Mitochondrial structure despite nuclear panmixia: sex-specific dispersal dictates population structure in sperm whales

Abstract

Marine mammals have high potential for dispersal, yet behavioral or environmental constraints can limit gene flow. This is true for the endangered sperm whale, Physeter macrocephalus, which has a global distribution and long-distance migrations. While previous studies revealed mitochondrial population structure with weak nuclear structure globally, genomic approaches examining this pattern have been limited. Understanding connectivity is critical for the management of this species due to population declines relative to pre-whaling, recent impacts from the Deepwater Horizon oil spill, and ongoing threats from anthropogenic sound. We investigated the connectivity between two regions, the U.S. Gulf of America (Mexico) and western North Atlantic Ocean, using reduced representation genomics and mitochondrial control region sequencing of 73 sperm whales. We found that relatedness decreased with geographic distance, likely due to the presence of familial structure. Nuclear markers showed no population structure (FST = 0.001-0.008), while mitochondrial structure was high (FST = 0.36-0.65), consistent with male-biased dispersal and female philopatry. Across all samples, genetic diversity (nuclear: 0.0014; mitochondrial: 0.0017) and effective population size (Ne=460) were low. Given this low diversity and evidence for the partitioning of genetic variation, we recommend managers treat these two regions as distinct in order to preserve existing variation and promote resilience of this species. These results show that despite the increased power of a genomic approach, it is essential to consider the biology of the species at hand and leverage both mitochondrial and nuclear markers to understand the genetic structure of threatened species.