Speciation with gene flow in equids despite extensive chromosomal plasticity

Hákon Jónsson; Mikkel Schubert; Andaine Seguin-Orlando; Aurélien Ginolhac; Lillian Petersen; Matteo Fumagalli; Anders Albrechtsen; Bent Petersen; Thorfinn Sand Korneliussen; Julia Thidamarth Vilstrup Mouatt; Teri Lear; Jennifer Leigh Myka; Judith Lundquist; Donald C. Miller; Ahmed H. Alfarhan; Saleh A. Alquraishi; Khaled A.S. Al-Rasheid; Julia Stagegaard; Günter Strauss; Mads Frost Bertelsen; Thomas Sicheritz-Ponten; Douglas F. Antczak; Ernest Bailey; Rasmus Nielsen; Eske Willerslev; Ludovic Antoine Alexandre Orlando

doi:10.1073/pnas.1412627111

Speciation with gene flow in equids despite extensive chromosomal plasticity

Hákon Jónsson, Mikkel Schubert, Andaine Seguin-Orlando, Aurélien Ginolhac, Lillian Petersen, Matteo Fumagalli, Anders Albrechtsen, Bent Petersen, Thorfinn Sand Korneliussen, Julia Thidamarth Vilstrup Mouatt, Teri Lear, Jennifer Leigh Myka, Judith Lundquist, Donald C. Miller, Ahmed H. Alfarhan, Saleh A. Alquraishi, Khaled A.S. Al-Rasheid, Julia Stagegaard, Günter Strauss, Mads Frost BertelsenThomas Sicheritz-Ponten, Douglas F. Antczak, Ernest Bailey, Rasmus Nielsen, Eske Willerslev, Ludovic Antoine Alexandre Orlando

Computational and RNA Biology

102 Citations (Scopus)

Abstract

Horses, asses, and zebras belong to a single genus, Equus, which emerged 4.0-4.5 Mya. Although the equine fossil record represents a textbook example of evolution, the succession of events that gave rise to the diversity of species existing today remains unclear. Here we present six genomes from each living species of asses and zebras. This completes the set of genomes available for all extant species in the genus, which was hitherto represented only by the horse and the domestic donkey. In addition, we used a museum specimen to characterize the genome of the quagga zebra, which was driven to extinction in the early 1900s. We scan the genomes for lineage-specific adaptations and identify 48 genes that have evolved under positive selection and are involved in olfaction, immune response, development, locomotion, and behavior. Our extensive genome dataset reveals a highly dynamic demographic history with synchronous expansions and collapses on different continents during the last 400 ky after major climatic events. We show that the earliest speciation occurred with gene flow in Northern America, and that the ancestor of present-day asses and zebras dispersed into the Old World 2.1-3.4 Mya. Strikingly, we also find evidence for gene flow involving three contemporary equine species despite chromosomal numbers varying from 16 pairs to 31 pairs. These findings challenge the claim that the accumulation of chromosomal rearrangements drive complete reproductive isolation, and promote equids as a fundamental model for understanding the interplay between chromosomal structure, gene flow, and, ultimately, speciation.

Original language	English
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	111
Issue number	52
Pages (from-to)	18655–18660
Number of pages	6
ISSN	0027-8424
DOIs	https://doi.org/10.1073/pnas.1412627111
Publication status	Published - 30 Dec 2014

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Jónsson, H., Schubert, M., Seguin-Orlando, A., Ginolhac, A., Petersen, L., Fumagalli, M., Albrechtsen, A., Petersen, B., Korneliussen, T. S., Mouatt, J. T. V., Lear, T., Myka, J. L., Lundquist, J., Miller, D. C., Alfarhan, A. H., Alquraishi, S. A., Al-Rasheid, K. A. S., Stagegaard, J., Strauss, G., ... Orlando, L. A. A. (2014). Speciation with gene flow in equids despite extensive chromosomal plasticity. Proceedings of the National Academy of Sciences of the United States of America, 111(52), 18655–18660. https://doi.org/10.1073/pnas.1412627111

Jónsson, H, Schubert, M, Seguin-Orlando, A, Ginolhac, A, Petersen, L, Fumagalli, M, Albrechtsen, A , Petersen, B , Korneliussen, TS, Mouatt, JTV, Lear, T, Myka, JL, Lundquist, J, Miller, DC, Alfarhan, AH, Alquraishi, SA, Al-Rasheid, KAS, Stagegaard, J, Strauss, G, Bertelsen, MF, Sicheritz-Ponten, T, Antczak, DF, Bailey, E, Nielsen, R, Willerslev, E & Orlando, LAA 2014, 'Speciation with gene flow in equids despite extensive chromosomal plasticity', Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 52, pp. 18655–18660. https://doi.org/10.1073/pnas.1412627111

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title = "Speciation with gene flow in equids despite extensive chromosomal plasticity",

abstract = "Horses, asses, and zebras belong to a single genus, Equus, which emerged 4.0-4.5 Mya. Although the equine fossil record represents a textbook example of evolution, the succession of events that gave rise to the diversity of species existing today remains unclear. Here we present six genomes from each living species of asses and zebras. This completes the set of genomes available for all extant species in the genus, which was hitherto represented only by the horse and the domestic donkey. In addition, we used a museum specimen to characterize the genome of the quagga zebra, which was driven to extinction in the early 1900s. We scan the genomes for lineage-specific adaptations and identify 48 genes that have evolved under positive selection and are involved in olfaction, immune response, development, locomotion, and behavior. Our extensive genome dataset reveals a highly dynamic demographic history with synchronous expansions and collapses on different continents during the last 400 ky after major climatic events. We show that the earliest speciation occurred with gene flow in Northern America, and that the ancestor of present-day asses and zebras dispersed into the Old World 2.1-3.4 Mya. Strikingly, we also find evidence for gene flow involving three contemporary equine species despite chromosomal numbers varying from 16 pairs to 31 pairs. These findings challenge the claim that the accumulation of chromosomal rearrangements drive complete reproductive isolation, and promote equids as a fundamental model for understanding the interplay between chromosomal structure, gene flow, and, ultimately, speciation.",

author = "H{\'a}kon J{\'o}nsson and Mikkel Schubert and Andaine Seguin-Orlando and Aur{\'e}lien Ginolhac and Lillian Petersen and Matteo Fumagalli and Anders Albrechtsen and Bent Petersen and Korneliussen, {Thorfinn Sand} and Mouatt, {Julia Thidamarth Vilstrup} and Teri Lear and Myka, {Jennifer Leigh} and Judith Lundquist and Miller, {Donald C.} and Alfarhan, {Ahmed H.} and Alquraishi, {Saleh A.} and Al-Rasheid, {Khaled A.S.} and Julia Stagegaard and G{\"u}nter Strauss and Bertelsen, {Mads Frost} and Thomas Sicheritz-Ponten and Antczak, {Douglas F.} and Ernest Bailey and Rasmus Nielsen and Eske Willerslev and Orlando, {Ludovic Antoine Alexandre}",

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T1 - Speciation with gene flow in equids despite extensive chromosomal plasticity

AU - Jónsson, Hákon

AU - Schubert, Mikkel

AU - Seguin-Orlando, Andaine

AU - Ginolhac, Aurélien

AU - Petersen, Lillian

AU - Fumagalli, Matteo

AU - Albrechtsen, Anders

AU - Petersen, Bent

AU - Korneliussen, Thorfinn Sand

AU - Mouatt, Julia Thidamarth Vilstrup

AU - Lear, Teri

AU - Myka, Jennifer Leigh

AU - Lundquist, Judith

AU - Miller, Donald C.

AU - Alfarhan, Ahmed H.

AU - Alquraishi, Saleh A.

AU - Al-Rasheid, Khaled A.S.

AU - Stagegaard, Julia

AU - Strauss, Günter

AU - Bertelsen, Mads Frost

AU - Sicheritz-Ponten, Thomas

AU - Antczak, Douglas F.

AU - Bailey, Ernest

AU - Nielsen, Rasmus

AU - Willerslev, Eske

AU - Orlando, Ludovic Antoine Alexandre

PY - 2014/12/30

Y1 - 2014/12/30

N2 - Horses, asses, and zebras belong to a single genus, Equus, which emerged 4.0-4.5 Mya. Although the equine fossil record represents a textbook example of evolution, the succession of events that gave rise to the diversity of species existing today remains unclear. Here we present six genomes from each living species of asses and zebras. This completes the set of genomes available for all extant species in the genus, which was hitherto represented only by the horse and the domestic donkey. In addition, we used a museum specimen to characterize the genome of the quagga zebra, which was driven to extinction in the early 1900s. We scan the genomes for lineage-specific adaptations and identify 48 genes that have evolved under positive selection and are involved in olfaction, immune response, development, locomotion, and behavior. Our extensive genome dataset reveals a highly dynamic demographic history with synchronous expansions and collapses on different continents during the last 400 ky after major climatic events. We show that the earliest speciation occurred with gene flow in Northern America, and that the ancestor of present-day asses and zebras dispersed into the Old World 2.1-3.4 Mya. Strikingly, we also find evidence for gene flow involving three contemporary equine species despite chromosomal numbers varying from 16 pairs to 31 pairs. These findings challenge the claim that the accumulation of chromosomal rearrangements drive complete reproductive isolation, and promote equids as a fundamental model for understanding the interplay between chromosomal structure, gene flow, and, ultimately, speciation.

AB - Horses, asses, and zebras belong to a single genus, Equus, which emerged 4.0-4.5 Mya. Although the equine fossil record represents a textbook example of evolution, the succession of events that gave rise to the diversity of species existing today remains unclear. Here we present six genomes from each living species of asses and zebras. This completes the set of genomes available for all extant species in the genus, which was hitherto represented only by the horse and the domestic donkey. In addition, we used a museum specimen to characterize the genome of the quagga zebra, which was driven to extinction in the early 1900s. We scan the genomes for lineage-specific adaptations and identify 48 genes that have evolved under positive selection and are involved in olfaction, immune response, development, locomotion, and behavior. Our extensive genome dataset reveals a highly dynamic demographic history with synchronous expansions and collapses on different continents during the last 400 ky after major climatic events. We show that the earliest speciation occurred with gene flow in Northern America, and that the ancestor of present-day asses and zebras dispersed into the Old World 2.1-3.4 Mya. Strikingly, we also find evidence for gene flow involving three contemporary equine species despite chromosomal numbers varying from 16 pairs to 31 pairs. These findings challenge the claim that the accumulation of chromosomal rearrangements drive complete reproductive isolation, and promote equids as a fundamental model for understanding the interplay between chromosomal structure, gene flow, and, ultimately, speciation.

U2 - 10.1073/pnas.1412627111

DO - 10.1073/pnas.1412627111

M3 - Journal article

C2 - 25453089

SN - 0027-8424

VL - 111

SP - 18655

EP - 18660

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 52

ER -

Speciation with gene flow in equids despite extensive chromosomal plasticity

Abstract

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