Why many Batesian mimics are inaccurate: evidence from hoverfly colour patterns

Abstract

Mimicry is considered a classic example of the elaborate adaptations that natural selection can produce, yet often similarity between Batesian (harmless) mimics and their unpalatable models is far from perfect. Variation in mimetic accuracy is a puzzle, as natural selection should favour mimics that are hardest to distinguish from their models. Numerous hypotheses exist to explain the persistence of inaccurate mimics, but most have rarely or never been tested against empirical observations from wild populations. One reason for this is the difficulty in measuring pattern similarity, a key aspect of mimicry. Here, we use a recently developed method, based on the distance transform of binary images, to quantify pattern similarity both within and among species for a group of hoverflies and their hymenopteran models. This allowed us to test three key hypotheses regarding inaccurate mimicry. Firstly, we tested the prediction that selection should be more relaxed in less accurate mimics, but found that levels of phenotypic variation are similar across most hoverfly species. Secondly, we found no evidence that mimics have to compromise between accuracy to multiple model species. However, we did find that darker-coloured hoverflies are less accurate mimics, which could lead to a trade-off between mimicry and thermoregulation in temperate regions. Our results shed light on a classic problem concerning the limitations of natural selection.

Mapping the evolution of accurate Batesian mimicry of social wasps in hoverflies

“…In all our analyses, wing length was a good predictor of wasp mimicry (Tables 1 and 2). Larger species were typically better wasp mimics, which corresponds with experimental results and theoretical hypotheses from previous papers (Penney et al 2012;Taylor et al 2016a). There may be greater selection pressure on larger hoverflies to deceive predator visual systems because they are more nutritionally profitable prey items (Penney et al 2012).…”

“…The abdomen was used for analysis because the color pattern is, in general, much more distinctive and variable on the abdomen than on the thorax in dipterans and hymenopterans (Marchini et al 2017), and the abdomen is typically conspicuous to potential predators. Studies have previously shown that abdominal color patterns of both hoverflies and wasps consist of clearly delineated contrasts in both achromatic and chromatic dimensions, and do not contain hidden ultraviolet signals (Taylor et al 2016b), meaning that the spatial elements of the pattern are visible to all but the most primitive of visual systems.…”

Geographic variation in mimetic precision among different species of coral snake mimics

“…Alternatively, C. coccinea might fail to show mimicry on the edge if there is a selective trade‐off between mimicry and thermoregulation: mimics that occur at higher latitudes might need more black coloration to achieve optimal body temperatures more rapidly (as in hoverflies; see Taylor et al ., ). Contrary to this expectation, however, all snake species – both mimics and models – either had less black on their patterns at higher latitudes or did not vary significantly with latitude (Fig.…”

“…How general our results will prove to be beyond coral snake mimics is uncertain. Most studies of variation in mimetic precision in insects have examined variation between species (Penney et al, 2012;Taylor et al, 2013;Wilson et al, 2013;Taylor et al 2016b). The few studies that have examined variation in mimetic precision within species in insects (Iserbyt et al, 2011) and other vertebrates (Kraemer et al, 2015) did not examine multiple mimic species.…”

Multiple models generate a geographical mosaic of resemblance in a Batesian mimicry complex

“…For example, Darst & Cummings [14] found that a poison frog mimic that co-occurs with two poison frog models only resembled a single model well. Similarly, Penney et al [64] and Taylor et al [65] failed to find any evidence that hoverfly mimics were intermediate in phenotype between different model wasp and bee species.…”