A comparative analysis of the evolution of imperfect mimicry

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 (Batesian1) mimics of stinging Hymenoptera2. However, although some hoverfly species are considered excellent mimics, other species bear only a superficial resemblance to their models3 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 perception4; second, no species of syrphid maps out in multidimensional space as being intermediate in appearance between several different hymenopteran model species, as the multimodel hypothesis5 requires; and third, we find no evidence for a negative relationship between mimetic fidelity and abundance, which calls into question the kin-selection6 hypothesis. By contrast, a strong positive relationship between mimetic fidelity and body size supports the relaxed-selection hypothesis7,8, suggesting that reduced predation pressure on less profitable prey species limits the selection for mimetic perfection.

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Figure 1: GCDA plot of biometrical measurements.
Figure 2: The relationship between Mahalanobis distances ( f MD ) and human rankings ( f HR ) measures of mimetic fidelity in hoverflies.
Figure 3: Phylogenetic relationships between the 31 hoverfly species (Diptera: Syphidae) for which fidelity and body-size data exist.
Figure 4: Relationship between body size (estimated as −PC1) and two measures of mimetic fidelity.

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Acknowledgements

We thank W. Knee for help with the Bayesian analysis, and R. Laird, G. Ruxton and M. Speed for comments on the manuscript. The human aspect of this research was approved by the Carleton University Research Ethics Committee and conducted according to the guidelines set out in the Tri-Council Policy Statement on Ethical Conduct for Research Involving Humans; subjects gave informed consent. The work was supported by grants to T.N.S. from the Natural Sciences and Engineering Research Council of Canada (NSERC), the Canada Foundation for Innovation and the Ontario Innovation Trust, and to J.H.S. from Agriculture and Agri-Food Canada, the Canadian Centre for DNA Barcoding and NSERC Canpolin. C.H. was supported by an Ontario MRI Fellowship.

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H.D.P. photographed and measured specimens, and collected data on human rankings. J.H.S. provided the novel molecular phylogeny. C.H. analysed the data. C.H., K.R.A. and T.N.S. wrote the paper. T.N.S. conceived the project. All authors discussed the results and provided comments on the manuscript.

Corresponding author

Correspondence to Thomas N. Sherratt.

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The authors declare no competing financial interests.

Additional information

All newgenetic sequences are deposited inGenBank andare listed in Supplementary Table 4.

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This file contains Supplementary Figures 1-6, Supplementary Tables 1-4, a Supplementary Discussions and additional references. (PDF 5796 kb)

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Penney, H., Hassall, C., Skevington, J. et al. A comparative analysis of the evolution of imperfect mimicry. Nature 483, 461–464 (2012). https://doi.org/10.1038/nature10961

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