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Sci Adv. 2017 Jul 19;3(7):e1700299. doi: 10.1126/sciadv.1700299. eCollection 2017 Jul.

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

Author information

1
Laboratório de Biologia Genômica e Molecular, Faculdade de Biociências, Pontifical Catholic University of Rio Grande do Sul (PUCRS), Porto Alegre, Rio Grande do Sul, Brazil.
2
Department of Veterinary Integrative Biosciences, Texas A&M University, College Station, TX 77843, USA.
3
Centro de Pesquisa René Rachou, FIOCRUZ/Minas, Belo Horizonte, Minas Gerais, Brazil.
4
School of Biology and Environmental Science, University College Dublin, Dublin, Ireland.
5
Theodosius Dobzhansky Center for Genome Bioinformatics, Saint Petersburg State University, St. Petersburg, Russia.
6
Departamento de Biologia, Faculdade de Ciências and CIIMAR/CIMAR, Universidade do Porto, Porto, Portugal.
7
Department of Integrative Biology, University of California, Berkeley, Berkeley, CA 94720-3140, USA.
8
Computational Genomics Resource Laboratory, California Institute for Quantitative Biosciences and Museum of Vertebrate Zoology, University of California, Berkeley, Berkeley, CA 94720, USA.
9
Instituto Onça-Pintada, Mineiros, Goiás, Brazil.
10
Universidade Federal de São João Del Rey, São João Del Rey, Minas Gerais, Brazil.
11
Instituto Pró-Carnívoros, Atibaia, São Paulo, Brazil.
12
Instituto Chico Mendes de Conservação da Biodiversidade, Brasília, Distrito Federal, Brazil.
13
Instituto de Desenvolvimento Sustentável Mamirauá, Tefé, Amazonas, Brazil.
14
Escola Superior de Agricultura Luiz de Queiroz (ESALQ-USP), Piracicaba, São Paulo, Brazil.
15
Zoológico Municipal de Sorocaba, Sorocaba, São Paulo, Brazil.
16
Programa de Pós-Graduação em Animais Selvagens, Universidade Estadual Paulista-Botucatu, São Paulo, Brazil.
17
Bioinformatics and Genomics Programme, Centre for Genomic Regulation (CRG), Barcelona, Spain.
18
Universitat Pompeu Fabra, Barcelona, Spain.
19
Instituto de Biología y Medicina Experimental, Buenos Aires, Argentina.
20
Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain.
21
Instituto Tecnológico Vale, Belém, Pará, Brazil.

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 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 ~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.

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