Genome-wide signatures of complex introgression and adaptive evolution in the big cats

Henrique V. Figueiró; Gang Li; Fernanda J. Trindade; Juliana Assis; Fabiano Pais; Gabriel Fernandes; Sarah H. D. Santos; Graham M. Hughes; Aleksey Komissarov; Agostinho Antunes; Cristine S. Trinca; Maíra R. Rodrigues; Tyler Linderoth; Ke Bi; Leandro Silveira; Fernando C. C. Azevedo; Daniel Kantek; Emiliano Ramalho; Ricardo A. Brassaloti; Priscilla M. S. Villela; Adauto L. V. Nunes; Rodrigo H. F. Teixeira; Ronaldo G. Morato; Damian Loska; Patricia Saragüeta; Toni Gabaldón; Emma C. Teeling; Stephen J. O'Brien; Rasmus Nielsen; Luiz L. Coutinho; Guilherme Oliveira; William J. Murphy; Eduardo Eizirik

doi:10.1126/sciadv.1700299

Genome-wide signatures of complex introgression and adaptive evolution in the big cats

Henrique V. Figueiró, Gang Li, Fernanda J. Trindade, Juliana Assis, Fabiano Pais, Gabriel Fernandes, Sarah H. D. Santos, Graham M. Hughes, Aleksey Komissarov, Agostinho Antunes, Cristine S. Trinca, Maíra R. Rodrigues, Tyler Linderoth, Ke Bi, Leandro Silveira, Fernando C. C. Azevedo, Daniel Kantek, Emiliano Ramalho, Ricardo A. Brassaloti, Priscilla M. S. VillelaAdauto L. V. Nunes, Rodrigo H. F. Teixeira, Ronaldo G. Morato, Damian Loska, Patricia Saragüeta, Toni Gabaldón, Emma C. Teeling, Stephen J. O'Brien, Rasmus Nielsen, Luiz L. Coutinho, Guilherme Oliveira, William J. Murphy^*, Eduardo Eizirik

^*Corresponding author for this work

38 Citations (Scopus)

Abstract

The great cats of the genus Panthera comprise a recent radiation whose evolutionary history is poorly understood. Their rapid diversification poses challenges to resolving their phylogenywhile offering opportunities to investigate the historical dynamics of adaptive divergence. We report the sequence, de novo assembly, and annotation of the jaguar (Panthera onca) genome, a novel genome sequence for the leopard (Panthera pardus), and comparative analyses encompassing all living Panthera species. Demographic reconstructions indicated that all of these species have experienced variable episodes of population decline during the Pleistocene, ultimately leading to small effective sizes in present-day genomes. We observed pervasive genealogical discordance across Panthera genomes, caused by both incomplete lineage sorting and complex patterns of historical interspecific hybridization. We identified multiple signatures of species-specific positive selection, affecting genes involved in craniofacial and limb development, protein metabolism, hypoxia, reproduction, pigmentation, and sensory perception. There was remarkable concordance in pathways enriched in genomic segments implicated in interspecies introgression and in positive selection, suggesting that these processes were connected. We tested this hypothesis by developing exome capture probes targeting ~19,000 Panthera genes and applying them to 30 wild-caught jaguars. We found at least two genes (DOCK3 and COL4A5, both related to optic nerve development) bearing significant signatures of interspecies introgression and within-species positive selection. These findings indicate that post-speciation admixture has contributed genetic material that facilitated the adaptive evolution of big cat lineages.

Original language	English
Article number	e1700299
Journal	Science Advances
Volume	3
Issue number	7
Number of pages	13
ISSN	2375-2548
DOIs	https://doi.org/10.1126/sciadv.1700299
Publication status	Published - 1 Jan 2017
Externally published	Yes

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Genome-wide signatures of complex introgression and adaptive evolution in the big catsFinal published version, 0.98 MBLicence: CC BY-NC

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Figueiró, H. V., Li, G., Trindade, F. J., Assis, J., Pais, F., Fernandes, G., Santos, S. H. D., Hughes, G. M., Komissarov, A., Antunes, A., Trinca, C. S., Rodrigues, M. R., Linderoth, T., Bi, K., Silveira, L., Azevedo, F. C. C., Kantek, D., Ramalho, E., Brassaloti, R. A., ... Eizirik, E. (2017). Genome-wide signatures of complex introgression and adaptive evolution in the big cats. Science Advances, 3(7), Article e1700299. https://doi.org/10.1126/sciadv.1700299

Figueiró, HV, Li, G, Trindade, FJ, Assis, J, Pais, F, Fernandes, G, Santos, SHD, Hughes, GM, Komissarov, A, Antunes, A, Trinca, CS, Rodrigues, MR, Linderoth, T, Bi, K, Silveira, L, Azevedo, FCC, Kantek, D, Ramalho, E, Brassaloti, RA, Villela, PMS, Nunes, ALV, Teixeira, RHF, Morato, RG, Loska, D, Saragüeta, P, Gabaldón, T, Teeling, EC, O'Brien, SJ, Nielsen, R, Coutinho, LL, Oliveira, G, Murphy, WJ & Eizirik, E 2017, 'Genome-wide signatures of complex introgression and adaptive evolution in the big cats', Science Advances, vol. 3, no. 7, e1700299. https://doi.org/10.1126/sciadv.1700299

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title = "Genome-wide signatures of complex introgression and adaptive evolution in the big cats",

abstract = "The great cats of the genus Panthera comprise a recent radiation whose evolutionary history is poorly understood. Their rapid diversification poses challenges to resolving their phylogenywhile offering opportunities to investigate the historical dynamics of adaptive divergence. We report the sequence, de novo assembly, and annotation of the jaguar (Panthera onca) genome, a novel genome sequence for the leopard (Panthera pardus), and comparative analyses encompassing all living Panthera species. Demographic reconstructions indicated that all of these species have experienced variable episodes of population decline during the Pleistocene, ultimately leading to small effective sizes in present-day genomes. We observed pervasive genealogical discordance across Panthera genomes, caused by both incomplete lineage sorting and complex patterns of historical interspecific hybridization. We identified multiple signatures of species-specific positive selection, affecting genes involved in craniofacial and limb development, protein metabolism, hypoxia, reproduction, pigmentation, and sensory perception. There was remarkable concordance in pathways enriched in genomic segments implicated in interspecies introgression and in positive selection, suggesting that these processes were connected. We tested this hypothesis by developing exome capture probes targeting ~19,000 Panthera genes and applying them to 30 wild-caught jaguars. We found at least two genes (DOCK3 and COL4A5, both related to optic nerve development) bearing significant signatures of interspecies introgression and within-species positive selection. These findings indicate that post-speciation admixture has contributed genetic material that facilitated the adaptive evolution of big cat lineages.",

author = "Figueir{\'o}, {Henrique V.} and Gang Li and Trindade, {Fernanda J.} and Juliana Assis and Fabiano Pais and Gabriel Fernandes and Santos, {Sarah H. D.} and Hughes, {Graham M.} and Aleksey Komissarov and Agostinho Antunes and Trinca, {Cristine S.} and Rodrigues, {Ma{\'i}ra R.} and Tyler Linderoth and Ke Bi and Leandro Silveira and Azevedo, {Fernando C. C.} and Daniel Kantek and Emiliano Ramalho and Brassaloti, {Ricardo A.} and Villela, {Priscilla M. S.} and Nunes, {Adauto L. V.} and Teixeira, {Rodrigo H. F.} and Morato, {Ronaldo G.} and Damian Loska and Patricia Sarag{\"u}eta and Toni Gabald{\'o}n and Teeling, {Emma C.} and O'Brien, {Stephen J.} and Rasmus Nielsen and Coutinho, {Luiz L.} and Guilherme Oliveira and Murphy, {William J.} and Eduardo Eizirik",

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T1 - Genome-wide signatures of complex introgression and adaptive evolution in the big cats

AU - Figueiró, Henrique V.

AU - Li, Gang

AU - Trindade, Fernanda J.

AU - Assis, Juliana

AU - Pais, Fabiano

AU - Fernandes, Gabriel

AU - Santos, Sarah H. D.

AU - Hughes, Graham M.

AU - Komissarov, Aleksey

AU - Antunes, Agostinho

AU - Trinca, Cristine S.

AU - Rodrigues, Maíra R.

AU - Linderoth, Tyler

AU - Bi, Ke

AU - Silveira, Leandro

AU - Azevedo, Fernando C. C.

AU - Kantek, Daniel

AU - Ramalho, Emiliano

AU - Brassaloti, Ricardo A.

AU - Villela, Priscilla M. S.

AU - Nunes, Adauto L. V.

AU - Teixeira, Rodrigo H. F.

AU - Morato, Ronaldo G.

AU - Loska, Damian

AU - Saragüeta, Patricia

AU - Gabaldón, Toni

AU - Teeling, Emma C.

AU - O'Brien, Stephen J.

AU - Nielsen, Rasmus

AU - Coutinho, Luiz L.

AU - Oliveira, Guilherme

AU - Murphy, William J.

AU - Eizirik, Eduardo

PY - 2017/1/1

Y1 - 2017/1/1

N2 - The great cats of the genus Panthera comprise a recent radiation whose evolutionary history is poorly understood. Their rapid diversification poses challenges to resolving their phylogenywhile offering opportunities to investigate the historical dynamics of adaptive divergence. We report the sequence, de novo assembly, and annotation of the jaguar (Panthera onca) genome, a novel genome sequence for the leopard (Panthera pardus), and comparative analyses encompassing all living Panthera species. Demographic reconstructions indicated that all of these species have experienced variable episodes of population decline during the Pleistocene, ultimately leading to small effective sizes in present-day genomes. We observed pervasive genealogical discordance across Panthera genomes, caused by both incomplete lineage sorting and complex patterns of historical interspecific hybridization. We identified multiple signatures of species-specific positive selection, affecting genes involved in craniofacial and limb development, protein metabolism, hypoxia, reproduction, pigmentation, and sensory perception. There was remarkable concordance in pathways enriched in genomic segments implicated in interspecies introgression and in positive selection, suggesting that these processes were connected. We tested this hypothesis by developing exome capture probes targeting ~19,000 Panthera genes and applying them to 30 wild-caught jaguars. We found at least two genes (DOCK3 and COL4A5, both related to optic nerve development) bearing significant signatures of interspecies introgression and within-species positive selection. These findings indicate that post-speciation admixture has contributed genetic material that facilitated the adaptive evolution of big cat lineages.

AB - The great cats of the genus Panthera comprise a recent radiation whose evolutionary history is poorly understood. Their rapid diversification poses challenges to resolving their phylogenywhile offering opportunities to investigate the historical dynamics of adaptive divergence. We report the sequence, de novo assembly, and annotation of the jaguar (Panthera onca) genome, a novel genome sequence for the leopard (Panthera pardus), and comparative analyses encompassing all living Panthera species. Demographic reconstructions indicated that all of these species have experienced variable episodes of population decline during the Pleistocene, ultimately leading to small effective sizes in present-day genomes. We observed pervasive genealogical discordance across Panthera genomes, caused by both incomplete lineage sorting and complex patterns of historical interspecific hybridization. We identified multiple signatures of species-specific positive selection, affecting genes involved in craniofacial and limb development, protein metabolism, hypoxia, reproduction, pigmentation, and sensory perception. There was remarkable concordance in pathways enriched in genomic segments implicated in interspecies introgression and in positive selection, suggesting that these processes were connected. We tested this hypothesis by developing exome capture probes targeting ~19,000 Panthera genes and applying them to 30 wild-caught jaguars. We found at least two genes (DOCK3 and COL4A5, both related to optic nerve development) bearing significant signatures of interspecies introgression and within-species positive selection. These findings indicate that post-speciation admixture has contributed genetic material that facilitated the adaptive evolution of big cat lineages.

U2 - 10.1126/sciadv.1700299

DO - 10.1126/sciadv.1700299

M3 - Journal article

C2 - 28776029

AN - SCOPUS:85041388083

SN - 2375-2548

VL - 3

JO - Science Advances

JF - Science Advances

IS - 7

M1 - e1700299

ER -

Genome-wide signatures of complex introgression and adaptive evolution in the big cats

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