Natural Selection and Genetic Diversity in the Butterfly Heliconius melpomene

Abstract

A combination of selective and neutral evolutionary forces shape patterns of genetic diversity in nature. Among the insects, most previous analyses of the roles of drift and selection in shaping variation across the genome have focused on the genus Drosophila. A more complete understanding of these forces will come from analyzing other taxa that differ in population demography and other aspects of biology. We have analyzed diversity and signatures of selection in the neotropical Heliconius butterflies using resequenced genomes from 58 wild-caught individuals of Heliconius melpomene and another 21 resequenced genomes representing 11 related species. By comparing intraspecific diversity and interspecific divergence, we estimate that 31% of amino acid substitutions between Heliconius species are adaptive. Diversity at putatively neutral sites is negatively correlated with the local density of coding sites as well as nonsynonymous substitutions and positively correlated with recombination rate, indicating widespread linked selection. This process also manifests in significantly reduced diversity on longer chromosomes, consistent with lower recombination rates. Although hitchhiking around beneficial nonsynonymous mutations has significantly shaped genetic variation in H. melpomene, evidence for strong selective sweeps is limited overall. We did however identify two regions where distinct haplotypes have swept in different populations, leading to increased population differentiation. On the whole, our study suggests that positive selection is less pervasive in these butterflies as compared to fruit flies, a fact that curiously results in very similar levels of neutral diversity in these very different insects.

No evidence for maintenance of a sympatricHeliconiusspecies barrier by chromosomal inversions

“…2016). The remaining 463 split read candidate inversions from the four samples were merged into 185 candidate groups based on their overlaps.…”

“…Furthermore, this is only slightly larger than the distance at which linkage disequilibrium in H. melpomene reaches background levels (∼10 kb; Martin et al. 2016), such that any effect of reduced recombination would be slight in population genetic terms. We conclude that there are a small number of likely species‐specific inversions, but that these are too small to play a role in speciation via reduced recombination.…”

“…Indeed, we can find no compelling fixed candidate inversions supported by both the split read and trio assembly datasets that also show evidence of an increase in F ST or d XY , except for the 11.7 kb inversion shown in Figure S11.4, which is probably too small to substantially increase linkage across this locus beyond that expected by normal decay of linkage disequilibrium (Martin et al. 2016). It is possible that some of the candidates with less robust evidence are genuine, given the limitations described above, but on the existing evidence we cannot identify any inversions that are likely to be involved in maintaining species barriers between H. melpomene and H. cydno .…”

“…Finally, candidates shorter than 1 kb were rejected, as linkage disequilibrium between SNPs separated by 1 kb or less in H. melpomene is significantly higher than background levels (Martin et al. 2016) and so inversions below this size are unlikely to be required to maintain linkage. The retained inversion candidates were then combined into groups by overlap.…”

A survey of methods and tools to detect recent and strong positive selection

“…More advanced methods that rely on the CLR test (e.g., SweepFinder [16], SweepFinder2 [56], and SweeD [17]) or on patterns of LD (e.g., OmegaPlus [18, 57]), perform a window-size optimization approach that provides information on the genomic region affected by a selective sweep at the cost of increased execution times. The aforementioned methods have been widely used to detect recent and strong positive selection in a variety of eukaryotic or prokaryotic organisms, such as human [16, 58, 59], D. melanogaster [60–63], lizards [64], rice [65], butterflies [66], and bacteria [67]. …”