Classic and introgressed selective sweeps shape mimicry loci across a butterfly adaptive radiation

Abstract

Natural selection leaves distinct signatures in the genome that can reveal the targets and history of adaptive evolution. By analysing high-coverage genome sequence data from four major colour pattern loci sampled from nearly 600 individuals in 53 populations, we show pervasive selection on wing patterns across the Heliconius adaptive radiation. The strongest signatures correspond to loci with the greatest phenotypic effects, consistent with visual selection by predators, and are found in colour patterns with geographically restricted distributions. These recent sweeps are similar between co-mimics and indicate colour pattern turn-over events despite strong stabilizing selection. Using simulations we compare sweep signatures expected under classic hard sweeps with those resulting from adaptive introgression, an important aspect of mimicry evolution in Heliconius. Simulated recipient populations show a distinct 'volcano' pattern with peaks of increased genetic diversity around the selected target, consistent with patterns found in some populations. Our genomic data provide unprecedented insights into the recent history of selection across the Heliconius adaptive radiation.

Ancestral hybridisation facilitated species diversification in the Lake Malawi cichlid fish adaptive radiation

“…A clear message from the increasing number of genomic investigations of non-model organisms is that hybridisation between related species is far more common than previously thought, leading to fundamentally reticulate patterns of evolution, where species relationships are represented by networks rather than trees. In many cases it has been shown that this process can transport selectively favourable alleles between species and thus contribute to adaptation (Herman et al 2018;Suarez-Gonzalez et al 2018;Walsh et al 2018;Moest et al 2019) . However, the effect of such hybridisation events on biological diversification, that is, whether it increases or reduces the rate at which new species emerge over time is not generally understood.…”

Deep Convergence, Shared Ancestry, and Evolutionary Novelty in the Genetic Architecture of Heliconius Mimicry

“…These butterflies appear to have a flexible toolkit of cis-regulatory enhancers (Wallbank et al 2016;Van Belleghem et al 2017) through which gene expression changes can rapidly alter phenotypes and drive adaptive evolution (Wray 2007); with a single mutation at an enhancer potentially enough to have major phenotypic effects (Chan et al 2010;Frankel et al 2012). Such genetic architecture combined with introgression can facilitate adaptive evolution through the swapping of these enhancers among lineages of Heliconius (Wallbank et al 2016;Moest et al 2019;Lewis and Belleghem 2020). For example, the evidence suggests that the ancestral sources of the ray and dennis elements were different, with the rays phenotype originating in the H. melpomene clade and the dennis phenotype originating in the silvaniform clade, before being brought together as the dennis-rayed phenotype in both H. melpomene and H. elevatus (Wallbank et al 2016).…”

“…The small number of mimicry genes controlling a majority of the colour pattern elements have been identified across Heliconius species using a combination of QTL mapping, genome-wide association studies across colour pattern hybrid zones, and gene expression studies. Across multiple species, parallel genetic evolution at the genes optix, cortex and WntA is known to control red-orange pattern elements (Baxter et al 2008;Reed et al 2011;Martin et al 2014;Huber et al 2015;Lewis et al 2019), white and yellow pattern elements (Nadeau et al 2016), and melanic patterning (Martin et al 2012;Gallant et al 2014;Mazo-Vargas et al 2017;Moest et al 2019;Morris et al 2019;Van Belleghem et al 2020) respectively.…”