Abstract
Although exceptional examples of adaptation are frequently celebrated, some outcomes of natural selection seem far from perfect. For example, many hoverflies (Diptera: Syrphidae) are harmless (Batesian) mimics of stinging Hymenoptera. However, although some hoverfly species are considered excellent mimics, other species bear only a superficial resemblance to their models and it is unclear why this is so. To evaluate hypotheses that have been put forward to explain interspecific variation in the mimetic fidelity of Palearctic Syrphidae we use a comparative approach. We show that the most plausible explanation is that predators impose less selection for mimetic fidelity on smaller hoverfly species because they are less profitable prey items. In particular, our findings, in combination with previous results, allow us to reject several key hypotheses for imperfect mimicry: first, human ratings of mimetic fidelity are positively correlated with both morphometric measures and avian rankings, indicating that variation in mimetic fidelity is not simply an illusion based on human perception; second, no species of syrphid maps out in multidimensional space as being intermediate in appearance between several different hymenopteran model species, as the multimodel hypothesis requires; and third, we find no evidence for a negative relationship between mimetic fidelity and abundance, which calls into question the kin-selection hypothesis. By contrast, a strong positive relationship between mimetic fidelity and body size supports the relaxed-selection hypothesis, suggesting that reduced predation pressure on less profitable prey species limits the selection for mimetic perfection.
Highlights
Much of evolutionary theory relating to mimicry has been based on the assumption that the fidelity of mimicry in any given system is extremely high
Meta-analysis of 11 independent studies (Table S1) demonstrated no evidence of a strong correlation between relative abundance and either measure of mimetic fidelity in our 38 focal species, either before controlling for phylogenetic autocorrelation (fidelityHR: r-bar = 0.065; fidelityMD: r-bar = 0.001) or after controlling for phylogeny using phylogenetic generalised least squares regression (PGLS) for a subset of 31 species (Figure 3) (fidelityHR: r-bar = -0.083; fidelityMD: r-bar = 0.223)
Our revelation of a strong positive relationship between body size and mimetic fidelity is readily explained if body size influences predation behaviour and thereby the intensity of selection for more perfect mimicry
Summary
Exceptional examples of adaptation are frequently celebrated, some outcomes of natural selection appear far from perfect and it is important to establish why this is so. We use a comparative approach to evaluate a series of largely untested hypotheses that have been put forward to explain inter-specific variation in the mimetic fidelity of Palearctic Syrphidae. The degree of mimetic perfection was quantified for each of 38 syrphid species using both human and multivariate morphometric rankings. In combination with previous results, allow us to reject several key hypotheses for imperfect mimicry: (i) human ratings of mimetic fidelity are positively correlated with both morphometric measures and avian rankings, indicating that variation in mimetic fidelity is not an illusion based on human perception 3, (ii) no species of syrphid maps out in multi-dimensional space as intermediate in appearance between several different hymenopteran model spe. -model hypothesis 4 requires, and (iii) we demonstrate no evidence for a negative relationship between mimetic fidelity and abundance, which calls into question the "kin selection" 5 hypothesis.
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