Is there extra-pair paternity in the cooperatively breeding Brown-headed Nuthatch?
Uncommon levels of relatedness and parentage in a cooperatively breeding bird, the Brown-headed Nuthatch (Sitta pusilla). Han, K.L., Cox, J.A., and Kimball, R.T. 2015. The Wilson Journal of Ornithology, DOI: 10.1676/14-193.1. VIEW
Cooperative breeding in birds occurs when more than two adults contribute to raising young at a single nest. Traditionally, these groups are thought to be family groups formed by a breeding pair and non-breeding helpers. Although helpers are usually male offspring from previous years (Ekman et al. 2004), some cooperative systems may also include helpers related to only one breeder, unrelated helpers, or a mixture of related and unrelated helpers. With the advent of genetic tools, we’ve learned that there is a lot of variation in patterns of relatedness. Additionally, while monogamy was assumed to be a component of cooperative groups, genetic tools have also allowed us to assess the extent of extra-pair (but within breeding group) and extra-group fertilizations observed. This variation in extra-group fertilizations and relatedness can affect behaviors such as parental investment and mate selection, and suggests that an understanding of relatedness is important to understanding the evolution of cooperative breeding in birds. Still, genetic studies of cooperatively breeding birds remains uncommon and represents less than 10% of cooperatively breeding species described (Riehl 2013).
Brown-headed nuthatches (Sitta pusilla) are cavity nesting birds that live in open pine forests of the southeastern United States (Slater et al. 2013). They are non-migratory and maintain territories year-round. They are facultative cooperative breeders, that is some, but not all, breeding groups have helpers. Although most helpers appear to be male offspring from previous years, very little is known about their mating system.
We studied a population at Tall Timbers Research Station in northern Florida from 2006 to 2010. Nuthatches excavate fresh cavities in decayed snags or dead trees each breeding season. Therefore, nests were relatively low, making them relatively accessible. We collected genetic samples from 50 family groups representing 59 clutches and genotyped them using 9 microsatellite markers developed for this species.
Figure 1 Brown-headed nuthatch nestlings
© Kin-Lan Han
About 23% of the population consisted of cooperative groups, and cooperative groups had just a single helper (87%), although up to three helpers were observed at a nest. Most helpers were related to at least one member of the breeding pair. Of the 23 helpers we genotyped, only four were unrelated to either member of the breeding pair, while ten were related to only one member of the breeding pair. Helpers were primarily male, although we had one case of a female helper who was unrelated to either member of the breeding pair. Most helpers were the result of delayed dispersal, although in a few cases older helpers were observed providing assistance after their own attempt to breed failed (redirected helping).
Helper relatedness to only a single parent could be due to a number of factors. One parent could die and the surviving adult acquires a new mate. Females have a higher mortality than males (Cox and Slater 2007) and is consistent with our observation that more helpers were related to the breeding male only than the breeding female only. Alternatively, helpers related to the breeding female only could be the result of past extra-pair copulations. In at least one instance, a helper was only related to the female although he was banded as a nestling of this breeding pair the previous year.
Although monogamy has been shown in some cooperative breeders such as the Florida Scrub Jay (Quinn et al. 1999), this was not necessarily the case with Brown-headed nuthatches. Of the 59 nests genotyped 41% showed evidence of extra-pair young. This level of extra-pair fertilizations that we detected is high compared to those observed in other passerines and most cooperative breeders (Westneat and Stewart 2003, Cornwallis et al. 2010).
Figure 2 The proportion of nests with extra-pair young in pair (N=40) and cooperative (N=19) groups. Proportions of extra-pair young were calculated within each group type. There was no significant difference in proportion of nests with extra-pair young between pairs and cooperative groups (Fisher’s exact P=0.40).
Extra-pair young were found in nests of both cooperative groups and pairs. Extra-pair young represented only a small fraction of the nestlings; most nestlings were sired by the dominant male, consistent with other studies of cooperative groups where extra-pair young were found (reviewed in Cockburn et al 2004). There was no difference in the proportion of nests with extra-pair young between pairs and cooperative groups. If helpers better defended a territory from intruders, we would have expected a higher level of extra-pair paternity in pairs. Alternatively, if helpers reproduced in cooperative groups, we would have expected to see higher extra-pair paternity in cooperative groups. Helpers generally did not sire offspring in the nests where multiple paternity was found, as might have been expected if helpers were related to the breeding female. However, we found two possible cases of incest, where helpers were related to both members of the breeding pair. The relatedness of the nestling to the helper in these instances (r = 0.72 and 0.79) was greater than would be expected (r = 0.5) if they were full siblings. Although incest overall appears to be rare in Brown-headed nuthatches, this suggests that mechanisms to avoid inbreeding are not perfect and could become a greater issue in smaller, more isolated populations, which may be occurring due to habitat loss and fragmentation.
Overall, Brown-headed nuthatches have a far more complex mating system than we originally expected based on field observations alone, and emphasizes the importance of combining genetic techniques with field studies.
Cockburn, A. 2004. Mating systems and sexual conflict. In: W.D. Koenig and J.L. Dickinson (eds.) Ecology and Evolution of Cooperative Breeding in Birds, pp. 81–101. Cambridge University Press, Cambridge, UK. View
Cornwallis, C.K., West, S.A., Davis, K.E., and Griffin, A.S. 2010. Promiscuity and the evolutionary transition to complex societies. Nature 466: 969–972. View
Ekman, J., Dickinson, J.L., Hatchwell, B.J. and Griesser, M. 2004 Delayed dispersal. In: W.D. Koenig and J.L. Dickinson (eds.) Ecology and evolution of cooperative breeding in birds, pp. 35-47. Cambridge University Press, Cambridge, UK. View
Riehl, C. 2013. Evolutionary routes to non-kin cooperative breeding in birds. Proceedings of the Royal Society of London, Series B 280: 2013.2245. View
Slater, G., Lloyd, J.D., Withgott, J.H., and Smith, K.G. 2013. Brown-headed Nuthatch (Sitta pusilla). The Birds of North America. Number 349. View
Cox, J.A. and Slater, G.L. 2007. Cooperative breeding in the Brown-headed Nuthatch. Wilson Journal of Ornithology 119: 1–8. View
Quinn, J.S., Woolfenden, G.E., Fitzpatrick, J.W., and White, B.N. 1999. Multi-locus DNA fingerprinting supports genetic monogamy in Florida Scrub-Jays. Behavioral Ecology and Sociobiology 45: 1–10. View
Westneat, D.F. and Stewart, I.R.K. 2003. Extra-pair paternity in birds: causes, correlates, and conflict. Annual Review of Ecology, Evolution, and Systematics 34: 365–396. View
Featured image: Brown-headed Nuthatch (Sitta pusilla) – Ash, North Carolina © Dick Daniels
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