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

Shanlin Liu; Michael V. Westbury; Nicolas Dussex; Kieren J. Mitchell; Mikkel Holger S. Sinding; Peter D. Heintzman; David A. Duchêne; Joshua D. Kapp; Johanna von Seth; Holly Heiniger; Fátima Sánchez-Barreiro; Ashot Margaryan; Remi André-Olsen; Binia De Cahsan; Guanliang Meng; Chentao Yang; Lei Chen; Tom van der Valk; Yoshan Moodley; Kees Rookmaaker; Michael W. Bruford; Oliver Ryder; Cynthia Steiner; Linda G. R. Bruins-van Sonsbeek; Sergey Vartanyan; Chunxue Guo; Alan Cooper; Pavel Kosintsev; Irina Kirillova; Adrian M. Lister; Tomas Marques-Bonet; Shyam Gopalakrishnan; Robert R. Dunn; Eline D. Lorenzen; Beth Shapiro; Guojie Zhang; Pierre Olivier Antoine; Love Dalén; M. Thomas P. Gilbert

doi:10.1016/j.cell.2021.07.032

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

Shanlin Liu^*, Michael V. Westbury, Nicolas Dussex, Kieren J. Mitchell, Mikkel Holger S. Sinding, Peter D. Heintzman, David A. Duchêne, Joshua D. Kapp, Johanna von Seth, Holly Heiniger, Fátima Sánchez-Barreiro, Ashot Margaryan, Remi André-Olsen, Binia De Cahsan, Guanliang Meng, Chentao Yang, Lei Chen, Tom van der Valk, Yoshan Moodley, Kees RookmaakerMichael W. Bruford, Oliver Ryder, Cynthia Steiner, Linda G. R. Bruins-van Sonsbeek, Sergey Vartanyan, Chunxue Guo, Alan Cooper, Pavel Kosintsev, Irina Kirillova, Adrian M. Lister, Tomas Marques-Bonet, Shyam Gopalakrishnan, Robert R. Dunn, Eline D. Lorenzen, Beth Shapiro, Guojie Zhang, Pierre Olivier Antoine, Love Dalén, M. Thomas P. Gilbert

^*Corresponding author for this work

Research output: Contribution to journal › Journal article › Research › peer-review

48 Citations (Scopus)

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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.

Original language	English
Journal	Cell
Volume	184
Issue number	19
Pages (from-to)	4874-4885.e16
ISSN	0092-8674
DOIs	https://doi.org/10.1016/j.cell.2021.07.032
Publication status	Published - 2021

Bibliographical note

Publisher Copyright:
© 2021 The Authors

Keywords

Rhinoceros, Perissodactyl, Conservation genomics, Phylogenomics, Genomic diversity

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10.1016/j.cell.2021.07.032Licence: CC BY

Ancient and modern genomes unravel the evolutionary history of the rhinoceros familyFinal published version, 6.06 MBLicence: CC BY

Cite this

Liu, S., Westbury, M. V., Dussex, N., Mitchell, K. J., Sinding, M. H. S., Heintzman, P. D., Duchêne, D. A., Kapp, J. D., von Seth, J., Heiniger, H., Sánchez-Barreiro, F., Margaryan, A., André-Olsen, R., De Cahsan, B., Meng, G., Yang, C., Chen, L., van der Valk, T., Moodley, Y., ... Gilbert, M. T. P. (2021). Ancient and modern genomes unravel the evolutionary history of the rhinoceros family. Cell, 184(19), 4874-4885.e16. https://doi.org/10.1016/j.cell.2021.07.032

Ancient and modern genomes unravel the evolutionary history of the rhinoceros family. / 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; Sonsbeek, Linda G. R. Bruins-van; 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.

In: Cell, Vol. 184, No. 19, 2021, p. 4874-4885.e16.

Research output: Contribution to journal › Journal article › Research › peer-review

Liu, S , Westbury, MV, Dussex, N, Mitchell, KJ, Sinding, MHS, Heintzman, PD, Duchêne, DA, Kapp, JD, von Seth, J, Heiniger, H, Sánchez-Barreiro, F, Margaryan, A, André-Olsen, R, De Cahsan, B, Meng, G, Yang, C, Chen, L, van der Valk, T, Moodley, Y, Rookmaaker, K, Bruford, MW, Ryder, O, Steiner, C, Sonsbeek, LGRB, Vartanyan, S, Guo, C, Cooper, A, Kosintsev, P, Kirillova, I, Lister, AM, Marques-Bonet, T, Gopalakrishnan, S , Dunn, RR , Lorenzen, ED, Shapiro, B, Zhang, G, Antoine, PO, Dalén, L & Gilbert, MTP 2021, 'Ancient and modern genomes unravel the evolutionary history of the rhinoceros family', Cell, vol. 184, no. 19, pp. 4874-4885.e16. https://doi.org/10.1016/j.cell.2021.07.032

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 ; Sonsbeek, Linda G. R. Bruins-van ; 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. / Ancient and modern genomes unravel the evolutionary history of the rhinoceros family. In: Cell. 2021 ; Vol. 184, No. 19. pp. 4874-4885.e16.

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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.",

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author = "Shanlin Liu and Westbury, {Michael V.} and Nicolas Dussex and Mitchell, {Kieren J.} and Sinding, {Mikkel Holger S.} and Heintzman, {Peter D.} and Duch{\^e}ne, {David A.} and Kapp, {Joshua D.} and {von Seth}, Johanna and Holly Heiniger and F{\'a}tima S{\'a}nchez-Barreiro and Ashot Margaryan and Remi Andr{\'e}-Olsen and {De Cahsan}, Binia and Guanliang Meng and Chentao Yang and Lei Chen and {van der Valk}, Tom and Yoshan Moodley and Kees Rookmaaker and Bruford, {Michael W.} and Oliver Ryder and Cynthia Steiner and Sonsbeek, {Linda G. R. Bruins-van} and Sergey Vartanyan and Chunxue Guo and Alan Cooper and Pavel Kosintsev and Irina Kirillova and Lister, {Adrian M.} and Tomas Marques-Bonet and Shyam Gopalakrishnan and Dunn, {Robert R.} and Lorenzen, {Eline D.} and Beth Shapiro and Guojie Zhang and Antoine, {Pierre Olivier} and Love Dal{\'e}n and Gilbert, {M. Thomas P.}",

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AU - Westbury, Michael V.

AU - Dussex, Nicolas

AU - Mitchell, Kieren J.

AU - Sinding, Mikkel Holger S.

AU - Heintzman, Peter D.

AU - Duchêne, David A.

AU - Kapp, Joshua D.

AU - von Seth, Johanna

AU - Heiniger, Holly

AU - Sánchez-Barreiro, Fátima

AU - Margaryan, Ashot

AU - André-Olsen, Remi

AU - De Cahsan, Binia

AU - Meng, Guanliang

AU - Yang, Chentao

AU - Chen, Lei

AU - van der Valk, Tom

AU - Moodley, Yoshan

AU - Rookmaaker, Kees

AU - Bruford, Michael W.

AU - Ryder, Oliver

AU - Steiner, Cynthia

AU - Sonsbeek, Linda G. R. Bruins-van

AU - Vartanyan, Sergey

AU - Guo, Chunxue

AU - Cooper, Alan

AU - Kosintsev, Pavel

AU - Kirillova, Irina

AU - Lister, Adrian M.

AU - Marques-Bonet, Tomas

AU - Gopalakrishnan, Shyam

AU - Dunn, Robert R.

AU - Lorenzen, Eline D.

AU - Shapiro, Beth

AU - Zhang, Guojie

AU - Antoine, Pierre Olivier

AU - Dalén, Love

AU - Gilbert, M. Thomas P.

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N2 - 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.

AB - 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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