Ancient and modern genomes unravel the evolutionary history of the rhinoceros family

Only five species of the once-diverse Rhinocerotidae remain, making the reconstruction of their evolutionary history a challenge to biologists since Darwin. We sequenced genomes from five rhinoceros species (three extinct and two living), which we compared to existing data from the remaining three l...

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Veröffentlicht in:Cell 2021-09, Vol.184 (19), p.4874-4885.e16
Hauptverfasser: Liu, Shanlin, Westbury, Michael V., Dussex, Nicolas, Mitchell, Kieren J., Sinding, Mikkel-Holger S., Heintzman, Peter D., Duchêne, David A., Kapp, Joshua D., von Seth, Johanna, Heiniger, Holly, Sánchez-Barreiro, Fátima, Margaryan, Ashot, André-Olsen, Remi, De Cahsan, Binia, Meng, Guanliang, Yang, Chentao, Chen, Lei, van der Valk, Tom, Moodley, Yoshan, Rookmaaker, Kees, Bruford, Michael W., Ryder, Oliver, Steiner, Cynthia, Bruins-van Sonsbeek, Linda G.R., Vartanyan, Sergey, Guo, Chunxue, Cooper, Alan, Kosintsev, Pavel, Kirillova, Irina, Lister, Adrian M., Marques-Bonet, Tomas, Gopalakrishnan, Shyam, Dunn, Robert R., Lorenzen, Eline D., Shapiro, Beth, Zhang, Guojie, Antoine, Pierre-Olivier, Dalén, Love, Gilbert, M. Thomas P.
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container_end_page 4885.e16
container_issue 19
container_start_page 4874
container_title Cell
container_volume 184
creator Liu, Shanlin
Westbury, Michael V.
Dussex, Nicolas
Mitchell, Kieren J.
Sinding, Mikkel-Holger S.
Heintzman, Peter D.
Duchêne, David A.
Kapp, Joshua D.
von Seth, Johanna
Heiniger, Holly
Sánchez-Barreiro, Fátima
Margaryan, Ashot
André-Olsen, Remi
De Cahsan, Binia
Meng, Guanliang
Yang, Chentao
Chen, Lei
van der Valk, Tom
Moodley, Yoshan
Rookmaaker, Kees
Bruford, Michael W.
Ryder, Oliver
Steiner, Cynthia
Bruins-van Sonsbeek, Linda G.R.
Vartanyan, Sergey
Guo, Chunxue
Cooper, Alan
Kosintsev, Pavel
Kirillova, Irina
Lister, Adrian M.
Marques-Bonet, Tomas
Gopalakrishnan, Shyam
Dunn, Robert R.
Lorenzen, Eline D.
Shapiro, Beth
Zhang, Guojie
Antoine, Pierre-Olivier
Dalén, Love
Gilbert, M. Thomas P.
description Only five species of the once-diverse Rhinocerotidae remain, making the reconstruction of their evolutionary history a challenge to biologists since Darwin. We sequenced genomes from five rhinoceros species (three extinct and two living), which we compared to existing data from the remaining three living species and a range of outgroups. We identify an early divergence between extant African and Eurasian lineages, resolving a key debate regarding the phylogeny of extant rhinoceroses. This early Miocene (∼16 million years ago [mya]) split post-dates the land bridge formation between the Afro-Arabian and Eurasian landmasses. Our analyses also show that while rhinoceros genomes in general exhibit low levels of genome-wide diversity, heterozygosity is lowest and inbreeding is highest in the modern species. These results suggest that while low genetic diversity is a long-term feature of the family, it has been particularly exacerbated recently, likely reflecting recent anthropogenic-driven population declines. [Display omitted] •Analysis of genomes from all five extant and three extinct rhinoceros species•Strong phylogenomic support for the geographical hypothesis of rhinoceros evolution•Basal split between African and Eurasian lineages in the early Miocene (∼16 mya)•While all rhinoceroses have low genome diversity, it is lowest in modern-day ones The comparison of de novo genomes from the white, black, Sumatran, and greater one-horned rhinoceroses with the genomes of a historic Javan rhinoceros and three extinct Pleistocene species resolves the evolutionary relationships within the Rhinocerotidae family and reveals that low genetic diversity is a long-term feature of rhinoceroses.
doi_str_mv 10.1016/j.cell.2021.07.032
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Thomas P.</creator><creatorcontrib>Liu, Shanlin ; Westbury, Michael V. ; Dussex, Nicolas ; Mitchell, Kieren J. ; Sinding, Mikkel-Holger S. ; Heintzman, Peter D. ; Duchêne, David A. ; Kapp, Joshua D. ; von Seth, Johanna ; Heiniger, Holly ; Sánchez-Barreiro, Fátima ; Margaryan, Ashot ; André-Olsen, Remi ; De Cahsan, Binia ; Meng, Guanliang ; Yang, Chentao ; Chen, Lei ; van der Valk, Tom ; Moodley, Yoshan ; Rookmaaker, Kees ; Bruford, Michael W. ; Ryder, Oliver ; Steiner, Cynthia ; Bruins-van Sonsbeek, Linda G.R. ; Vartanyan, Sergey ; Guo, Chunxue ; Cooper, Alan ; Kosintsev, Pavel ; Kirillova, Irina ; Lister, Adrian M. ; Marques-Bonet, Tomas ; Gopalakrishnan, Shyam ; Dunn, Robert R. ; Lorenzen, Eline D. ; Shapiro, Beth ; Zhang, Guojie ; Antoine, Pierre-Olivier ; Dalén, Love ; Gilbert, M. Thomas P.</creatorcontrib><description>Only five species of the once-diverse Rhinocerotidae remain, making the reconstruction of their evolutionary history a challenge to biologists since Darwin. We sequenced genomes from five rhinoceros species (three extinct and two living), which we compared to existing data from the remaining three living species and a range of outgroups. We identify an early divergence between extant African and Eurasian lineages, resolving a key debate regarding the phylogeny of extant rhinoceroses. This early Miocene (∼16 million years ago [mya]) split post-dates the land bridge formation between the Afro-Arabian and Eurasian landmasses. Our analyses also show that while rhinoceros genomes in general exhibit low levels of genome-wide diversity, heterozygosity is lowest and inbreeding is highest in the modern species. These results suggest that while low genetic diversity is a long-term feature of the family, it has been particularly exacerbated recently, likely reflecting recent anthropogenic-driven population declines. [Display omitted] •Analysis of genomes from all five extant and three extinct rhinoceros species•Strong phylogenomic support for the geographical hypothesis of rhinoceros evolution•Basal split between African and Eurasian lineages in the early Miocene (∼16 mya)•While all rhinoceroses have low genome diversity, it is lowest in modern-day ones The comparison of de novo genomes from the white, black, Sumatran, and greater one-horned rhinoceroses with the genomes of a historic Javan rhinoceros and three extinct Pleistocene species resolves the evolutionary relationships within the Rhinocerotidae family and reveals that low genetic diversity is a long-term feature of rhinoceroses.</description><identifier>ISSN: 0092-8674</identifier><identifier>ISSN: 1097-4172</identifier><identifier>EISSN: 1097-4172</identifier><identifier>DOI: 10.1016/j.cell.2021.07.032</identifier><identifier>PMID: 34433011</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animal biology ; Animals ; Demography ; Environmental Sciences ; Evolution, Molecular ; Gene Flow ; Genetic Variation ; Genome ; Geography ; Heterozygote ; Homozygote ; Host Specificity ; Life Sciences ; Markov Chains ; Matematikk og Naturvitenskap: 400 ; Mathematics and natural science: 400 ; Mutation - genetics ; Perissodactyla - genetics ; Phylogeny ; Rhinoceros, Perissodactyl, Conservation genomics, Phylogenomics, Genomic diversity ; Species Specificity ; Time Factors ; VDP ; Zoological anatomy: 481 ; Zoologisk anatomi: 481 ; Zoologiske og botaniske fag: 480 ; Zoology and botany: 480</subject><ispartof>Cell, 2021-09, Vol.184 (19), p.4874-4885.e16</ispartof><rights>2021 The Authors</rights><rights>Copyright © 2021 The Authors. 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Thomas P.</creatorcontrib><title>Ancient and modern genomes unravel the evolutionary history of the rhinoceros family</title><title>Cell</title><addtitle>Cell</addtitle><description>Only five species of the once-diverse Rhinocerotidae remain, making the reconstruction of their evolutionary history a challenge to biologists since Darwin. We sequenced genomes from five rhinoceros species (three extinct and two living), which we compared to existing data from the remaining three living species and a range of outgroups. We identify an early divergence between extant African and Eurasian lineages, resolving a key debate regarding the phylogeny of extant rhinoceroses. This early Miocene (∼16 million years ago [mya]) split post-dates the land bridge formation between the Afro-Arabian and Eurasian landmasses. Our analyses also show that while rhinoceros genomes in general exhibit low levels of genome-wide diversity, heterozygosity is lowest and inbreeding is highest in the modern species. These results suggest that while low genetic diversity is a long-term feature of the family, it has been particularly exacerbated recently, likely reflecting recent anthropogenic-driven population declines. 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Thomas P.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3732-77d41c0c19c70b6dbfd0e42b56810bd3ebd75523103572f4d35200e2707466b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animal biology</topic><topic>Animals</topic><topic>Demography</topic><topic>Environmental Sciences</topic><topic>Evolution, Molecular</topic><topic>Gene Flow</topic><topic>Genetic Variation</topic><topic>Genome</topic><topic>Geography</topic><topic>Heterozygote</topic><topic>Homozygote</topic><topic>Host Specificity</topic><topic>Life Sciences</topic><topic>Markov Chains</topic><topic>Matematikk og Naturvitenskap: 400</topic><topic>Mathematics and natural science: 400</topic><topic>Mutation - genetics</topic><topic>Perissodactyla - genetics</topic><topic>Phylogeny</topic><topic>Rhinoceros, Perissodactyl, Conservation genomics, Phylogenomics, Genomic diversity</topic><topic>Species Specificity</topic><topic>Time Factors</topic><topic>VDP</topic><topic>Zoological anatomy: 481</topic><topic>Zoologisk anatomi: 481</topic><topic>Zoologiske og botaniske fag: 480</topic><topic>Zoology and botany: 480</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Shanlin</creatorcontrib><creatorcontrib>Westbury, Michael V.</creatorcontrib><creatorcontrib>Dussex, Nicolas</creatorcontrib><creatorcontrib>Mitchell, Kieren J.</creatorcontrib><creatorcontrib>Sinding, Mikkel-Holger S.</creatorcontrib><creatorcontrib>Heintzman, Peter D.</creatorcontrib><creatorcontrib>Duchêne, David A.</creatorcontrib><creatorcontrib>Kapp, Joshua D.</creatorcontrib><creatorcontrib>von Seth, Johanna</creatorcontrib><creatorcontrib>Heiniger, Holly</creatorcontrib><creatorcontrib>Sánchez-Barreiro, Fátima</creatorcontrib><creatorcontrib>Margaryan, Ashot</creatorcontrib><creatorcontrib>André-Olsen, Remi</creatorcontrib><creatorcontrib>De Cahsan, Binia</creatorcontrib><creatorcontrib>Meng, Guanliang</creatorcontrib><creatorcontrib>Yang, Chentao</creatorcontrib><creatorcontrib>Chen, Lei</creatorcontrib><creatorcontrib>van der Valk, Tom</creatorcontrib><creatorcontrib>Moodley, Yoshan</creatorcontrib><creatorcontrib>Rookmaaker, Kees</creatorcontrib><creatorcontrib>Bruford, Michael W.</creatorcontrib><creatorcontrib>Ryder, Oliver</creatorcontrib><creatorcontrib>Steiner, Cynthia</creatorcontrib><creatorcontrib>Bruins-van Sonsbeek, Linda G.R.</creatorcontrib><creatorcontrib>Vartanyan, Sergey</creatorcontrib><creatorcontrib>Guo, Chunxue</creatorcontrib><creatorcontrib>Cooper, Alan</creatorcontrib><creatorcontrib>Kosintsev, Pavel</creatorcontrib><creatorcontrib>Kirillova, Irina</creatorcontrib><creatorcontrib>Lister, Adrian M.</creatorcontrib><creatorcontrib>Marques-Bonet, Tomas</creatorcontrib><creatorcontrib>Gopalakrishnan, Shyam</creatorcontrib><creatorcontrib>Dunn, Robert R.</creatorcontrib><creatorcontrib>Lorenzen, Eline D.</creatorcontrib><creatorcontrib>Shapiro, Beth</creatorcontrib><creatorcontrib>Zhang, Guojie</creatorcontrib><creatorcontrib>Antoine, Pierre-Olivier</creatorcontrib><creatorcontrib>Dalén, Love</creatorcontrib><creatorcontrib>Gilbert, M. Thomas P.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>NORA - Norwegian Open Research Archives</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Shanlin</au><au>Westbury, Michael V.</au><au>Dussex, Nicolas</au><au>Mitchell, Kieren J.</au><au>Sinding, Mikkel-Holger S.</au><au>Heintzman, Peter D.</au><au>Duchêne, David A.</au><au>Kapp, Joshua D.</au><au>von Seth, Johanna</au><au>Heiniger, Holly</au><au>Sánchez-Barreiro, Fátima</au><au>Margaryan, Ashot</au><au>André-Olsen, Remi</au><au>De Cahsan, Binia</au><au>Meng, Guanliang</au><au>Yang, Chentao</au><au>Chen, Lei</au><au>van der Valk, Tom</au><au>Moodley, Yoshan</au><au>Rookmaaker, Kees</au><au>Bruford, Michael W.</au><au>Ryder, Oliver</au><au>Steiner, Cynthia</au><au>Bruins-van Sonsbeek, Linda G.R.</au><au>Vartanyan, Sergey</au><au>Guo, Chunxue</au><au>Cooper, Alan</au><au>Kosintsev, Pavel</au><au>Kirillova, Irina</au><au>Lister, Adrian M.</au><au>Marques-Bonet, Tomas</au><au>Gopalakrishnan, Shyam</au><au>Dunn, Robert R.</au><au>Lorenzen, Eline D.</au><au>Shapiro, Beth</au><au>Zhang, Guojie</au><au>Antoine, Pierre-Olivier</au><au>Dalén, Love</au><au>Gilbert, M. Thomas P.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Ancient and modern genomes unravel the evolutionary history of the rhinoceros family</atitle><jtitle>Cell</jtitle><addtitle>Cell</addtitle><date>2021-09-16</date><risdate>2021</risdate><volume>184</volume><issue>19</issue><spage>4874</spage><epage>4885.e16</epage><pages>4874-4885.e16</pages><issn>0092-8674</issn><issn>1097-4172</issn><eissn>1097-4172</eissn><abstract>Only five species of the once-diverse Rhinocerotidae remain, making the reconstruction of their evolutionary history a challenge to biologists since Darwin. We sequenced genomes from five rhinoceros species (three extinct and two living), which we compared to existing data from the remaining three living species and a range of outgroups. We identify an early divergence between extant African and Eurasian lineages, resolving a key debate regarding the phylogeny of extant rhinoceroses. This early Miocene (∼16 million years ago [mya]) split post-dates the land bridge formation between the Afro-Arabian and Eurasian landmasses. Our analyses also show that while rhinoceros genomes in general exhibit low levels of genome-wide diversity, heterozygosity is lowest and inbreeding is highest in the modern species. These results suggest that while low genetic diversity is a long-term feature of the family, it has been particularly exacerbated recently, likely reflecting recent anthropogenic-driven population declines. [Display omitted] •Analysis of genomes from all five extant and three extinct rhinoceros species•Strong phylogenomic support for the geographical hypothesis of rhinoceros evolution•Basal split between African and Eurasian lineages in the early Miocene (∼16 mya)•While all rhinoceroses have low genome diversity, it is lowest in modern-day ones The comparison of de novo genomes from the white, black, Sumatran, and greater one-horned rhinoceroses with the genomes of a historic Javan rhinoceros and three extinct Pleistocene species resolves the evolutionary relationships within the Rhinocerotidae family and reveals that low genetic diversity is a long-term feature of rhinoceroses.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>34433011</pmid><doi>10.1016/j.cell.2021.07.032</doi><orcidid>https://orcid.org/0000-0002-6978-6633</orcidid><orcidid>https://orcid.org/0000-0002-7985-138X</orcidid><orcidid>https://orcid.org/0000-0002-2733-7776</orcidid><orcidid>https://orcid.org/0000-0002-6449-0219</orcidid><orcidid>https://orcid.org/0000-0002-3921-0262</orcidid><orcidid>https://orcid.org/0000-0003-3447-2316</orcidid><orcidid>https://orcid.org/0000-0002-6488-1527</orcidid><orcidid>https://orcid.org/0000-0002-2131-8072</orcidid><orcidid>https://orcid.org/0000-0001-8118-8313</orcidid><orcidid>https://orcid.org/0000-0003-0478-3930</orcidid><orcidid>https://orcid.org/0000-0002-1324-7489</orcidid><orcidid>https://orcid.org/0000-0003-3121-5197</orcidid><orcidid>https://orcid.org/0000-0003-4216-2924</orcidid><orcidid>https://orcid.org/0000-0003-1371-219X</orcidid><orcidid>https://orcid.org/0000-0001-9122-1818</orcidid><orcidid>https://orcid.org/0000-0002-5597-3075</orcidid><orcidid>https://orcid.org/0000-0001-6307-8188</orcidid><oa>free_for_read</oa></addata></record>
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1097-4172
1097-4172
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source MEDLINE; NORA - Norwegian Open Research Archives; Elsevier ScienceDirect Journals Complete; Cell Press Free Archives; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals
subjects Animal biology
Animals
Demography
Environmental Sciences
Evolution, Molecular
Gene Flow
Genetic Variation
Genome
Geography
Heterozygote
Homozygote
Host Specificity
Life Sciences
Markov Chains
Matematikk og Naturvitenskap: 400
Mathematics and natural science: 400
Mutation - genetics
Perissodactyla - genetics
Phylogeny
Rhinoceros, Perissodactyl, Conservation genomics, Phylogenomics, Genomic diversity
Species Specificity
Time Factors
VDP
Zoological anatomy: 481
Zoologisk anatomi: 481
Zoologiske og botaniske fag: 480
Zoology and botany: 480
title Ancient and modern genomes unravel the evolutionary history of the rhinoceros family
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