Danforth BN, Neff JL and Barretto‐Ko P (1996) Nestmate relatedness in a communal bee, Perdita Texana (Hymenoptera: Andrenidae), based on DNA fingerprinting. Evolution 50(1): 276–284.

Glichrist JD (2006) Reproductive success in a low skew, communal breeding mammal: the banded mongoose, Mungos mungo. Behavioural Ecology and Sociobiology 60: 854–863.

Hager R (2003) Models of reproductive skew applied to primates. In: Jones CB (ed.) Sexual Selection and Reproductive Competition in Primates: New Perspectives and Directions, pp. 65–101. Norman: American Society of Primatologists.

Hager R (2009) Explaining variation in reproductive skew among male langurs: effects of future mating prospects and ecological factors. In: Hager R and Jones CB (eds) Reproductive Skew in Vertebrates: Proximate and Ultimate Causes, pp. 134–164. Cambridge: Cambridge University Press.

Hager R and Johnstone RA (2004) Infanticide and control of reproduction in cooperative and communal breeders. Animal Behaviour 67(5): 941–949.

Harris WE and Hager R (2009) On the evolution of reproductive skew: a genetical view. In: Hager R and Jones CB (eds) Reproductive Skew in Vertebrates: Proximate and Ultimate Causes, pp. 467–479. Cambridge: Cambridge University Press.

Heg D, Bergmüller R, Bonfils D et al. (2006) Cichlids do not adjust reproductive skew to the availability of independent breeding options. Behavioral Ecology 17(3): 419–429.

Johnstone RA (2000) Current issues – perspectives and reviews. Ethology 106: 5–26.

Johnstone RA and Cant MA (1999a) Reproductive skew and indiscriminate infanticide. Animal Behaviour 57(1): 243–249.

Johnstone RA and Cant MA (1999b) Reproductive skew and the threat of eviction: a new perspective. Proceedings of the Royal Society of London. Series B: Biological Sciences 266(1416): 275–279.

Keane B, Waser PM, Creel SR et al. (1994) Subordinate reproduction in dwarf mongooses. Animal Behaviour 47(1): 65–75.

Keller L and Reeve HK (1994) Partitioning of reproduction in animal societies. Trends in Ecology & Evolution 9(3): 98–102.

Keller L and Vargo EL (1993) Reproductive structure and reproductive roles in colonies of eusocial insects. In: Keller L (ed.) Queen Number and Sociality in Insects, pp. 16–44. Oxford: Oxford University Press.

Kokko H and Johnstone RA (1999) Social queuing in animal societies: a dynamic model of reproductive skew. Proceedings of the Royal Society of London. Series B: Biological Sciences 266(1419): 571–578.

Kokko H and Lindström JAN (1997) Measuring the mating skew. American Naturalist 149(4): 794–799.

Kokko H, Mackenzie A, Reynolds JD, Lindström J and Sutherland WJ (1999) Measures of inequality are not equal. American Naturalist 72: 358–382 ST.

Kutsukake N and Nunn CL (2006) Comparative tests of reproductive skew in male primates: the roles of demographic factors and incomplete control. Behavioral Ecology and Sociobiology 60(5): 695–706.

Lu X, Wang C and Du B (2011) Reproductive skew in an avian cooperative breeder: an empirical test for theoretical models. Behavioral Ecology 23(1): 11–17.

Magrath RD and Heinsohn RG (2000) Reproductive skew in birds: models, problems and prospects. Journal of Avian Biology 31(2): 247–258.

Moore J (1982) Coalitions in langur all‐male bands. International Journal of Primatolgy 5: 537–589.

Nonacs P (2000) Measuring and using skew in the study of social behavior and evolution. American Naturalist 156(6): 577–589.

Nonacs P (2002) Sex ratios and skew models: the special case of evolution of cooperation in polistine wasps. American Naturalist 160(1): 103–118.

Nonacs P (2003) Measuring the reliability of skew indices: is there one best index? Animal Behaviour 65(3): 615–627.

Nonacs P, Liebert AE and Starks PT (2006) Transactional skew and assured fitness return models fail to predict patterns of cooperation in wasps. American Naturalist 167(4): 467–480.

Nonacs P, Reeve HK and Starks PT (2004) Optimal reproductive‐skew models fail to predict aggression in wasps. Proceedings of the Royal Society of London. Series B: Biological Sciences 271(1541): 811–817.

Pamilo P (1996) Reproductive skew simplified. Oikos 75(3): 533–535.

Paxton RJ, Thorén PA, Tengö J, Estoup A and Pamilo P (1996) Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera, Andrenidae), using microsatellites. Molecular Ecology 5(4): 511–519.

Ratnieks FLW, Foster KR and Wenseleers T (2006) Conflict resolution in insect societies. Annual Review of Entomology 51: 581–608.

Reeve HK (1991) Polistes. In: Ross K and Matdiews R (eds) The Social Biology of Wasps, pp. 99–148. Ithaca, New York: Cornell University Press.

Reeve HK (1998) Game theory, reproductive skew and nepotism. In: Dugatkin LA and Reeve HK (eds) Game Theory and Animal Behavior, pp. 118–145. Oxford: Oxford University Press.

Reeve HK (2000a) A transactional theory of within‐group conflict. American Naturalist 155(3): 365–382.

Reeve HK (2000b) Reproductive skew and group size: an N‐person staying incentive model. Behavioral Ecology 11(6): 640–647.

Reeve HK, Emlen ST and Keller L (1998) Reproductive sharing in animal societies: reproductive incentives or incomplete control by dominant breeders? Behavioral Ecology 9(3): 267–278.

Reeve HK and Jeanne R (2003) From individual control to majority rule: extending transactional models of reproductive skew in animal societies. Proceedings of the Royal Society of London. Series B: Biological Sciences 270(1519): 1041–1045.

Reeve HK and Keller L (1995) Partitioning of reproduction in mother‐daughter versus sibling associations: a test of optimal skew theory. American Naturalist 145(1): 119–132.

Reeve HK and Keller L (2001) Tests of reproductive‐skew models in social insects. Annual Review of Entomology 46: 347–385.

Reeve HK and Ratnieks FLW (1993) Queen‐queen conflict in polygynous societies: mutual tolerance and reproductive skew. In: Keller L (ed.) Queen Number and Sociality in Insects, pp. 45–85. Oxford: Oxford University Press.

Reeve HK and Shen SF (2006) A missing model in reproductive skew theory the bordered tug‐of‐war. Proceedings of the National Academy of Sciences of the USA 103(22): 8430–8434.

Shen SF and Reeve HK (2010) Reproductive skew theory unified: the general bordered tug‐of‐war model. Journal of Theoretical Biology 263(1): 1–12.

Sherman PW, Lacey EA, Reeve HK and Keller L (1995) The eusocialitiy continuum. Behavioral Ecology 6(1): 102–108.

Sumner S, Casiraghi M, Foster W and Field J (2002) High reproductive skew in tropical hover wasps. Proceedings of the Royal Society of London. Series B: Biological Sciences 269(1487): 179–186.

Tsuji K and Kasuya E (2001) What do the indices of reproductive skew measure? American Naturalist 158(2): 155–165.

Tsuji K and Tsuji N (1998) Indices of reproductive skew depend on average reproductive success. Evolutionary Ecology 12: 141–152.

Vehrencamp SL (1979) The roles of individual kin and group selection in the evolution of sociality. In: Marler P and Vandenbergh J (eds) Handbook of Behavioral Neurobiology, pp. 351–394. New York: Plenum Press.

Vehrencamp SL (1983) A model for the evolution of despotic vs. egalitarian societies. Animal Behaviour 31: 667–682.

Further Reading

Field J and Cant MA (2009) Social stability and helping in small animal societies. Philosophical Transactions of the Royal Society of London Series B 364(1533): 3181–3189.

Hager R and Jones CB (2009) Reproductive Skew in Vertebrates. Cambridge: Cambridge University Press.

Jeon J and Chun Choe J (2003) Reproductive skew and the origin of sterile castes. American Naturalist 161: 206–224.

Langer P, Hogendoorn K and Keller L (2004) Tug‐of‐war over reproduction in a social bee. Nature 428: 844–847.

Nonacs P and Hager R (2011) The past, present and future of reproductive skew theory and experiments. Biological Reviews of the Cambridge Philosophical Society 86(2): 271–298.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Trubenová, Barbora, and Hager, Reinmar(Jul 2012) Reproductive Skew Theory. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023661]