Genomic analysis of differentiation and demography of the formerly conspecific agile (Dipodomys agilis) and Dulzura (D. simulans) kangaroo rats

Karyotype variation within Pacific kangaroo rat Dipodomys agilis motivated its division in 1997 into the agile kangaroo rat (AKR, D. agilis, 2N = 62) in the north of its range in California, and Dulzura kangaroo rat (DKR, D. simulans, 2N = 60) to the south, with a suspected sympatric zone south of the San Gabriel and San Bernardino Mountains. This division was supported by our whole genome sequencing that sampled a ~120 km transect from north of the mountains to SW Riverside County. The taxa showed marked genetic differentiation, with no evidence of hybridization or sympatry. AKR was found at the southern edge of the mountains, precluding the mountain barrier driving isolation, suggesting ecological separation linked to habitat differences between the mountains and the arid area to the south. Adding four additional Dipodomys species, we estimated genetic divergence times in the genus back to ∼3.5 mya. AKR and DKR diverged from D. stephensi ∼1.7 mya, and from each other ∼0.5 mya, when their joint effective population size (Ne) was ~100,000. After separation, DKR’s Ne declined to ~20,000, while AKR’s was little changed. More recently their Ne converged at ~50,000. Runs of homozygosity were longer in AKR, indicating a smaller neighborhood size, which may have promoted the karyotype change; however, nucleotide diversity was higher in AKR, but both had levels typical for rodents, indicating neither experienced recent bottlenecks. These patterns provide a baseline for any future conservation efforts. More generally, this study shows how a detailed genomic study can resolve taxonomic and demographic questions among morphologically indistinguishable taxa.