Dataset Information

Recombining without Hotspots: A Comprehensive Evolutionary Portrait of Recombination in Two Closely Related Species of Drosophila.

ABSTRACT: Meiotic recombination rate varies across the genome within and between individuals, populations, and species in virtually all taxa studied. In almost every species, this variation takes the form of discrete recombination hotspots, determined in some mammals by a protein called PRDM9. Hotspots and their determinants have a profound effect on the genomic landscape, and share certain features that extend across the tree of life. Drosophila, in contrast, are anomalous in their absence of hotspots, PRDM9, and other species-specific differences in the determination of recombination. To better understand the evolution of meiosis and general patterns of recombination across diverse taxa, we present a truly comprehensive portrait of recombination across time, combining recently published cross-based contemporary recombination estimates from each of two sister species with newly obtained linkage-disequilibrium-based historic estimates of recombination from both of these species. Using Drosophila pseudoobscura and Drosophila miranda as a model system, we compare recombination rate between species at multiple scales, and we suggest that Drosophila replicate the pattern seen in human-chimpanzee in which recombination rate is conserved at broad scales. We also find evidence of a species-wide recombination modifier(s), resulting in both a present and historic genome-wide elevation of recombination rates in D. miranda, and identify broad scale effects on recombination from the presence of an inversion. Finally, we reveal an unprecedented view of the distribution of recombination in D. pseudoobscura, illustrating patterns of linked selection and where recombination is taking place. Overall, by combining these estimation approaches, we highlight key similarities and differences in recombination between Drosophila and other organisms.

SUBMITTER: Smukowski Heil CS

PROVIDER: S-EPMC4684701 | biostudies-literature | 2015 Oct

REPOSITORIES: biostudies-literature

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Publications

Recombining without Hotspots: A Comprehensive Evolutionary Portrait of Recombination in Two Closely Related Species of Drosophila.

Smukowski Heil Caiti S CS Ellison Chris C Dubin Matthew M Noor Mohamed A F MA

Genome biology and evolution 20151001 10

Meiotic recombination rate varies across the genome within and between individuals, populations, and species in virtually all taxa studied. In almost every species, this variation takes the form of discrete recombination hotspots, determined in some mammals by a protein called PRDM9. Hotspots and their determinants have a profound effect on the genomic landscape, and share certain features that extend across the tree of life. Drosophila, in contrast, are anomalous in their absence of hotspots, P ...[more]

PMID: 26430062

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Project description:Using genetic data to resolve the evolutionary relationships of species is of major interest in evolutionary and systematic biology. However, reconstructing the sequence of speciation events, the so-called species tree, in closely related and potentially hybridizing species is very challenging. Processes such as incomplete lineage sorting and interspecific gene flow result in local gene genealogies that differ in their topology from the species tree, and analyses of few loci with a single sequence per species are likely to produce conflicting or even misleading results. To study these phenomena on a full phylogenomic scale, we use whole-genome sequence data from 200 individuals of four black-and-white flycatcher species with so far unresolved phylogenetic relationships to infer gene tree topologies and visualize genome-wide patterns of gene tree incongruence. Using phylogenetic analysis in nonoverlapping 10-kb windows, we show that gene tree topologies are extremely diverse and change on a very small physical scale. Moreover, we find strong evidence for gene flow among flycatcher species, with distinct patterns of reduced introgression on the Z chromosome. To resolve species relationships on the background of widespread gene tree incongruence, we used four complementary coalescent-based methods for species tree reconstruction, including complex modeling approaches that incorporate post-divergence gene flow among species. This allowed us to infer the most likely species tree with high confidence. Based on this finding, we show that regions of reduced effective population size, which have been suggested as particularly useful for species tree inference, can produce positively misleading species tree topologies. Our findings disclose the pitfalls of using loci potentially under selection as phylogenetic markers and highlight the potential of modeling approaches to disentangle species relationships in systems with large effective population sizes and post-divergence gene flow.

Project description:BackgroundDuring the speciation process several types of isolating barriers can arise that limit gene flow between diverging populations. Studying recently isolated species can inform our understanding of how and when these barriers arise, and which barriers may be most important to limiting gene flow. Here we focus on Drosophila suboccidentalis and D. occidentalis, which are closely related mushroom-feeding species that inhabit western North America and are not known to overlap in geographic range. We investigate patterns of reproductive isolation between these species, including premating, postmating prezygotic, and postzygotic barriers to gene flow.ResultsUsing flies that originate from a single population of each species, we find that the strength of premating sexual isolation between these species is asymmetric: while D. occidentalis females mate with D. suboccidentalis males at a reduced but moderate rate, D. suboccidentalis females discriminate strongly against mating with D. occidentalis males. Female hybrids will mate at high rates with males of either species, indicating that this discrimination has a recessive genetic basis. Hybrid males are accepted by females of both species. We do not find evidence for postmating prezygotic or postzygotic isolating barriers, as females use the sperm of heterospecific males and both male and female hybrids are fully fertile.ConclusionsPremating isolation is substantial but incomplete, and appears to be the primary form of reproductive isolation between these species. If these species do hybridize, the lack of postzygotic barriers may allow for gene flow between them. Given that these species are recently diverged and are not known to be sympatric, the level of premating isolation is relatively strong given the lack of intrinsic postzygotic isolation. Further work is necessary to characterize the geographic and genetic variation in reproductive isolating barriers, as well as to determine the factors that drive reproductive isolation and the consequences that isolating barriers as well as geographic isolation have had on patterns of gene flow between these species.

Dataset Information

Recombining without Hotspots: A Comprehensive Evolutionary Portrait of Recombination in Two Closely Related Species of Drosophila.

Publications

Recombining without Hotspots: A Comprehensive Evolutionary Portrait of Recombination in Two Closely Related Species of Drosophila.

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