Fine scale mapping of genomic introgressions within theDrosophila yakubaclade

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.AUTHOR SUMMARYEven though hybridization is thought to be pervasive among animal species, the frequency of introgression, the transfer of genetic material between species, remains largely unknown. In this report we quantify the magnitude and genomic distribution of introgression among three species of Drosophila that encompass the two known stable hybrid zones in this genetic model genus. We obtained whole genome sequences for individuals of the three species across their geographic range (including their hybrid zones) and developed a hidden Markov model-based method to identify patterns of genomic introgression between species. We found that nuclear introgression is rare between both species pairs, suggesting hybrids in nature rarely successfully backcross with parental species. Nevertheless, some D. santomea alleles introgressed into D. yakuba have spread from São Tomé to other islands in the Gulf of Guinea where D. santomea is not found. Our results indicate that in spite of contemporary hybridization between species that produces fertile hybrids, the rates of gene exchange between species are low.

Fine‐scale geographic patterns of gene flow and reproductive character displacement inDrosophila subquinariaandDrosophila recens

“…The signature of admixture between species has been tested in some other systems undergoing reinforcement, and results vary in the magnitude and direction of introgression (e.g., Burri et al., ; Kulathinal, Stevison, & Noor, ; Lemmon & Juenger, ; Roda, Mendes, Hahn, & Hopkins, ; Turissini & Matute, ). A similar pattern to our system is seen in Phlox plants, where introgression between species occurs in sympatric but not in allopatric populations and the direction of introgression is asymmetric (Roda et al., ).…”

“…A similar pattern to our system is seen in Phlox plants, where introgression between species occurs in sympatric but not in allopatric populations and the direction of introgression is asymmetric (Roda et al., ). In contrast, collared and pied Ficedula flycatchers are not more differentiated in sympatric vs. allopatric populations (Burri et al., ), and in D. yakuba and D. santomea introgression is rare in the genome and tracts appear to be old (Turissini & Matute, ).…”

Gene exchange between two divergent species of the fungal human pathogen,Coccidioides

“…D‐statistics can be used to test whether populations have exchanged genes, but they do not identify the location of introgressed haplotypes in the genome. To identify introgressed regions in individuals from the two Coccidioides species, we used a hidden Markov model (HMM), originally designed to detect introgression in diploids (i.e., Int‐HMM; Turissini and Matute ) that had been modified to detect introgressed haploblocks in haploids (i.e., by assuming no heterozygosity; Maxwell et al. ).…”

“…(). As proposed in the original description of the method (Turissini and Matute ), we assumed starting probabilities for each SNP follow a Poisson distribution with a constant recombination rate. We ran the model with three different recombination rates: 5 × 10 –5 , 1 × 10 –6 , and 1 × 10 –7 Morgans/bp.…”

“Two Rules of Speciation” revisited

“…Further, there are a fair number of studies showing occasional hybridization between sympatric and parapatric species that still maintain their integrity in the wild, probably because of the low intrinsic fitness of hybrids (e.g., Kruuk, Gilchrist, & Barton, ; Turner & Harr, ). This is complemented by work showing that X chromosomes often introgress far less broadly between taxa than do autosomes, probably because in part there are large X effects on postzygotic isolation (Storchová, Reif, & Nachman, ; Tucker, Sage, Warner, Wilson, & Eicher, ; Turissini & Matute, ). This, however, does not give us carte blanche to equate hybrid sterility and inviability with speciation.…”