Puma genomes from North and South America provide insights into the genomic consequences of inbreeding

Nedda F. Saremi; Megan A. Supple; Ashley Byrne; James A. Cahill; Luiz Lehmann Coutinho; Love Dalén; Henrique V. Figueiró; Warren E. Johnson; Heather J. Milne; Stephen J. O’Brien; Brendan O’Connell; David P. Onorato; Seth P.D. Riley; Jeff A. Sikich; Daniel R. Stahler; Priscilla Marqui Schmidt Villela; Christopher Vollmers; Robert K. Wayne; Eduardo Eizirik; Russell B. Corbett-Detig; Richard E. Green; Christopher C. Wilmers; Beth Shapiro; Stephen James O'Brien

doi:10.1038/s41467-019-12741-1

Puma genomes from North and South America provide insights into the genomic consequences of inbreeding

Nedda F. Saremi
, Megan A. Supple
, Ashley Byrne
, James A. Cahill
, Luiz Lehmann Coutinho
, Love Dalén
, Henrique V. Figueiró
, Warren E. Johnson
, Heather J. Milne
, Stephen J. O’Brien
, Brendan O’Connell
, David P. Onorato
, Seth P.D. Riley
, Jeff A. Sikich
, Daniel R. Stahler
, Priscilla Marqui Schmidt Villela
, Christopher Vollmers
, Robert K. Wayne
, Eduardo Eizirik
, Russell B. Corbett-Detig

Richard E. Green, Christopher C. Wilmers, Beth Shapiro, Stephen James O'Brien

Research output: Contribution to journal › Article › peer-review

83 Scopus citations

Abstract

Pumas are the most widely distributed felid in the Western Hemisphere. Increasingly, however, human persecution and habitat loss are isolating puma populations. To explore the genomic consequences of this isolation, we assemble a draft puma genome and a geographically broad panel of resequenced individuals. We estimate that the lineage leading to present-day North American pumas diverged from South American lineages 300–100 thousand years ago. We find signatures of close inbreeding in geographically isolated North American populations, but also that tracts of homozygosity are rarely shared among these populations, suggesting that assisted gene flow would restore local genetic diversity. The genome of a Florida panther descended from translocated Central American individuals has long tracts of homozygosity despite recent outbreeding. This suggests that while translocations may introduce diversity, sustaining diversity in small and isolated populations will require either repeated translocations or restoration of landscape connectivity. Our approach provides a framework for genome-wide analyses that can be applied to the management of similarly small and isolated populations.

Original language	American English
Article number	4769
Journal	Nature Communications
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-12741-1
State	Published - Dec 1 2019

Bibliographical note

Publisher Copyright:
© 2019, The Author(s).

Funding

We thank Paul Houghtaling for helping to collect samples, R. Miotto, E. Amorim, J. May, CENAP/ICMBio/Brazil and AMC/Brazil for access to samples, and S. Webber and C. Scelfo-Dalbey for assistance in generating sequencing data. The authors would like to acknowledge support from Science for Life Laboratory, the National Genomics Infrastructure, and UPPMAX for providing assistance in massive parallel sequencing and computational infrastructure. Sequencing was also performed by the Laborató de Biotecnologia Animal at the Universidade de Sã Paulo in Brazil, UC San Diego Institute for Genomic Medicine Genomics Center, UC Berkeley Vincent J. Coates Genomics Sequencing Laboratory, and UC Santa Cruz Ancient and Degraded Processing Center. Funding was provided by the Blue Foundation, and by a grant to C.C.W. from the Gordon and Betty Moore Foundation. C.C.W. was funded in part by NSF grants 1255913 and 0963022. B.S., M.A.S., N.F.S., and R.K.W. were funded by a grant from the University of California Office of the President. N.F.S. was funded in part by T32 HG008345/ HG/NHGRI NIH HHS/United States. L.D. was funded by Formas grant 2015-676. D.R.S. was funded in part by Yellowstone Forever. R.B.C.-D. was funded by NIH-R35GM128932. B.S. and R.E.G. were funded in part by NSF DEB-1754551. E.E., L.L.C., and H.V.F. were supported by funds from CNPq/Brazil and INCT-EECBio/Brazil.

Funders	Funder number
Blue Foundation
CNPq/Brazil
INCT-EECBio/Brazil
NIH-R35GM128932
Yellowstone Forever
National Science Foundation	DEB-1754551, 0963022, 1255913
National Science Foundation
National Human Genome Research Institute	T32HG008345
National Human Genome Research Institute
Gordon and Betty Moore Foundation
University of California
Office of the President, University of California
Svenska Forskningsrådet Formas	2015-676
Svenska Forskningsrådet Formas
Science for Life Laboratory
Uppsala Multidisciplinary Center for Advanced Computational Science

ASJC Scopus Subject Areas

General Chemistry
General Biochemistry,Genetics and Molecular Biology
General Physics and Astronomy

Keywords

Animals
Gene Flow
Genetic Variation
Genetics, Population
Genome-Wide Association Study/methods
Genomics/methods
Geography
Inbreeding/methods
North America
Phylogeny
Puma/classification
South America

Disciplines

Genetics and Genomics
Life Sciences

Access to Document

10.1038/s41467-019-12741-1

https://doi.org/10.1038/s41467-019-12741-1

Cite this

Saremi, N. F., Supple, M. A., Byrne, A., Cahill, J. A., Coutinho, L. L., Dalén, L., Figueiró, H. V., Johnson, W. E., Milne, H. J., O’Brien, S. J., O’Connell, B., Onorato, D. P., Riley, S. P. D., Sikich, J. A., Stahler, D. R., Villela, P. M. S., Vollmers, C., Wayne, R. K., Eizirik, E., ... O'Brien, S. J. (2019). Puma genomes from North and South America provide insights into the genomic consequences of inbreeding. Nature Communications, 10(1), Article 4769. https://doi.org/10.1038/s41467-019-12741-1

Saremi, NF, Supple, MA, Byrne, A, Cahill, JA, Coutinho, LL, Dalén, L, Figueiró, HV, Johnson, WE, Milne, HJ, O’Brien, SJ, O’Connell, B, Onorato, DP, Riley, SPD, Sikich, JA, Stahler, DR, Villela, PMS, Vollmers, C, Wayne, RK, Eizirik, E, Corbett-Detig, RB, Green, RE, Wilmers, CC, Shapiro, B & O'Brien, SJ 2019, 'Puma genomes from North and South America provide insights into the genomic consequences of inbreeding', Nature Communications, vol. 10, no. 1, 4769. https://doi.org/10.1038/s41467-019-12741-1

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abstract = " Pumas are the most widely distributed felid in the Western Hemisphere. Increasingly, however, human persecution and habitat loss are isolating puma populations. To explore the genomic consequences of this isolation, we assemble a draft puma genome and a geographically broad panel of resequenced individuals. We estimate that the lineage leading to present-day North American pumas diverged from South American lineages 300–100 thousand years ago. We find signatures of close inbreeding in geographically isolated North American populations, but also that tracts of homozygosity are rarely shared among these populations, suggesting that assisted gene flow would restore local genetic diversity. The genome of a Florida panther descended from translocated Central American individuals has long tracts of homozygosity despite recent outbreeding. This suggests that while translocations may introduce diversity, sustaining diversity in small and isolated populations will require either repeated translocations or restoration of landscape connectivity. Our approach provides a framework for genome-wide analyses that can be applied to the management of similarly small and isolated populations.",

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AU - Coutinho, Luiz Lehmann

AU - Dalén, Love

AU - Figueiró, Henrique V.

AU - Johnson, Warren E.

AU - Milne, Heather J.

AU - O’Brien, Stephen J.

AU - O’Connell, Brendan

AU - Onorato, David P.

AU - Riley, Seth P.D.

AU - Sikich, Jeff A.

AU - Stahler, Daniel R.

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AU - Vollmers, Christopher

AU - Wayne, Robert K.

AU - Eizirik, Eduardo

AU - Corbett-Detig, Russell B.

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AU - Wilmers, Christopher C.

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AB - Pumas are the most widely distributed felid in the Western Hemisphere. Increasingly, however, human persecution and habitat loss are isolating puma populations. To explore the genomic consequences of this isolation, we assemble a draft puma genome and a geographically broad panel of resequenced individuals. We estimate that the lineage leading to present-day North American pumas diverged from South American lineages 300–100 thousand years ago. We find signatures of close inbreeding in geographically isolated North American populations, but also that tracts of homozygosity are rarely shared among these populations, suggesting that assisted gene flow would restore local genetic diversity. The genome of a Florida panther descended from translocated Central American individuals has long tracts of homozygosity despite recent outbreeding. This suggests that while translocations may introduce diversity, sustaining diversity in small and isolated populations will require either repeated translocations or restoration of landscape connectivity. Our approach provides a framework for genome-wide analyses that can be applied to the management of similarly small and isolated populations.

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KW - Inbreeding/methods

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KW - Phylogeny

KW - Puma/classification

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VL - 10

JO - Nature Communications

JF - Nature Communications

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ER -

Puma genomes from North and South America provide insights into the genomic consequences of inbreeding

Abstract

Bibliographical note

Funding

ASJC Scopus Subject Areas

Keywords

Disciplines

Access to Document

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