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

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

doi:10.1038/s41467-019-12741-1

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.

Highlights

Today, pumas are among the most widely distributed mammals in the Western hemisphere, ranging from Canada’s Yukon to the southern tip of South America (Fig. 1)[10,11]
We present a draft assembly of a puma genome, which we use to reconstruct the demographic history of the species and measure genome-wide heterozygosity and runs of homozygosity (ROH), the latter of which is less practical with lower-quality or reference-guided genome assemblies
We showed that extant North American pumas are descended from a population that dispersed northward from South America by at least 200 kya, consistent with the age of the oldest puma fossils in North America

Summary

Introduction

Pumas are among the most widely distributed mammals in the Western hemisphere, ranging from Canada’s Yukon to the southern tip of South America (Fig. 1)[10,11]. During the 19th and 20th centuries, bounty hunting reduced, and in some cases extirpated, puma populations across North America[10], restricting them to the North American West and the southern. The absence of observed phenotypic defects in the Everglades population may be attributable to the release during the 1950s and 1960s of captive-bred Florida panthers with mixed Central American ancestry into Everglades National Park. The introduced individuals’ ancestry was unclear at the time of release, it was known that the captive population had greater reproductive success than wild Florida panthers[20]. The admixed ancestry of the Everglades population and potential explanation for the reproductive success of the captive population was later discovered through genotyping[21]

Methods

Results

Conclusion