Genomic diversity as a key conservation criterion: proof-of-concept from mammalian whole-genome resequencing data

Abstract Many international, national, state, and local organizations prioritize the ranking of threatened and endangered species to help direct conservation efforts. For example, the International Union for Conservation of Nature (IUCN) regularly publishes the influential Red List of Threatened Species. Unfortunately, current approaches to categorizing the conservation status of species do not explicitly consider genetic or genomic diversity (GD), even though GD is positively associated with both contemporary evolutionary fitness and with future evolutionary potential. To test if genome sequences can help improve conservation ranking efforts, we estimated GD metrics from publicly available mammalian population data and examined their statistical association with formal Red List conservation categories. We considered intrinsic biological factors that could impact GD and quantified their relative influences. Key population GD metrics are both reflective and predictive of IUCN conservation categories. Specifically, our analyses revealed that genome-wide heterozygosity and autozygosity (a product of inbreeding) are associated with the current Red List categorization, likely because demographic declines that lead to “listing” decisions also reduce levels of standing genetic variation. We argue that by virtue of this relationship, conservation organizations like IUCN can leverage genome sequence data to help infer conservation status in otherwise data-deficient species. This study 1) outlines the theoretical and empirical justification for a new GD criterion based on the mean loss of genome-wide heterozygosity over time; 2) provides a bioinformatic pipeline for estimating GD from population genomic data; and 3) provides an analytical framework and explicit recommendations for use by conservation authorities.