Abstract
In host–parasite arms races, hosts can evolve signatures of identity to enhance the detection of parasite mimics. In theory, signatures are most effective when within-individual variation is low (‘consistency’), and between-individual variation is high (‘distinctiveness’). However, empirical support for positive covariation in signature consistency and distinctiveness across species is mixed. Here, we attempt to resolve this puzzle by partitioning distinctiveness according to how it is achieved: (i) greater variation within each trait, contributing to elevated ‘absolute distinctiveness’ or (ii) combining phenotypic traits in unpredictable combinations (‘combinatorial distinctiveness’). We tested how consistency covaries with each type of distinctiveness by measuring variation in egg colour and pattern in two African bird families (Cisticolidae and Ploceidae) that experience mimetic brood parasitism. Contrary to predictions, parasitized species, but not unparasitized species, exhibited a negative relationship between consistency and combinatorial distinctiveness. Moreover, regardless of parasitism status, consistency was negatively correlated with absolute distinctiveness across species. Together, these results suggest that (i) selection from parasites acts on how traits combine rather than absolute variation in traits, (ii) consistency and distinctiveness are alternative rather than complementary elements of signatures and (iii) mechanistic constraints may explain the negative relationship between consistency and absolute distinctiveness across species.
Highlights
Whenever antagonistic coevolution involves mimicry as an offence, individuals are under selection to improve their detection of enemies [1,2]
According to a very similar previous analysis [33], differing only with respect to the exact formulation of the linear models used and in applying a more updated phylogenetic tree for phylogenetic least-squares (PGLS) analyses, we found that only combinatorial distinctiveness, and not absolute distinctiveness, was consistently elevated in parasitized over unparasitized species
We found a negative relationship between consistency and absolute distinctiveness that was the same for parasitized and unparasitized species, suggesting that selection from brood parasites favours combinatorial rather than absolute distinctiveness
Summary
Whenever antagonistic coevolution involves mimicry as an offence, individuals are under selection to improve their detection of enemies [1,2]. We previously found that the eggs of host species had consistently elevated combinatorial distinctiveness (reflected by the correlation component of entropy), but not absolute distinctiveness (reflected by the variance component of entropy), compared with the eggs of non-hosts [33] This suggested that selection from brood parasites may act on how hosts deploy phenotypic variation into combinations of trait values, rather than on absolute levels of variation within each metric. As most of these metrics predict egg discrimination in cuckoo finch host species [29], we assumed that they represent biologically relevant metrics on which selection may act We used these metrics to calculate consistency, absolute distinctiveness and combinatorial distinctiveness in colour and pattern for each species, which we analysed in relation to current selection from brood parasites. PGLS models did not include family membership as a fixed effect
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