Fine scale mapping of genomic introgressions within the Drosophila yakuba clade

Abstract

The process of speciation involves populations diverging over time until they are genetically and reproductively isolated. Hybridization between nascent species was long thought to directly oppose speciation. However, the amount of interspecific genetic exchange (introgression) mediated by hybridization remains largely unknown, although recent progress in genome sequencing has made measuring introgression more tractable. A natural place to look for individuals with admixed ancestry (indicative of introgression) is in regions where species co-occur. In west Africa, D. santomea and D. yakuba hybridize on the island of São Tomé, while D. yakuba and D. teissieri hybridize on the nearby island of Bioko. In this report, we quantify the genomic extent of introgression between the three species of the Drosophila yakuba clade (D. yakuba, D. santomea), D. teissieri). We sequenced the genomes of 86 individuals from all three species. We also developed and applied a new statistical framework, using a hidden Markov approach, to identify introgression. We found that introgression has occurred between both species pairs but most introgressed segments are small (on the order of a few kilobases). After ruling out the retention of ancestral polymorphism as an explanation for these similar regions, we find that the sizes of introgressed haplotypes indicate that genetic exchange is not recent (>1,000 generations ago). We additionally show that in both cases, introgression was rarer on X chromosomes than on autosomes which is consistent with sex chromosomes playing a large role in reproductive isolation. Even though the two species pairs have stable contemporary hybrid zones, providing the opportunity for ongoing gene flow, our results indicate that genetic exchange between these species is currently rare.

A Maladaptive Combination of Traits Contributes to the Maintenance of a Drosophila Hybrid Zone

“…Using the temperature dependence of development time to convert generations to absolute ages, we estimate admixture occurred between 23 and 320 years ago (Table S4). Previous simulations using introgressed haplotype size estimated admixture between 1,600 and 8,100 generations ago, assuming very low rates of migration [1]. These prior estimates correspond to admixture between about 60 and 1,100 years ago, which overlaps with our estimates here.…”

“…Although we did not sample advanced-generation hybrids on Bioko, genome data provide evidence for some introgression [1,8]. We used the distribution of haplotype lengths and possible generation times to estimate the timing of admixture.…”

“…The D. yakuba Flybase assembly (version 1.05, [52]) was masked for repeats (RepeatMasker, [53]) and used as the first parental reference. The second parental input for MSG was made by mapping reads from the outbred individual Bioko_cascade_2_2 [1] to the D. yakuba flybase assembly and creating an updated FASTA file with genotype calls from GATK [54,55]. The updated FASTA file uses only single nucleotide polymorphisms (SNPs), and masks all inferred indels plus 5 bases both up and downstream.…”

“… SUMMARY Drosophila teissieri and D. yakuba diverged approximately 3 million years ago and are thought to share a large, ancestral, African range [1–3]. These species now co-occur in parts of continental Africa and in west Africa on the island of Bioko [1,4].…”

“…These species now co-occur in parts of continental Africa and in west Africa on the island of Bioko [1,4]. While D. yakuba is a human commensal, D. teissieri seems to be associated with Parinari fruits, restricting its range to forests [4–6].…”