Multilocus species trees show the recent adaptive radiation of the mimetic heliconius butterflies

Abstract

Müllerian mimicry among Neotropical Heliconiini butterflies is an excellent example of natural selection, associated with the diversification of a large continental-scale radiation. Some of the processes driving the evolution of mimicry rings are likely to generate incongruent phylogenetic signals across the assemblage, and thus pose a challenge for systematics. We use a data set of 22 mitochondrial and nuclear markers from 92% of species in the tribe, obtained by Sanger sequencing and de novo assembly of short read data, to re-examine the phylogeny of Heliconiini with both supermatrix and multispecies coalescent approaches, characterize the patterns of conflicting signal, and compare the performance of various methodological approaches to reflect the heterogeneity across the data. Despite the large extent of reticulate signal and strong conflict between markers, nearly identical topologies are consistently recovered by most of the analyses, although the supermatrix approach failed to reflect the underlying variation in the history of individual loci. However, the supermatrix represents a useful approximation where multiple rare species represented by short sequences can be incorporated easily. The first comprehensive, time-calibrated phylogeny of this group is used to test the hypotheses of a diversification rate increase driven by the dramatic environmental changes in the Neotropics over the past 23 myr, or changes caused by diversity-dependent effects on the rate of diversification. We find that the rate of diversification has increased on the branch leading to the presently most species-rich genus Heliconius, but the change occurred gradually and cannot be unequivocally attributed to a specific environmental driver. Our study provides comprehensive comparison of philosophically distinct species tree reconstruction methods and provides insights into the diversification of an important insect radiation in the most biodiverse region of the planet.

Keywords: Amazonia; Lepidoptera; Miocene; diversification rate; incongruence; mimicry; multispecies coalescent.

Figure 1.

a) Bayesian phylogeny of 71 out of 77 butterflies in the tribe Heliconiini with outgroups, estimated using 20 nuclear and 2 mitochondrial markers with an uncorrelated molecular clock method (BEAST). The age of the root is calibrated based on the results of Wahlberg et al. (2009) and the bars signify the 95% credible intervals around the mean node ages. Scale axis in Ma. Deep splits are shown within the well-studied H. erato and H. melpomene. Heliconiini exhibit complex patterns of divergence and convergence in aposematic wing patterns, top to bottom: Actinote latior (outgroup), P. telesiphe telesiphe, Philaethria dido chocoensis, Dione juno, Eueides tales michaeli, Eueides lampeto lampeto, Heliconius telesiphe telesiphe, H. erato favorinus, Heliconius demeter ucayalensis, H. sara sara, H. aoede cupidineus, H. doris (blue morph), H. burneyi jamesi, H. melpomene amaryllis, H. timareta contigua, H. numata lyrcaeus, and H. pardalinus dilatus. b) The mean phylorate plot from the BAMM analysis. Net diversification rate is averaged across 2000 models fitted to the MCC chronogram. Colors from blue to red indicate the range of diversification rates from 0.2 to 0.4 new lineages per lineage per million years. $X$axis in millions of years ago. Photos © C. Jiggins, M. Joron and L. Constantino.

Figure 2.

Whole mitochondrial ML (RAxML) phylogeny of the genus Heliconius. Bootstrap support values indicated. Scale bar in units of substitution per site per million years.

Figure 3.

A phylogenetic hypothesis for Heliconius showing the extent of concordance between tree topologies of the 21 loci estimated by BCA in BUCKy. Dots indicate the CF values for the nodes, with darker shades of gray corresponding to lower support values.