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


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Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)

FAPERGS/Brazil

Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG)

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Morris Animal Foundation

Russian Science Foundation

Russian Ministry of Science

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 phylogeny while 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 similar to 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.

Pontificial Catholic Univ Rio Grande Sul PUCRS, Lab Biol Genom & Mol, Fac Biociencias, Porto Alegre, RS, Brazil

Texas A&M Univ, Dept Vet Integrat Biosci, College Stn, TX 77843 USA

FIOCRUZ Minas, Ctr Pesquisa Rene Rachou, Belo Horizonte, MG, Brazil

Univ Coll Dublin, Sch Biol & Environm Sci, Dublin, Ireland

St Petersburg State Univ, Theodosius Dobzhansky Ctr Genome Bioinformat, St Petersburg, Russia

Univ Porto, Dept Biol, Fac Ciencias, Oporto, Portugal

Univ Porto, CIIMAR CIMAR, Oporto, Portugal

Univ Calif Berkeley, Dept Integrat Biol, Berkeley, CA 94720 USA

Univ Calif Berkeley, Calif Inst Quantitat Biosci, Computat Genom Resource Lab, Berkeley, CA 94720 USA

Univ Calif Berkeley, Museum Vertebrate Zool, Berkeley, CA 94720 USA

Inst Onca Pintada, Mineiros, Go, Brazil

Univ Fed Sao Joao, Sao Joao Del Rei, MG, Brazil

Inst Pro Carnivoros, Atibaia, SP, Brazil

Inst Chico Mendes Conservacao Biodiversida, Brasilia, DF, Brazil

Inst Desenvolvimento Sustentavel Mamiraua, Tefe, Amazonas, Brazil

Univ Sao Paulo, ESALQ, Piracicaba, SP, Brazil

Zool Municipal Sorocaba, Sorocaba, SP, Brazil

Univ Estadual Paulista Botucatu, Programa Posgrad Anim Selvagens, Sao Paulo, Brazil

Ctr Genom Regulat CRG, Bioinformat & Genom Programme, Barcelona, Spain

Univ Pompeu Fabra, Barcelona, Spain

Inst Biol & Med Expt, Buenos Aires, DF, Argentina

ICREA, Barcelona, Spain

Inst Tecnol Vale, Belem, Para, Brazil

Univ Estadual Paulista Botucatu, Programa Posgrad Anim Selvagens, Sao Paulo, Brazil

CNPq: 311327/2011-7

CNPq: 487396/2012-0

CNPq: 309312/2012-4

FAPERGS/Brazil: 12/2236-0

FAPEMIG: RED-00014-14

Morris Animal Foundation: D12FE-019

Morris Animal Foundation: D12FE-502

Russian Science Foundation: 17-14-01138

Russian Ministry of Science: 11.G34.31.0068

Document Type Journal article
Language English
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