Extensive introgression in a malaria vector species complex revealed by phylogenomics

Fontaine, Michaël C.; Pease, James B.; Steele, Aaron; Waterhouse, Robert M.; Neafsey, Daniel E.; Sharakhov, Igor V.; Jiang, Xiaofang; Hall, Andrew Brantley; Catteruccia, Flaminia; Kakani, Evdoxia G.; Mitchell, Sara N.; Wu, Yi-Chieh; Smith, Hilary A.; Love, R. Rebecca; Lawniczak, Mara; Slotman, Michel A.; Emrich, Scott J.; Hahn, Matthew W.; Besansky, Nora J.

doi:10.1126/science.1258524

Cited by 564 publications

(974 citation statements)

References 105 publications

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“…Contrary to the species branching order, the YG2 gene tree from the An. gambiae complex supported the grouping of two major malaria vectors with a history of substantial autosomal introgression (32), consistent with the hypothesis that even the Y chromosome may have crossed species boundaries. Although a Y chromosome assembly awaits further technological developments, the compilation and comparative analysis of Y chromosome sequences in the An.…”

supporting

confidence: 56%

“…arabiensis as most closely related ( Fig. 6 and SI Appendix, Text S8), an arrangement previously shown to be the result of massive historical introgression between these two species that involved most of the autosomes and the proximal ∼10 Mb of the X chromosome (32). The simplest explanation for a gene tree disagreeing with the species tree in a rapid radiation, such as the An.…”

Section: Extensive Structural Dynamism Of the Y Chromosome In A Youngmentioning

confidence: 93%

“…gambiae complex species-in the face of otherwise rampant structural dynamism and genic turnover on the Y-is consistent with a primary role in male determination in this group. For this reason, we predicted that a gene tree reconstructed from YG2 would reflect the known species branching order (32). Although sibling species in the An.…”

Section: Extensive Structural Dynamism Of the Y Chromosome In A Youngmentioning

confidence: 99%

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Radical remodeling of the Y chromosome in a recent radiation of malaria mosquitoes

Hall

Papathanos

Sharma

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Y chromosomes control essential male functions in many species, including sex determination and fertility. However, because of obstacles posed by repeat-rich heterochromatin, knowledge of Y chromosome sequences is limited to a handful of model organisms, constraining our understanding of Y biology across the tree of life. Here, we leverage long single-molecule sequencing to determine the content and structure of the nonrecombining Y chromosome of the primary African malaria mosquito, Anopheles gambiae. We find that the An. gambiae Y consists almost entirely of a few massively amplified, tandemly arrayed repeats, some of which can recombine with similar repeats on the X chromosome. Sex-specific genome resequencing in a recent species radiation, the An. gambiae complex, revealed rapid sequence turnover within An. gambiae and among species. Exploiting 52 sex-specific An. gambiae RNA-Seq datasets representing all developmental stages, we identified a small repertoire of Y-linked genes that lack X gametologs and are not Y-linked in any other species except An. gambiae, with the notable exception of YG2, a candidate male-determining gene. YG2 is the only gene conserved and exclusive to the Y in all species examined, yet sequence similarity to YG2 is not detectable in the genome of a more distant mosquito relative, suggesting rapid evolution of Y chromosome genes in this highly dynamic genus of malaria vectors. The extensive characterization of the An. gambiae Y provides a long-awaited foundation for studying male mosquito biology, and will inform novel mosquito control strategies based on the manipulation of Y chromosomes.

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supporting

confidence: 56%

Section: Extensive Structural Dynamism Of the Y Chromosome In A Youngmentioning

confidence: 93%

Section: Extensive Structural Dynamism Of the Y Chromosome In A Youngmentioning

confidence: 99%

See 1 more Smart Citation

Radical remodeling of the Y chromosome in a recent radiation of malaria mosquitoes

Hall

Papathanos

Sharma

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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137

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“…2011; Nachman and Payseur 2012; Fontaine et al. 2015; Love et al. 2016), and an inversion enabling the spread of an adaptive cassette between species (Kirkpatrick and Barrett 2015) might produce a signal of elevated f d .…”

Section: Resultsmentioning

confidence: 99%

No evidence for maintenance of a sympatricHeliconiusspecies barrier by chromosomal inversions

et al. 2017

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Mechanisms that suppress recombination are known to help maintain species barriers by preventing the breakup of coadapted gene combinations. The sympatric butterfly species Heliconius melpomene and Heliconius cydno are separated by many strong barriers, but the species still hybridize infrequently in the wild, and around 40% of the genome is influenced by introgression. We tested the hypothesis that genetic barriers between the species are maintained by inversions or other mechanisms that reduce between‐species recombination rate. We constructed fine‐scale recombination maps for Panamanian populations of both species and their hybrids to directly measure recombination rate within and between species, and generated long sequence reads to detect inversions. We find no evidence for a systematic reduction in recombination rates in F1 hybrids, and also no evidence for inversions longer than 50 kb that might be involved in generating or maintaining species barriers. This suggests that mechanisms leading to global or local reduction in recombination do not play a significant role in the maintenance of species barriers between H. melpomene and H. cydno.

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“…Evidence for the role of purifying selection in shaping introgression landscape come from particular categories of genes experiencing different amounts of introgression as previously demonstrated for non-human species (Fontaine et al, 2015;Janoušek et al, 2015;Runemark et al, 2018;Schumer et al, 2016). This is also true for the autosomal regions deficient in both Neanderthal and Denisovan ancestries, which contain a significant enrichment of genes transcribed in meiotic germ cells (Jégou et al, 2017).…”

Section: Selection Against Introgressed Regions At the Level Of Genommentioning

confidence: 54%

Evolutionary and Medical Consequences of Archaic Introgression into Modern Human Genomes

Dolgova

Lao

2018

Preprint

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The demographic history of anatomically modern humans (AMH) involves multiple migration events, population extinctions and genetic adaptations. As genome-wide data from complete genome sequencing becomes increasingly abundant and available even from extinct hominins, new insights of the evolutionary history of our species are discovered.It is currently known that AMH introgressed with archaic hominins once they left the African continent. Current out of African human genomes carry fragments of archaic origin. This review focuses on the fitness consequences of archaic interbreeding in current human populations. We discuss new insights and challenges that researchers face when interpreting the potential impact of introgression on fitness and testing hypotheses about the role of selection within the context of health and disease.Keywords: archaic introgression, fitness, natural selection, Neanderthal, Denisova, anatomically modern humans. Peer-reviewed version available at Genes 2018, 9, 358; doi:10.3390/genes9070358 2 Widespread interbreeding between homininsThe demographic history of anatomically modern humans (AMH) is complex, and involves a large number of migrations, genetic admixtures and introgressions, population extinctions and genetic adaptations, which overlap both in time and in space (see Figure 1). Due to this complexity, the evolutionary history of humankind is still far from being fully understood (Nielsen et al., 2017). During the last 30 years, the most accepted demographic scenario for explaining recent evolution of AMH has been the Out of Africa model (OOA). According to this model, AMH evolved in Africa around 100-200 thousands years ago (kya) in East Africa and migrated to the rest of the world. Classical "pure" OOA assumes that admixture with other archaic populations such as Neanderthals or Denisovans, present at the time of the rise of AMH, either did not occur or was negligible (Lalueza-Fox & Gilbert, 2011). Figure 1. Family tree of the four groups of early humans living in Eurasia 50,000 years ago and the inferred gene flow between the groups due to interbreeding (based on Prüfer et al., 2014;Mondal et al., 2016;Hsieh et al., 2016; Medina-Gomez et al., 2017). The direction and estimated magnitude of inferred gene flow events are shown. Branch lengths and timing of gene flows are not scaled. The dashed line indicates that it is uncertain whether Denisovan gene flow into modern humans in mainland Asia occurred directly or via Oceania. Light violet color indicates introgression events from unknown archaic populations (Ghost).However, genomic studies of ancient DNA have revealed that AMH interbred with other hominid lineages, such as Neanderthals and Denisovans, present in Eurasia up to ∼30,000-50,000 years ago Quach & Quintana-Murci, 2017;Vattathil & Akey, 2015 New studies based on current genetic diversity are suggesting that the events of archaic introgression in AMH did occur out of Africa with other hidden "ghost" archaic populations (Mondal et al., 2016). Furthermore, there i...

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Extensive introgression in a malaria vector species complex revealed by phylogenomics

Cited by 564 publications

References 105 publications

Radical remodeling of the Y chromosome in a recent radiation of malaria mosquitoes

Radical remodeling of the Y chromosome in a recent radiation of malaria mosquitoes

No evidence for maintenance of a sympatricHeliconiusspecies barrier by chromosomal inversions

Evolutionary and Medical Consequences of Archaic Introgression into Modern Human Genomes

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