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The evolution of alternative parasitic life histories in large blue butterflies

Abstract

Large blue (Maculinea) butterflies are highly endangered throughout the Palaearctic region, and have been the focus of intense conservation research1,2,3. In addition, their extraordinary parasitic lifestyles make them ideal for studies of life history evolution. Early instars consume flower buds of specific host plants, but later instars live in ant nests where they either devour the brood (predators), or are fed mouth-to-mouth by the adult ants (cuckoos). Here we present the phylogeny for the group, which shows that it is a monophyletic clade nested within Phengaris, a rare Oriental genus whose species have similar life histories4,5. Cuckoo species are likely to have evolved from predatory ancestors. As early as five million years ago, two Maculinea clades diverged, leading to the different parasitic strategies seen in the genus today. Contrary to current belief, the two recognized cuckoo species show little genetic divergence and are probably a single ecologically differentiated species6,7,8,9,10. On the other hand, some of the predatory morphospecies exhibit considerable genetic divergence and may contain cryptic species. These findings have important implications for conservation and reintroduction efforts.

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Figure 1: Phylogeny of the obligately parasitic genera Phengaris and Maculinea in relation to outgroup taxa that have facultative, mutualistic relationships with ants.
Figure 2: Phylogeny of Maculinea taxa with Phengaris as outgroup.

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Acknowledgements

We thank S. Aoki, S. C. Collins, J. T. Costa, J. Dantart, A. V. Dantchenko, H. Deng, V. Dinca, K. Dunn, G. W. Elmes, K. Emura, E. Figurny-Puchalska, M. Goia, D. Hsu, H.-C. Huang, T. Inomata, Y.-J. Jang, J. L. Jean, J. Jubany, U. Kurosu, D. J. Lohman, V. A. Lukhtanov, T. Mizusawa, P. S. Nielsen, M. Owada, R. Rougerie, A. Shapiro, C. Stefanescu, H. Sugiyama, M. W. Tan, J. A. Thomas, M. A. Travassos, S. Viader, J. C. Wardlaw, S. Yamaguchi and D. Zitnan for providing material. D. K. Aanen, R. Eastwood, B. D. Farrell, G. E. Morse, D. B. Rand, J. A. Thomas, A. S. Sequeira and P. Villesen gave suggestions and comments, and P. Ackery allowed us to use images from the BMNH. Support for this research was provided by a National Science Foundation grant to N.E.P., a Danish Natural Science Research council grant to J.J.B., a Fulbright Postdoctoral Fellowship to R.V., grants from the Putnam Expeditionary Fund of the Museum of Comparative Zoology to N.E.P., N.P.K. and R.V., the Natural Conservation Foundation, Council of Agriculture and National Science Council, Taiwan, R.O.C. to Y.F.H., a PhD student fellowship from Harvard's Department of Organismic and Evolutionary Biology to N.P.K., a PhD student fellowship from the University of Aarhus to T.D.A., and the EU RTD network ‘MacMan’.

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Correspondence to Naomi E. Pierce.

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Supplementary Information

This text contains Supplementary Methods, including Taxon and outgroup sampling, DNA extraction and sequencing, phylogenetic analysis. In addition, the file contains Supplementary Results, including character and tree statistics, tree reconstruction (maximum parsimony, Bayesian and maximum likelihood), sequence divergences, dating, ancestral character reconstruction (host plants, parasitic strategies), host ant specificity, systematic conclusions and butterfly information. The entire file also contains ten Supplementary Tables and nine Supplementary Figures). (PDF 585 kb)

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Als, T., Vila, R., Kandul, N. et al. The evolution of alternative parasitic life histories in large blue butterflies. Nature 432, 386–390 (2004). https://doi.org/10.1038/nature03020

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