The Lengths Birds Will Go to Avoid Incest

Journal of Animal Ecology 2012, 81, 735–737 doi: 10.1111/j.1365-2656.2012.02008.x

IN FOCUS The lengths birds will go to avoid incest

A southern pied babbler (Turdoides bicolor) subordinate female immediately before dispersal to become dominant in a new group. Dispersal is an important mechanism whereby southern pied babblers avoid inbreeding; though there is no sex-bias in dispersal distance, individuals move twice as far from birth groups as from subsequent groups. Southern pied babblers are found throughout the Kalahari Desert. A habituated population is intensively studied at the Pied Babbler Research Project, Kuruman River Reserve, Northern Cape, South Africa. Image courtesy Tom Flower.

Nelson-Flower, M.J., Hockey, A.R., O’Ryan, C.O. & Ridley, A.R. (2012) Inbreeding avoidance mechanisms: dispersal dynamics in cooperatively breeding southern pied babblers. Journal of Animal Ecology, 81, 875–882.

Cooperatively breeding species, in which some individuals help others to rear their offspring, face a high risk of inbreeding because of close relatedness within social groups. Many species circumvent this problem via sex-biased dispersal, in which one sex is more likely to disperse (and to disperse further), while the other stays and helps. In the absence of sex-biased dispersal, more complex dispersal patterns can arise, based on kin recognition. However, this can also present challenges when dispersal distances are short, leading to clusters of relatives on neighbouring territories. In this issue, Nelson-Flower et al. (2012) break important new ground by unravelling adaptive incest-avoidance mechanisms in a cooperatively breeding bird without sex-biased dispersal. They provide an elegant demonstration of ﬁnely tuned dispersal distances together with cognitively based methods for knowing whom to avoid as mates.

Not all animals avoid inbreeding, but it seems that most do mulated in our scientific thinking, and indeed that we seek, (Keller & Waller 2002). This is because breeding with close find and explain similar patterns in the mating systems of relatives can cause inbreeding depression and loss of fitness other species. The reward for behavioural ecologists who (Pusey & Wolf 1996). Humans are no different, and most of delve deeply enough is the wide and intricate array of strate- us have set standards regarding who is considered suitable gies animals use to avoid incest. and unsuitable as mates. An almost universal rule seems to Cooperatively breeding species provide a wonderful arena be the exclusion of close relatives as sexual partners (Wester- for establishing the importance of inbreeding avoidance in marck 1921; Lieberman & Symons 1998). Such ‘incest other animals. Like humans, they often live in kin-based taboos’ are likely the cultural implementation of the evolved groups with highly variable mating systems and similar ten- preference for sexual partners who do not share too many sions between the costs and benefits of group living (Emlen genes. With such strong roots in our psyche, it is hardly sur- 1997; Cockburn 1998). Many cooperative breeders are also prising that the notion of incest taboos has been so well for- sedentary and only disperse over short distances, leading to difficulties in avoiding kin as mates (Koenig & Haydock 2004). Although individuals in cooperative species often Correspondence author. E-mail: [email protected]

Ó 2012 The Author. Journal of Animal Ecology Ó 2012 British Ecological Society 736 R. Heinsohn forgo breeding themselves and instead help others (often makes it hard for a breeder to seek extra-pair copulations, their relatives) to breed, the stage is set for kin competition and this could ultimately explain why they are not at all open and potential inbreeding when they mature and weigh their to pairings with relatives in the first place. Similarly, intense options about whether to stay in the group or seek their for- competition for breeding opportunities might explain why tunes elsewhere. dominant females in this species never give up their breeding The potential for inbreeding remains high at this point for positions when their mates die. two reasons. First, a shortage of breeding vacancies (often The greatest insights by Nelson-Flower et al. (2012) arise the cause of group living in the first place, Koenig et al. 1992; via their fine-scale analysis of spatial autocorrelation using Cockburn 1998) means that individuals have limited oppor- geographic and genetic distance matrices (Peakall & tunities to disperse and choose their social partner, to the Smouse 2006). Although dispersal distances were short, extent that even close relatives can end up paired to each dispersers moved twice as far from natal groups as they other. Second, although there are mechanisms that prevent did from non-natal groups, taking them beyond the range inbreeding within groups, limited dispersal distances can lead of most close relatives (roughly 1Æ2 km). Another species, to spatial clusters of relatives, often in adjacent territories. the red-winged fairywren (Malurus elegans) also avoids How individuals avoid mating with familiar and unfamiliar inbreeding by mating preferentially outside the neighbour- relatives in both sets of circumstances is of great interest. hood containing close relatives, although in that case, the Nelson-Flower et al. (2012) provide fascinating details results came about via female mating forays as far as was for how cooperatively breeding southern pied babblers necessary, rather than dispersal per se (Brouwer et al. (Turdoides bicolor) avoid the first problem altogether and 2011). Intriguingly, there was no evidence for a sex differ- how they overcome the second problem concerning clusters ence in southern pied babbler dispersal distance, meaning of relatives they might not explicitly recognise. Their sophisti- that they rely instead on use of a minimum distance to cated analysis, using both population genetics and observa- avoid relatives. However, short dispersal distances mean tional data, combines with a wave of other recent studies to they must still have some chance of bumping into related demonstrate just how far (literally, in their case) birds will go birds that they do not recognise and incur some risk of to avoid inbreeding. unknown incestuous matings. Nelson-Flower et al. (2012) The most obvious way birds avoid mating with relatives is argue that this might again relate to the dangers and stress to move away from the natal territory (Greenwood 1980; of longer distance dispersal and prospecting, and the bene- Szulkin & Sheldon 2008). This is normally enhanced by one fits of being able to return to the safe haven of the home sex (usually females) dispersing farther on average so that territory until new space is found. Theoretical reasoning opposite-sex relatives become spatially separated (Koenig has shown that inbreeding might be the lesser of evils when et al. 1992; Cockburn 1998). Another mechanism is for indi- the cost of dispersal is high (Lehmann & Perrin 2003). This viduals to avoid breeding with ‘natal-familiar’ partners reminds us that inbreeding, although costly, is probably (those that were present in one’s infancy, Komdeur & Hatch- better than no breeding and is definitely better than death. well 1999). This is equivalent to the Westermarck effect in This leads to the intriguing and related question of why humans (Westermarck 1921; Rantala & MarcinKowska these birds do not have sex-biased dispersal, as differential 2011), in which people who live in close domestic proximity behaviour would provide the usual guarantee of spatial during the first few years of their lives become desensitized to separation of related opposite-sex birds Only two other coop- later sexual attraction. Avoidance of natal-familiar partners eratively breeding species, white-winged choughs (Corcorax leads to well-cited patterns of behaviour among coopera- melanorhamphos – Beck, Peakall & Heinsohn 2008) and grey- tively breeding birds upon the death of a breeder. For exam- crowned babblers (Pomatostomus temporalis – Blackmore, ple, individuals often disperse (either voluntarily or by force) Peakall & Heinsohn 2011), have been demonstrated geneti- following the death of a same-sex breeder (e.g. Koenig, Hay- cally to lack sex differences in this way, and these have dock & Stanback 1998), and breeding individuals can even broadly similar life styles to southern pied babblers. All three abandon their coveted position within the group when all live in large and highly cohesive groups with long-term pair other members of the opposite sex are close relatives (e.g. bonds between dominants, helpers that greatly enhance the Cockburn et al. 2003). reproductive success of breeders, and a chronic lack of new The study by Nelson-Flower et al. (2012) shows that breeding opportunities. Intriguingly, however, grey-crowned southern pied babblers combine knowledge of who they babblers show little clustering of relatives outside the social might be related to with adaptive dispersal distances that are group and long dispersal distances (when they do disperse), not sex-specific. They will only inherit breeding positions in whereas white-winged choughs (like southern pied babblers) their groups when the opposite-sex breeder is unrelated. This are closely related to others within a small (2-km) radius. For pattern occurs in a variety of cooperative species (Koenig & southern pied babblers and white-winged choughs at least, it Haydock 2004), but appears to be a strict rule in southern appears to be better for both sexes to seek opportunities clo- pied babblers. In other species where social pairing of rela- ser to home and risk breeding with unknown kin. tives does occur, the breeders often avoid mating with each When close relatives form a social pair, and know about it, other and instead seek extra-group matings. It might be the extra-pair paternity (where the female mates with someone unusually intense territoriality of southern pied babblers that other than her social mate) has been suggested as an alterna-

Ó 2012 The Author. Journal of Animal Ecology Ó 2012 British Ecological Society, Journal of Animal Ecology, 81,735–737 The lengths birds will go to avoid incest 737 tive strategy to avoid inbreeding (Brooker et al. 1990; Pusey Brooker, M.G., Rowley, I., Adams, M. & Baverstock, P.R. (1990) Promiscuity & Wolf 1996). However, this is only a solution from the – an inbreeding avoidance mechanism in a socially monogamous species. Behavioral Ecology and Sociobiology, 26, 191–199. female’s perspective and can lead to retaliatory withdrawal Brouwer, L., Van de Pol, M., Atema, E. & Cockburn, A. (2011) Strategic pro- of paternal care if the male loses confidence in his paternity miscuity helps avoid inbreeding at multiple levels in a cooperative breeder (Arnold & Owens 2002). The presence of an alternative work- where both sexes are philopatric. Molecular Ecology, 20, 4796–4807. Cockburn, A. 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Ó 2012 The Author. Journal of Animal Ecology Ó 2012 British Ecological Society, Journal of Animal Ecology, 81,735–737