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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.

SUBMITTER: Martin SH

PROVIDER: S-EPMC6366726 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Recombination rate variation shapes barriers to introgression across butterfly genomes.

Martin Simon H SH Davey John W JW Salazar Camilo C Jiggins Chris D CD

PLoS biology 20190207 2

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, whi ...[more]

PMID: 30730876

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Project description:Recombination is a key molecular mechanism that has profound implications on both micro- and macroevolutionary processes. However, the determinants of recombination rate variation in holocentric organisms are poorly understood, in particular in Lepidoptera (moths and butterflies). The wood white butterfly (Leptidea sinapis) shows considerable intraspecific variation in chromosome numbers and is a suitable system for studying regional recombination rate variation and its potential molecular underpinnings. Here, we developed a large whole-genome resequencing data set from a population of wood whites to obtain high-resolution recombination maps using linkage disequilibrium information. The analyses revealed that larger chromosomes had a bimodal recombination landscape, potentially caused by interference between simultaneous chiasmata. The recombination rate was significantly lower in subtelomeric regions, with exceptions associated with segregating chromosome rearrangements, showing that fissions and fusions can have considerable effects on the recombination landscape. There was no association between the inferred recombination rate and base composition, supporting a limited influence of GC-biased gene conversion in butterflies. We found significant but variable associations between the recombination rate and the density of different classes of transposable elements, most notably a significant enrichment of short interspersed nucleotide elements in genomic regions with higher recombination rate. Finally, the analyses unveiled significant enrichment of genes involved in farnesyltranstransferase activity in recombination coldspots, potentially indicating that expression of transferases can inhibit formation of chiasmata during meiotic division. Our results provide novel information about recombination rate variation in holocentric organisms and have particular implications for forthcoming research in population genetics, molecular/genome evolution, and speciation.

Project description:The data set submitted here contains the raw SNP genotyping data obtained from the analysis of 24 biparental segregating maize (Zea mays L.) populations and their respective parents. The processed and filtered data were used to construct genetic linkage maps which we used in our study of variation of recombination rate in maize. In sexually reproducing organisms, meiotic crossovers ensure the proper segregation of chromosomes and contribute to genetic diversity by shuffling allelic combinations. Such genetic reassortment is exploited in breeding to combine favorable alleles, and in genetic research to identify genetic factors underlying traits of interest via linkage or association-based approaches. Crossover numbers and distributions along chromosomes vary between species, but little is known about their intraspecies variation. In our study, we report on the variation of recombination rates between 22 European maize inbred lines that belong to the Dent and Flint gene pools. We genotyped 23 doubled-haploid populations derived from crosses between these lines with a 50k-SNP array and constructed high-density genetic maps, showing good correspondence with the maize B73 genome sequence assembly. By aligning each genetic map to the B73 sequence, we obtained the recombination rates along chromosomes specific to each population. We identified significant differences in recombination rates at the genome-wide, chromosome, and intrachromosomal levels between populations, as well as significant variation for genome-wide recombination rates among maize lines. Crossover interference analysis using a two-pathway modeling framework revealed a negative association between recombination rate and interference strength. To our knowledge, the present work provides the most comprehensive study on intraspecific variation of recombination rates and crossover interference strength in eukaryotes. Differences found in recombination rates will allow for selection of high or low recombining lines in crossing programs. Our methodology should pave the way for precise identification of genes controlling recombination rates in maize and other organisms. Related publication: Bauer E, Falque M, Walter H, Bauland C, Camisan C, Campo L, Meyer N, Ranc N, Rincent R, Schipprack W, Altmann T, Flament P, Melchinger AE, Menz M, Moreno-González J, Ouzunova M, Revilla P, Charcosset A, Martin OC, Schön C-C (2013) Intraspecific variation of recombination rate in maize. Genome Biology (submitted) We genotyped 2233 maize DH lines from 24 biparental populations, and the 23 parents of these populations using the Illumina MaizeSNP50 BeadChip. We created two large half-sib panels, one each for the Dent and the Flint germplasm. The Dent populations have the prefix CFD, the Flint populations have the prefix CFF. In each panel, a common central parent was crossed to diverse founder lines, and doubled haploids were generated from the respective F1 plants. For a detailed description of the material, see Bauer et al. (2013) Genome Biology (submitted). We submit here three datasets: 1) Dataset Parents comprises all 23 parental lines. 2) Dataset CFD comprises all 1005 DH lines from Dent crosses, 3) Dataset CFF comprises all 1262 DH lines from Flint crosses.

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Dataset Information

Recombination rate variation shapes barriers to introgression across butterfly genomes.

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Recombination rate variation shapes barriers to introgression across butterfly genomes.

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