Recombination rate variation shapes barriers to introgression across butterfly genomes

Abstract

Hybridisation and introgression can dramatically alter the relationships among groups of species, leading to phylogenetic discordance across the genome and between populations. Introgression can also erode species differences over time, but selection against introgression at certain loci acts to maintain postmating species barriers. Theory predicts that species barriers made up of many loci throughout the genome should lead to a broad correlation between introgression and recombination rate, which determines the extent to which selection on deleterious foreign alleles will affect neutral alleles at physically linked loci. Here, we describe the variation in genealogical relationships across the genome among three species of Heliconius butterflies: H. melpomene (mel), H. cydno (cyd), and H. timareta (tim), using whole genomes of 92 individuals, and ask whether this variation can be explained by heterogeneous barriers to introgression. We find that species relationships vary predictably at the chromosomal scale. By quantifying recombination rate and admixture proportions, we then show that rates of introgression are predicted by variation in recombination rate. This implies that species barriers are highly polygenic, with selection acting against introgressed alleles across most of the genome. In addition, long chromosomes, which have lower recombination rates, produce stronger barriers on average than short chromosomes. Finally, we find a consistent difference between two species pairs on either side of the Andes, which suggests differences in the architecture of the species barriers. Our findings illustrate how the combined effects of hybridisation, recombination, and natural selection, acting at multitudes of loci over long periods, can dramatically sculpt the phylogenetic relationships among species.

Massive postglacial gene flow between European white oaks uncovered genes underlying species barriers

“…S6). This finding is consistent with the increasing numbers of reports of a correlation between the recombination rate and the rates of introgression, for example in the house mouse (Janoušek et al ., ), in Mimulus monkey flowers (Aeschbacher et al ., ), in Heliconius butterflies (Martin et al ., ) or in humans (Juric et al ., ) and expected to be due to the variation of linkage to introgressed deleterious alleles (background selection, Charlesworth et al ., ). The recent report of a markedly high rate of deleterious mutations relative to 28 other plant species (Plomion et al ., ) highlighted the putative role of deleterious mutations in shaping the genomic landscape of species differentiation in oaks.…”

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

“…Genomic differentiation across hybrid zones in Müllerian mimetic butterflies have mostly been documented in the genus Heliconius . While Heliconius subspecific lineages sometimes exhibit high genome‐wide differentiation across hybrid zones (Martin, Davey, Salazar, & Jiggins, 2019; Van Belleghem et al, 2018), this appears not to be the case in the Tarapoto suture zone. In this region, Nadeau et al (2014) found that in phenotypically differentiated lineages of H. erato and H. melpomene only loci around pattern gene loci showed genetic differentiation, while the rest of the genome was highly permeable to gene flow, with F ST values ranging from 0.0112 to 0.0280 (see also Martin et al, 2013).…”

Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels

“…They are therefore expected to be incompatible at a high number of differentiated sites (Simon et al, 2018). With such a highly polygenic determinism of post-zygotic selection one expect a correlation between recombination rates and introgression (Barton & Bengtsson, 1986), which has recently been observed in multiple study systems (Mimulus, Aeschbacher, Selby, Willis, and Coop, 2017; sea bass, Duranton et al, 2018;oyster, Gagnaire et al, 2018;stickleback, Roesti, Moser, and Berner, 2013;swordtail fish, Schumer et al, 2018 or Heliconius, Martin, Davey, Salazar, andJiggins, 2019). While patterns of hybridisation are strongly repeatable when the same M. galloprovincialis lineages are involved, equally notable is the lack of repeatability with different lineages.…”