Abstract
The existence of a coevolutionary process between avian brood parasites and their hosts predicts a lower intra-clutch variation in egg appearance of host eggs among rejecters as this would favor egg discrimination of parasite eggs by hosts once parasitic egg mimicry had evolved. So far empirical tests of this prediction have ignored the fact that different aspects of host egg phenotypes may differ in the relative role of environmental vs. genetic determination, and hence that the role of intra-clutch variation in egg rejection within a population cannot be invariant. Here, we estimated whether the intra-clutch variation in several aspects of host eggshell features is consistently associated to rejection of parasitic foreign eggs across years in a magpie host population parasitized by great spotted cuckoos. We innovatively estimated spottiness by means of the fractal dimension of eggs, which considers the homogeneity of spot pattern complexity in eggshells. Our results show that low intra-clutch variation in the blue-green coloration at the middle area of the eggs associated with a high chance of rejection, but only in one of the 3 years we conducted the study. In addition, females that rejected foreign eggs presented more homogenous spot patterns in their clutches as estimated by their fractal dimension than females that accepted experimental eggs, independently of the year of study. Finally, intra-clutch variation in egg volume of host eggs was not associated to rejection. Analyses at the individual level revealed that the relative role of genetic vs. environmental factors that determine egg phenotype would be feature-specific in magpies, females having a characteristic spottiness, but not color or volume, pattern. Our work stresses the importance of considering a holistic approach including several aspects of variation in host egg phenotype (size, color, and homogeneity of spot pattern), as some aspects might be more susceptible to selection through egg rejection than others, presumably because they are less influenced by variation in the environmental conditions. Moreover, our study highlights the importance of replication in studies on the adaptive value of host traits in egg rejection.
Highlights
Avian brood parasites impose dramatic costs on the reproductive success of their hosts, which has led to the evolution of counteradaptations to circumvent them (Rothstein, 1990; Davies, 2000)
Our results show a clear, consistent relationship between intraclutch variation in magpie egg phenotype and the probability of egg rejection by females
Victoria (1972) proposed that high homogeneity in the appearance of host eggs could be under strong selection in parasitized host populations because it would make easier the detection of noticeable features of parasite eggs by comparison of hosts own eggs with foreign ones (Øien et al, 1995; Soler and Møller, 1996)
Summary
Avian brood parasites impose dramatic costs on the reproductive success of their hosts, which has led to the evolution of counteradaptations to circumvent them (Rothstein, 1990; Davies, 2000). Once brood parasites have evolved eggs that mimic those of their hosts, a further step in the arms race would be the evolution of a smaller degree of intra-clutch variation in the appearance of host eggs, as this could facilitate hosts to discriminate parasitic eggs (Victoria, 1972; Øien et al, 1995; Soler and Møller, 1996; Moskát et al, 2008). After more than two decades of empirical work examining the key prediction of this hypothesis (the intra-clutch variation hypothesis) in different host-brood parasite systems, the literature is equivocal regarding whether homogeneity in host egg appearance favors or not the discrimination of parasitic egg. Some studies have shown that females with lower intra-clutch variation were more likely to reject artificial foreign eggs as it would be expected (Stokke et al, 1999; Soler et al, 2000; Peer et al, 2010; Wang et al, 2016), but others found the opposite trend (Lotem et al, 1995; Avilés et al, 2004). Discrepancy in the pattern arises when the eggs used in experiments were conspecific or real cuckoo eggs (Procházka and Honza, 2003; Moskát and Lovászi, 2004; Stokke et al, 2004; Cherry et al, 2007; Landstrom et al, 2010; Polaciková et al, 2011; Abernathy and Peer, 2014)
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