Long-term population decline and recombination heterogeneity shape genomic diversity in the American alligator

Abstract

The loss of genetic diversity caused by population bottlenecks can significantly impact the ability of a species to adapt to disease, natural disasters, and changing environments. Over the last 175, years, American alligator (A. mississippiensis) populations underwent a decline due to habitat destruction and exploitation followed by a rebound resulting from dedicated conservation efforts. Despite a current census population of millions, microsatellite data indicates a significant paucity of genetic variation within alligators. Using whole genome sequences from 19 individuals sampled from the species geographic range, we quantified nucleotide diversity, heterozygosity, inbreeding, demographic history, and fine-scale recombination rates. We find that American alligator genomes exhibit low nucleotide diversity and elevated homozygosity relative to many vertebrates, but these patterns are dominated by numerous short runs of homozygosity (ROHs), rather than long tracts indicative of recent inbreeding. Demographic history reconstruction based on site-frequency-spectrum analyses support a prolonged decline in effective population size beginning in the last glacial period, indicating that this reduced genetic diversity largely predates intensive human exploitation. Additionally, we uncover a highly structured recombination landscape, with recombination consistently elevated at distal chromosomal regions and suppressed across large central segments. This heterogeneity is associated with genomic spatial variation in nucleotide diversity, suggesting that the recombination landscape contributes to the persistence of homozygosity following population expansion. Together, our results highlight that demographic recovery does not necessarily equate to genetic recovery and show how long-term population history and genomic architecture continue to shape diversity in a "recovered" species.