Whole genomes reveal how Andean climate history shapes genetic diversity and modern conservation risk in South American pumas

Abstract

Climatic oscillations in the Andes have repeatedly reshaped habitats over millions of years, yet their long-term genomic consequences for wide-ranging carnivores remain unclear. We generated whole-genome sequences from pumas (Puma concolor) across ecologically distinct regions of Ecuador to test how paleoclimate shaped population structure, demography, and genetic load. We show that northwestern forest pumas persisted in long-term isolation within humid refugia, whereas northern Andean and southern Pacific populations reconnected intermittently during warm interglacial periods. Southern coastal pumas maintained persistently small effective population sizes, leading to elevated runs of homozygosity and increased burdens of homozygous loss-of-function variants. In contrast, northern populations historically remained larger but exhibit early signs of inbreeding in one individual, marked by long runs of homozygosity and a kinked tail phenotype. Our findings indicate that recent fragmentation may be disrupting historical connectivity. Restoring corridors around the western foothills could reestablish gene flow and reduce inbreeding risk, while targeted genetic rescue may support chronically isolated southern populations. By integrating paleoclimate history with genome-wide data, we provide a framework for region-specific conservation strategies that balance connectivity restoration with the preservation of local adaptation.