First genomic evidence of inbreeding in South American pumas and the role of Andean climate history in shaping genetic diversity

Abstract Climatic oscillations in the Andes have repeatedly reshaped habitats over millions of years, yet their long-term genomic consequences for carnivores with broad geographic distributions remain unclear. Given the long evolutionary history of pumas ( Puma concolor ) in South America, the continent has long been considered a reservoir of genetic diversity. Here, we generated whole-genome sequences from pumas across ecologically distinct regions of Ecuador to test how paleoclimate shaped population structure and demography, and to assess patterns of contemporary genetic diversity across populations. Our results suggest that northwestern forest pumas persisted within environmentally stable habitats over the last 100 kyr, while periods of greater climatic similarity around 17 kya may have reduced environmental barriers and provided conditions more favorable for habitat connectivity and puma dispersal along the western Andean and Pacific coastal regions. On a more recent timescale, our results suggest that the collapse of Indigenous human populations around 400 years ago may have promoted a marked increase in puma population size. Despite this, we provide the first evidence of inbreeding in South American pumas, indicating that recent fragmentation over the last 70 years is disrupting historically connected populations. Together, our findings suggest that Ecuadorian pumas have experienced contrasting historical demographic and evolutionary trajectories and, consequently, may face different contemporary conservation risks. Northwestern populations require corridor restoration to preserve gene flow, whereas isolated southern populations may need more targeted interventions to prevent further genomic erosion.