The relative role of relatives in conspecific brood parasitism

Conspecific brood parasites lay their eggs in the nests of other females in the same population, leading to a fascinating array of possible ‘games’ among parasites and their hosts ( Davies 2000 ; Lyon & Eadie 2008 ). Almost 30 years ago, Andersson & Eriksson (1982) first suggested that perhaps this form of parasitism was not what it seemed—indeed, perhaps it was not parasitism at all! Andersson & Eriksson (1982) observed that conspecific brood parasitism (CBP) was disproportionally common in waterfowl (Anatidae), a group of birds for which natal philopatry is female‐biased rather than the more usual avian pattern of male‐biased natal philopatry. Accordingly, Andersson (1984) reasoned (and demonstrated in an elegantly simple model) that relatedness among females might facilitate the evolution of CBP—prodding us to reconsider it as a kin‐selected and possibly cooperative breeding system rather than a parasitic interaction. The idea was much cited but rarely tested empirically until recently—a number of new studies, empowered with a battery of molecular techniques, have now put Andersson’s hypothesis to the test ( Table 1 ). The results are tantalizing, but also somewhat conflicting. Several studies, focusing on waterfowl, have found clear evidence that hosts and parasites are often related ( Andersson & Åhlund 2000 ; Roy Nielsen et al. 2006 ; Andersson & Waldeck 2007 ; Waldeck et al. 2008 ; Jaatinen et al. 2009 ; Tiedemann et al. 2011 ). However, this is not always the case ( Semel & Sherman 2001 ; Anderholm et al. 2009 ; and see Pöysa 2004 ). In a new study reported in this issue of Molecular Ecology, Jaatinen et al. (2011a) provide yet another twist to this story that might explain not only why such variable results have been obtained, but also suggests that the games between parasites and their hosts—and the role of kinship in these games—may be even more complex than Andersson (1984) imagined. Indeed, the role of kinship in CBP may be very much one of relative degree!

Table 1. A summary of recent studies that have tested for evidence of relatedness between hosts and parasites in avian conspecific brood parasites

Species	Evidence of host–parasite relatedness?	Evidence of local kin structure?	Relatedness > expected spatially	r Host–Parasite	r Population	Costs or benefits measured?	Method	Source
Common moorhen (Gallinula chloropus)	Mixed Some parasitism between relatives	Yes Limited dispersal of both sexes	No Not greater than expected	—	—	No (but discussed)	DNA minisatellite fingerprints	McRae & Burke (1996 )
Common goldeneye (Bucephala clangula)	Yes Number of parasitic eggs also increased with relatedness	Not tested; high female philopatry	Yes	0.132	—	No	Protein fingerprints 50 bands	Andersson & Åhlund (2000 )
Wood duck (Aix sponsa)	No (parasites avoid relatives)	Not tested; high female philopatry	No Significantly less likely to parasitize local kin	—	—	No	Behavioural observation	Semel & Sherman (2001 )
Common goldeneye (B. clangula)	No Relatedness unlikely to explain CBP	Not tested	Not measured	—	—	Yes	Field measures	Pöysa (2004 )
Wood duck (A. sponsa)	Yes (for primary parasites)	No	Yes (for primary parasites)	0.04 (all) 0.11 (primary parasites)	0.01–0.02	No	5 microsatellites	Roy Nielsen et al. (2006 )
Common eider (Mollissima somateria)	Yes	No	Yes	0.122 (all) 0.126, 0.162 (two colonies)	?0.065 (neighbours 1–10 m)	No	Protein fingerprints 30 bands	Andersson & Waldeck (2007 )
Common eider (M. somateria)	Yes Number of parasitic eggs also increased with relatedness	Yes Relatedness declined with distance	Possibly Host–parasite relatedness > close neighbours in 1 of 2 analyses	0.18–0.21	0.09 (neighbours)	No	Protein fingerprints 51 bands	Waldeck et al. (2008 )
Barnacle goose (Branta llucopsis)	No	Weak Females within 40 m more closely related	No	0.04	?0.0008	No	Protein fingerprints 28 bands	Anderholm et al. (2009 )
Barrow’s goldeneye (Bucephala islandica)	Yes Number of parasitic eggs increased with relatedness	Weak Slight decline in relatedness with distance	No Host–parasite relatedness similar to neighbours	0.08	?0.015 0.11 (neighbours)	No	19 microsatellites	Jaatinen et al. 2009
Common eider (M. somateria)	Yes Interaction with parasite status	No	Yes	0.39 (mean) 0.48, 0.28 (different sites)	0.0	No	7 microsatellites	Tiedemann et al. (2011 )

• CBP, conspecific brood parasitism.

Jaatinen et al.’s (2011a) study highlights several intriguing and as yet not fully resolved issues. First, they confirm results from an earlier study ( Jaatinen et al. 2009 ) showing that relatedness influences conspecific brood parasitism (CBP) in the Barrow’s goldeneye (Bucephala islandica; Fig. 1 ), a species of cavity‐nesting sea duck well known to engage in parasitic egg‐laying ( Eadie 1989 ; Eadie & Fryxell 1992 ). CBP in this species was more frequent among related females that nested in close proximity ( Jaatinen et al. 2009, 2011a ). Female natal philopatry is pronounced in the Barrow’s goldeneye ( Eadie et al. 2000 ), and it is possible the spatial proximity of kin could account for this pattern. However, Jaatinen et al. (2011a) show that relatedness and distance independently affected the extent of parasitism, suggesting that natal philopatry alone cannot provide an explanation. Similar patterns of elevated host–parasite relatedness after controlling for spatial proximity of kin have been reported for other species ( Table 1 ). The novel observation of Jaatinen et al.’s newest study is that the nesting status of the parasite profoundly altered the influence of relatedness on host–parasite interactions. Parasitic females that also had a nest of their own (‘nesting parasites’) increased the number of eggs laid in a host nest with increasing relatedness to the host, whereas parasites without a nest of their own (‘non‐nesting parasites’) did not. Apparently, females within the same population may be using different decision rules with respect to relatedness, and the effects of kinship on CBP may be far more subtle than previously appreciated.

Figure 1 Open in figure viewer PowerPoint A pair of Barrow’s goldeneyes (Bucephala islandica) in central British Columbia. Photo credit: Bruce Lyon.