Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing

Abstract

Heliconius butterflies represent a recent radiation of species, in which wing pattern divergence has been implicated in speciation. Several loci that control wing pattern phenotypes have been mapped and two were identified through sequencing. These same gene regions play a role in adaptation across the whole Heliconius radiation. Previous studies of population genetic patterns at these regions have sequenced small amplicons. Here, we use targeted next-generation sequence capture to survey patterns of divergence across these entire regions in divergent geographical races and species of Heliconius. This technique was successful both within and between species for obtaining high coverage of almost all coding regions and sufficient coverage of non-coding regions to perform population genetic analyses. We find major peaks of elevated population differentiation between races across hybrid zones, which indicate regions under strong divergent selection. These 'islands' of divergence appear to be more extensive between closely related species, but there is less clear evidence for such islands between more distantly related species at two further points along the 'speciation continuum'. We also sequence fosmid clones across these regions in different Heliconius melpomene races. We find no major structural rearrangements but many relatively large (greater than 1 kb) insertion/deletion events (including gain/loss of transposable elements) that are variable between races.

Genomic divergence during speciation: causes and consequences

“…The contribution to this theme issue by Nadeau et al [32] on genomic divergence among hybridizing Heliconius butterflies further illustrates the points exemplified by the Rhagoletis study. Nadeau et al…”

“…Elucidating the specific targets of divergent selection in the first place, and distinguishing them from neutral regions that simply hitchhike to divergence, is a difficult task. The focused sequencing of gene regions implicated in colour-pattern diversification of Heliconius butterflies demonstrates how steps in the direction towards finding the specific targets of selection can be made [32]. Once the specific targets of selection are determined, work can then focus on the consequences for neutral regions linked and unlinked to the selected ones.…”

“…For example, the inverted chromosomal regions described by McGaugh & Noor [31] contain genes causing intrinsic dysfunctions in hybrids between species of Drosophila. In addition, regions containing loci involved in divergent adaptation, which thus likely cause extrinsic selection against migrants and hybrids, have been described in several systems, including those in this issue [25,32,33]. Nonetheless, even in such examples, it remains unknown how the specific patterns of divergence and genetic architecture observed truly promoted or constrained the evolution of reproductive isolation.…”

Transitions between phases of genomic differentiation during stick-insect speciation

“…Specifically, there are some 50 migrants per generation (Nem) in populations found in the same 17 locality and ~5-10 Nem in populations separated by 1-10 kilometres (km) 13,39 . As in most other 18 systems 1,2 , the dynamics of speciation from its onset to end are unresolved.…”

“…The data set includes all the Californian sexual species of 16 Timema (the others are found outside California). We extracted DNA and prepared libraries for 17 GBS sequencing of all these individuals, as in previous work 39 .…”