Genomic Evidence for the Purging of Deleterious Genetic Variation in the Endangered North Atlantic Right Whale.

Abstract

The reduced genetic diversity and frequent inbreeding associated with small population size may underpin the accumulation and expression of deleterious mutations (mutation load) in some declining populations. However, demographic perturbations and inbreeding coupled with purifying selection can also purge declining populations of deleterious mutations, leading to intriguing recoveries. To better understand the links between deleterious genetic variation and population status, we assess patterns of genetic diversity, inbreeding, and mutation load across the genomes of three species of Balaenidae whale with different demographic histories and recoveries following the end of commercial whaling in the 1980s. Unlike bowhead (BH) and Southern right whales (SRW), which show signs of recent recovery, reproductive rates of the endangered North Atlantic right whale (NARW) remain lower than expected. We show that the NARW is currently marked by low genetic diversity, historical inbreeding, and a high mutation load. Still, we reveal evidence that genetic purging has reduced the frequency of highly deleterious alleles in NARW, which could increase chances of future population recovery. We also identify a suite of mutations putatively linked to congenital defects that occur at high frequencies in nulliparous NARW females but are rare in NARW with high reproductive success. These same mutations are nearly absent in BH and SRW in this study, suggesting that the purging of key variants may shape the probability of population recovery. As anthropogenic disturbances continue to reduce the sizes of many populations in nature, resolving the links between population dynamics and mutation load could become increasingly important.