Genetic and Geographic Variation in Rejection Behavior of Cuckoo Eggs by European Magpie Populations: An Experimental Test of Rejecter-Gene Flow

Abstract

Host responses toward brood parasitism have been shown to differ among populations depending on the duration of sympatry between host and parasite, although populations not currently parasitized show rejection behavior against parasitic eggs. The persistence of rejection behavior in unparasitized host populations and rapid increases of rejection rate in parasitized ones have sometimes been explained as the result of gene flow of rejecter genes from sympatry to allopatry (rejecter-gene flow hypothesis). We present data on the rejection behavior of magpies (Pica pica) the main European host of the great spotted cuckoo (Clamator glandarius), in 15 populations (nine sympatric six allopatric) across their distribution range in Europe. Rejection rates of mimetic and nonmimetic model eggs were significantly higher in sympatric than in allopatric magpie populations, although differences in rejection rate of both mimetic and nonmimetic model eggs between magpie populations were significantly correlated even after controlling tor phylogenetic effects, with differences between sympatric and allopatric magpie populations being larger for mimetic than for nonmimetic model eggs. Differences in rejection of mimetic model eggs were related to both genetic and geographic distances between populations, but differences in rejection rate of nonmimetic model eggs were unrelated to these distances. However, when comparing only sympatric populations, differences in rejection rate of both mimetic and nonmimetic model eggs were related to geographic distances. A multiple autocorrelation analysis revealed that differences among populations in rejection rates of mimetic model eggs had a strong geographic component whereas the main component of rejection rate of nonmimetic model eggs was genetic rather than geographic. These results support the rejecter-gene flow hypothesis. We discuss differences in rejection rates of mimetic and nonmimetic model eggs that suggest the egg-recognition ability of the host is genetically based, but is affected by a learning process for fine tuning of recognition.

Geographic variation in egg ejection rate by great tits across 2 continents

“…However, Møller and Soler (2012) recently reviewed the literature on consistency in host responses to brood parasites and found large intraspecific variation in resistance in several host species (Cruz and Wiley 1989;Nakamura 1990;Soler 1990;Soler and Møller 1990;Briskie et al 1992;Lindholm 1999;Soler, Martínez, et al 1999;Moskát et al 2002;Martín-Gálvez et al 2006Moskát et al 2008;Stokke et al 2008;Avilés et al 2011;Soler et al 2011;Langmore et al 2012). These studies indicate that speciesspecific consistency in resistance is far from the rule.…”

“…Soler, Martínez, et al (1999, 2001 showed for magpie Pica pica hosts that allopatric populations retained significant levels of resistance to cuckoos with this level depending on distance from areas of sympatry. The data that we have analyzed here do not allow for discrimination between the 2 hypothetical mechanisms (see also Thorogood and Davies 2013).…”

“…Second, cuckoos are typically very secretive and hard to detect (Erritzøe et al 2012), and thus our estimates of local cuckoo presence may be imprecise (underestimated). Third, hosts typically show some dispersal and thus their responses in any particular study site (which we sampled) would reflect larger-scale geographical patterns of cuckoo diversity (which we did not sample) (Soler, Martínez, et al 1999). Fourth, brood parasite-host interactions are typically dynamic, with repeated local extinction and recolonization of both parasites and hosts.…”

Host sexual selection and cuckoo parasitism: an analysis of nest size in sympatric and allopatric magpie Pica pica populations parasitized by the great spotted cuckoo Clamator glandarius

“…We used both kinds of eggs because the rejection rate of non-mimetic model eggs has a strong genetic component, whereas the main component of the rejection rate of mimetic model eggs is geographical distance rather than genetic distance (Soler et al 1999b). Thus, while di¡erences in the rejection rate of non-mimetic model eggs provide information on genetic di¡erences between populations of magpies, di¡erences in the rejection rate of mimetic model eggs provide information on the adult migration rates between populations (Soler et al 1999b).…”

“…We used both kinds of eggs because the rejection rate of non-mimetic model eggs has a strong genetic component, whereas the main component of the rejection rate of mimetic model eggs is geographical distance rather than genetic distance (Soler et al 1999b). Thus, while di¡erences in the rejection rate of non-mimetic model eggs provide information on genetic di¡erences between populations of magpies, di¡erences in the rejection rate of mimetic model eggs provide information on the adult migration rates between populations (Soler et al 1999b). In other words, the rejection rates of non-mimetic model eggs could be used as an index of genetic di¡erences between populations in relation to the ability of magpies to recognize dissimilar eggs in their nests, but it could not be directly related to the current impact of brood parasitism on host populations because the rejection rates of non-mimetic model eggs will probably be related to gene £ow due to recognizer individuals from areas of sympatry or allopatry with the great spotted cuckoo (Soler et al 1999b).…”