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.
Coloration is an easily quantifiable visual trait that has proven to be a highly tractable system for genetic analysis and for studying adaptive evolution. The application of genomic approaches to ...evolutionary studies of coloration is providing new insight into the genetic architectures underlying colour traits, including the importance of large-effect mutations and supergenes, the role of development in shaping genetic variation and the origins of adaptive variation, which often involves adaptive introgression. Improved knowledge of the genetic basis of traits can facilitate field studies of natural selection and sexual selection, making it possible for strong selection and its influence on the genome to be demonstrated in wild populations.
Several methods have been proposed to test for introgression across genomes. One method tests for a genome-wide excess of shared derived alleles between taxa using Patterson's D statistic, but does ...not establish which loci show such an excess or whether the excess is due to introgression or ancestral population structure. Several recent studies have extended the use of D by applying the statistic to small genomic regions, rather than genome-wide. Here, we use simulations and whole-genome data from Heliconius butterflies to investigate the behavior of D in small genomic regions. We find that D is unreliable in this situation as it gives inflated values when effective population size is low, causing D outliers to cluster in genomic regions of reduced diversity. As an alternative, we propose a related statistic ƒ(d), a modified version of a statistic originally developed to estimate the genome-wide fraction of admixture. ƒ(d) is not subject to the same biases as D, and is better at identifying introgressed loci. Finally, we show that both D and ƒ(d) outliers tend to cluster in regions of low absolute divergence (d(XY)), which can confound a recently proposed test for differentiating introgression from shared ancestral variation at individual loci.
•The genomic landscape of introgression carries information about the fitness consequences of hybridisation.•Studies are moving from documenting single examples to characterising genome-wide ...trends.•While adaptive introgression appears to be common, most introgressed variation is selected against.•Simulations help to complement interpretations of the landscape of introgression.
Introgression, the transfer of genetic material between species through hybridisation, occurs in many taxa and has important consequences. Genomic studies allow us to characterise the landscape of introgression across the genome, shedding light on both its adaptive benefits and the incompatibilities that help to maintain species barriers. Studies taking a genome-wide view suggest that adaptive introgression may be common, but that introgressed variation between many species is selected against throughout much of the genome. Confounding factors can complicate interpretations from these data, and computational simulations have proved vital to illustrate expected patterns under different scenarios. Future developments will move beyond correlative evidence to explicit models that account for how selection and genetic drift influence introgressed variation.
Evolutionary biologists are increasingly using population genetic variation across genomes to address questions around the origin and ongoing evolution of species. Patterns of differentiation between ...closely related species are highly variable across the genome, and a wide variety of processes contribute to that variation. There is an emerging pattern of parallelism, whereby different species pairs in groups of related species show similar differentiation patterns across their genomes, offering an opportunity to test hypotheses regarding the processes underlying species differentiation. A recent study used both simulations and empirical data to investigate different forms of selection in a radiation of monkeyflowers. The parallel patterns emerged very rapidly after divergence and could not be readily explained by selection for removal of deleterious mutations but instead likely results from some combination of adaptive evolution, species incompatibilities, and ongoing gene flow. Overall, an emerging pattern is that there may be a surprising degree of predictability in the genetic architecture of species differences across groups of related species.
Restriction-site associated DNA (RAD) sequencing is a powerful new method for targeted sequencing across the genomes of many individuals. This approach has broad potential for genetic analysis of ...non-model organisms including genotype-phenotype association mapping, phylogeography, population genetics and scaffolding genome assemblies through linkage mapping. We constructed a RAD library using genomic DNA from a Plutella xylostella (diamondback moth) backcross that segregated for resistance to the insecticide spinosad. Sequencing of 24 individuals was performed on a single Illumina GAIIx lane (51 base paired-end reads). Taking advantage of the lack of crossing over in homologous chromosomes in female Lepidoptera, 3,177 maternally inherited RAD alleles were assigned to the 31 chromosomes, enabling identification of the spinosad resistance and W/Z sex chromosomes. Paired-end reads for each RAD allele were assembled into contigs and compared to the genome of Bombyx mori (n = 28) using BLAST, revealing 28 homologous matches plus 3 expected fusion/breakage events which account for the difference in chromosome number. A genome-wide linkage map (1292 cM) was inferred with 2,878 segregating RAD alleles inherited from the backcross father, producing chromosome and location specific sequenced RAD markers. Here we have used RAD sequencing to construct a genetic linkage map de novo for an organism that has no previous genome data. Comparative analysis of P. xyloxtella linkage groups with B. mori chromosomes shows for the first time, genetic synteny appears common beyond the Macrolepidoptera. RAD sequencing is a powerful system capable of rapidly generating chromosome specific data for non-model organisms.
An important goal in evolutionary biology is to understand the genetic changes underlying novel morphological structures. We investigated the origins of a complex wing pattern found among Amazonian ...Heliconius butterflies. Genome sequence data from 142 individuals across 17 species identified narrow regions associated with two distinct red colour pattern elements, dennis and ray. We hypothesise that these modules in non-coding sequence represent distinct cis-regulatory loci that control expression of the transcription factor optix, which in turn controls red pattern variation across Heliconius. Phylogenetic analysis of the two elements demonstrated that they have distinct evolutionary histories and that novel adaptive morphological variation was created by shuffling these cis-regulatory modules through recombination between divergent lineages. In addition, recombination of modules into different combinations within species further contributes to diversity. Analysis of the timing of diversification in these two regions supports the hypothesis of introgression moving regulatory modules between species, rather than shared ancestral variation. The dennis phenotype introgressed into Heliconius melpomene at about the same time that ray originated in this group, while ray introgressed back into H. elevatus much more recently. We show that shuffling of existing enhancer elements both within and between species provides a mechanism for rapid diversification and generation of novel morphological combinations during adaptive radiation.
Neo-sex chromosomes are found in many taxa, but the forces driving their emergence and spread are poorly understood. The female-specific neo-W chromosome of the African monarch (or queen) butterfly ...Danaus chrysippus presents an intriguing case study because it is restricted to a single 'contact zone' population, involves a putative colour patterning supergene, and co-occurs with infection by the male-killing endosymbiont Spiroplasma. We investigated the origin and evolution of this system using whole genome sequencing. We first identify the 'BC supergene', a broad region of suppressed recombination across nearly half a chromosome, which links two colour patterning loci. Association analysis suggests that the genes yellow and arrow in this region control the forewing colour pattern differences between D. chrysippus subspecies. We then show that the same chromosome has recently formed a neo-W that has spread through the contact zone within approximately 2,200 years. We also assembled the genome of the male-killing Spiroplasma, and find that it shows perfect genealogical congruence with the neo-W, suggesting that the neo-W has hitchhiked to high frequency as the male-killer has spread through the population. The complete absence of female crossing-over in the Lepidoptera causes whole-chromosome hitchhiking of a single neo-W haplotype, carrying a single allele of the BC supergene and dragging multiple non-synonymous mutations to high frequency. This has created a population of infected females that all carry the same recessive colour patterning allele, making the phenotypes of each successive generation highly dependent on uninfected male immigrants. Our findings show how hitchhiking can occur between the physically unlinked genomes of host and endosymbiont, with dramatic consequences.
It is widely documented that hybridisation occurs between many closely related species, but the importance of introgression in adaptive evolution remains unclear, especially in animals. Here, we have ...examined the role of introgressive hybridisation in transferring adaptations between mimetic Heliconius butterflies, taking advantage of the recent identification of a gene regulating red wing patterns in this genus. By sequencing regions both linked and unlinked to the red colour locus, we found a region that displays an almost perfect genotype by phenotype association across four species, H. melpomene, H. cydno, H. timareta, and H. heurippa. This particular segment is located 70 kb downstream of the red colour specification gene optix, and coalescent analysis indicates repeated introgression of adaptive alleles from H. melpomene into the H. cydno species clade. Our analytical methods complement recent genome scale data for the same region and suggest adaptive introgression has a crucial role in generating adaptive wing colour diversity in this group of butterflies.
Studies of invasive species can simultaneously inform management strategies and quantify rapid evolution in the wild. The role of genomics in invasion science is increasingly recognised, and the ...growing availability of reference genomes for invasive species is paving the way for whole‐genome resequencing studies in a wide range of systems. Here, we survey the literature to assess the application of whole‐genome resequencing data in invasion biology. For some applications, such as the reconstruction of invasion routes in time and space, sequencing the whole genome of many individuals can increase the accuracy of existing methods. In other cases, population genomic approaches such as haplotype analysis can permit entirely new questions to be addressed and new technologies applied. To date whole‐genome resequencing has only been used in a handful of invasive systems, but these studies have confirmed the importance of processes such as balancing selection and hybridization in allowing invasive species to reuse existing adaptations and rapidly overcome the challenges of a foreign ecosystem. The use of genomic data does not constitute a paradigm shift per se, but by leveraging new theory, tools, and technologies, population genomics can provide unprecedented insight into basic and applied aspects of invasion science.
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