Butterfly genetic theft

The Heliconius butterfly genome paper [1] is supercool for many reasons. Most important from my point of view is the attention to introgression among the different species of these South American butterflies.

The Heliconius reference genome allowed us to perform rigorous tests for introgression among melpomene–silvaniform clade species. We used RAD resequencing to reconstruct a robust phylogenetic tree based on 84 individuals of H. melpomene and its relatives, sampling on average 12 Mb, or 4%, of the genome (Fig. 1a and Supplementary Information, sections 12–18). We then tested for introgression between the sympatric co-mimetic postman butterfly races of Heliconius melpomene amaryllis and H. timareta ssp. nov. (Fig. 1) in Peru, using ‘ABBA/BABA’ single nucleotide sites and Patterson’s D-statistics (Fig. 3a), originally developed to test for admixture between Neanderthals and modern humans 21, 22 (Supplementary Information, section 12). Genome-wide, we found an excess of ABBA sites, giving a significantly positive Patterson’s D of 0.037 ± 0.003 (two-tailed Z-test for D = 0, P = 1 × 10−40), indicating greater genome-wide introgression between the sympatric mimetic taxa H. melpomene amaryllis and H. timareta ssp. nov. than between H. melpomene aglaope and H. timareta ssp. nov., which do not overlap spatially (Fig. 1b). On the basis of these D-statistics, we estimate that 2–5% of the genome was exchanged between H. timareta and H. melpomene amaryllis, to the exclusion of H. melpomene aglaope. (Supplementary Information, section 12). Exchange was not random. Of the 21 chromosomes, 11 have significantly positive D-statistics, and the strongest signals of introgression were found on the two chromosomes containing known mimicry loci B/D and N/Yb (Fig. 3b and Supplementary Information, section 15).

The paper goes on to demonstrate that color patterning genes have introgressed preferentially in cases where one geographically variable species mimics the local variants of another. Mimicry in these butterflies amounts to genetic theft, pure and simple.

I'll point out that the introgression of 2% of the genome is not a small amount. In the case of these butterflies, introgressed regions are clustered in particular areas, and some of them appear to have happened under the influence of selection (adaptive introgression). Still, there must be some strong reinforcement selection keeping the "species" reproductively separate enough to maintain their gene pools in the face of large-scale sympatric hybridization. Either that, or the current pattern is really a temporary snapshot of a longer, dynamic process of population dispersal and introgression.

There's also a section describing the extent of the chemosensory genes in butterflies, which have more than moths (34 compared to 23) despite their diurnality and greater reliance on visual cues. Funny to read of these being the most complicated insect olfaction systems yet known, considering the hundreds of olfactory receptors in mammalian genomes (UPDATE 2012-05-17: the paper refers to odorant-binding and chemosensory families, which are a subset of the total olfaction system [2]).

References