Female extrapair mate choice in a cooperative breeder: trading sex for help and increasing offspring heterozygosity

Proceedings of the Royal Society B: Biological Sciences, Aug 2007

Sexual conflict between males and females over mating is common. Females that copulate with extrapair mates outside the pair-bond may gain (i) direct benefits such as resources or increased paternal care, (ii) indirect genetic benefits for their offspring, or (iii) insurance against infertility in their own social mate. Few studies have been able to demonstrate the different contexts in which females receive varying types of benefits from extrapair mates. Here, I examined sexual conflict, female extrapair mate choice, and patterns of extrapair paternity in the cooperatively breeding superb starling Lamprotornis superbus using microsatellite markers. Although extrapair paternity was lower than many other avian cooperative breeders (14% of offspring and 25% of nests), females exhibited two distinct mating patterns: half of the extrapair fertilizations were with males from inside the group, whereas half were with males from outside the group. Females with few potential helpers copulated with extrapair mates from within their group and thereby gained direct benefits in the form of additional helpers at the nest, whereas females paired to mates that were relatively less heterozygous than themselves copulated with extrapair mates from outside the group and thereby gained indirect genetic benefits in the form of increased offspring heterozygosity. Females did not appear to gain fertility insurance from copulating with extrapair mates. This is the first study to show that individuals from the same population mate with extrapair males and gain both direct and indirect benefits, but that they do so in different contexts.

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Female extrapair mate choice in a cooperative breeder: trading sex for help and increasing offspring heterozygosity

Dustin R. Rubenstein () 0 1 2 0 Cornell Laboratory of Ornithology, Fuller Evolutionary Biology Program , 159 Sapsucker Woods Road, Ithaca, NY 14850-1999 , USA 1 Museum of Vertebrate Zoology, University of California , 3060 Valley Life Sciences Building, Berkeley, CA 94720-3140 , USA 2 Department of Neurobiology and Behavior, Cornell University , Seeley G. Mudd Hall, Ithaca, NY 14853-2702 , USA Sexual conflict between males and females over mating is common. Females that copulate with extrapair mates outside the pair-bond may gain (i) direct benefits such as resources or increased paternal care, (ii) indirect genetic benefits for their offspring, or (iii) insurance against infertility in their own social mate. Few studies have been able to demonstrate the different contexts in which females receive varying types of benefits from extrapair mates. Here, I examined sexual conflict, female extrapair mate choice, and patterns of extrapair paternity in the cooperatively breeding superb starling Lamprotornis superbus using microsatellite markers. Although extrapair paternity was lower than many other avian cooperative breeders (14% of offspring and 25% of nests), females exhibited two distinct mating patterns: half of the extrapair fertilizations were with males from inside the group, whereas half were with males from outside the group. Females with few potential helpers copulated with extrapair mates from within their group and thereby gained direct benefits in the form of additional helpers at the nest, whereas females paired to mates that were relatively less heterozygous than themselves copulated with extrapair mates from outside the group and thereby gained indirect genetic benefits in the form of increased offspring heterozygosity. Females did not appear to gain fertility insurance from copulating with extrapair mates. This is the first study to show that individuals from the same population mate with extrapair males and gain both direct and indirect benefits, but that they do so in different contexts. 1. INTRODUCTION Conflict between males and females over reproduction is common in many species of animals (Arnqvist & Rowe 2005). Sexual conflict over mating often occurs because males and females benefit differentially from mating with (i) multiple individuals, since males typically have a higher optimal mating frequency than females or (ii) specific individuals, since males are typically less choosy than females about mates ( Wedell et al. 2006). Although males typically have more to gain from mating multiply than do females (Bateman 1948; but see Andersson & Simmons 2006), studying why females might engage in, or even initiate, mating with multiple males has generated substantial controversy ( Westneat & Stewart 2003; Arnqvist & Kirkpatrick 2005, 2007; Albrecht et al. 2006; Charmantier & Sheldon 2006; Hadfield et al. 2006; Qvarnsrtom et al. 2006; Griffith 2007). Irrespective of which sex initiates extrapair matings, there is good evidence to suggest that females actively make extrapair mate-choice decisions ( Jennions & Petrie 2000; Griffith et al. 2002; Westneat & Stewart 2003; Mays & Hill 2004; Neff & Pitcher 2005; Hoffman et al. 2007) and even dynamically allocate paternity (Safran et al. 2005). However, despite a great deal of empirical work on female extrapair mate choice, few studies have been able to demonstrate the different contexts in which females receive varying types of benefits from extrapair mates ( Westneat & Stewart 2003). Females may copulate with males outside the pair-bond to (i) guard against infertility in their own social mate (fertility insurance hypothesis; Wetton & Parkin 1991; Sheldon 1994) or gain two non-exclusive types of benefits (reviewed in Birkhead & Mller 1992; Griffith et al. 2002; Cockburn 2004). The potential benefits that females may receive from extrapair mates include: (ii) direct benefits such as resources or increased paternal care provided by helpers at the nest (direct benefits hypothesis; Wolf 1975; Burke et al. 1989; Colwell & Oring 1989) or (iii) indirect genetic reproductive benefits including obtaining good genes for their offspring (genetic quality hypothesis; Mller 1988; Hamilton 1990; Westneat et al. 1990; Birkhead & Mller 1992; Gray 1997), maximizing genetic diversity among their offspring (genetic diversity hypothesis; Westneat et al. 1990) or maximizing genetic compatibility between themselves and the father of the offspring (genetic compatibility hypothesis; Zeh & Zeh 1996; Kempenaers et al. 1999; Tregenza & Wedell 2000). These hypotheses have not been tested simultaneously in any cooperative breeders (Cockburn 2004), despite the fact that cooperatively breeding species are tractable and powerful study systems in which to test these ideas since having helpers at the nest may reduce the potential costs of female extrapair mating decisions. In other words, if cuckoldry results in a reduction of paternal care and constrains females from seeking extrap (...truncated)


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Dustin R Rubenstein. Female extrapair mate choice in a cooperative breeder: trading sex for help and increasing offspring heterozygosity, Proceedings of the Royal Society B: Biological Sciences, 2007, pp. 1895-1903, 274/1620, DOI: 10.1098/rspb.2007.0424