Multilocus Species Trees Show the Recent Adaptive Radiation of the Mimetic Heliconius Butterflies

Abstract

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.

Species specificity and intraspecific variation in the chemical profiles of Heliconius butterflies across a large geographic range

“…Heliconius butterflies represent a continental‐scale adaptive radiation (Kozak et al, 2015). Speciation in this group is often associated with divergence in wing color pattern, and pattern variation plays an important role in speciation and mate preference (Jiggins, 2008; Jiggins et al, 2001; Merrill et al, 2011, 2015, 2019; Sánchez et al, 2015).…”

“…See Table A1 in Appendix for sample numbers. The phylogeny was previously published by Kozak et al (2015)…”

“…An interspecific genetic distance matrix was constructed using the function “cophenetic.phylo” from the ape package (Paradis & Schliep, 2018) with a previously published phylogeny (Kozak et al, 2015). Geographic distance matrices were created by inputting the coordinates of collection localities into the function “distm” in the geosphere package to calculate the Haversine great‐circle distance between points (Hijmans, 2017).…”

“…To investigate the role of geographic distance in chemical profile divergence, we compared geographic and chemical distances matrices, controlling for genetic distance, with partial Mantel tests. To visualize the species phylogeny (Kozak et al, 2015), we used the “plot.phylo” function from the ape package (Paradis & Schliep, 2018).…”

Contrasting genomic and phenotypic outcomes of hybridization between pairs of mimetic butterfly taxa across a suture zone

“…Mimicry generates postzygotic reproductive isolation via higher predation on intermediate‐patterned, nonmimetic hybrids (Merrill et al, 2012) and prezygotic reproductive isolation if there is also assortative mating for colour pattern among subspecies (Jiggins, Naisbit, Coe, & Mallet, 2001; McClure et al, 2019; Merrill et al, 2011, 2012). Mimicry is therefore a strong ecological driver of speciation, and is believed to have triggered the diversification of large radiations of heliconiine and ithomiine butterflies (Jiggins et al, 2001; Kozak et al, 2015). Studies of genetic differentiation and the basis of colour pattern variation in mimetic butterflies have almost exclusively focused on heliconiine butterflies (particularly the genus Heliconius ), where a few major‐effect genes (dubbed the mimicry “toolkit” [Joron et al, 2006]) have been found to control wing pattern variation (Martin et al, 2012; Mazo‐Vargas et al, 2017; Nadeau et al, 2016; Reed et al, 2011; Westerman et al, 2018) and to be highly differentiated across hybrid zones, while the rest of the genome seems highly permeable (Nadeau et al, 2014).…”