Systematics, biogeography and phylogenomics of northern bog lemmings (Cricetidae), cold-temperate rodents of conservation concern under global change

Abstract

Northern bog lemmings, Mictomys (Synaptomys) borealis, are currently being assessed for protections under the U.S. Endangered Species Act. A major impediment to comprehensive evaluation is a deficiency of data towards understanding the biology of these rodents. Inherent rarity and scarce specimen sampling, despite a continent-wide distribution, has precluded our ability to implement modern methods for resolving taxonomy, evolutionary history, and investigating multiple other species traits. Here we use a maternally inherited locus (mitochondrial cytochrome b) and between 5939 and 11 513 nuclear loci from reduced representation sequencing (ddRADseq) to investigate the evolutionary history of northern bog lemmings. We (1) qualify evidence based on morphological and early molecular studies for the genus assignment of Mictomys, (2) test the validity of multiple sub-species designations, (3) provide spatial and temporal historical biogeographic perspectives, and (4) discuss how incomplete sampling might influence conservation efforts. Both mitochondrial and nuclear datasets exhibit deep divergence and paraphyly between two recognized species, the northern (Mictomys borealis) and southern (Synaptomys cooperi) bog lemmings. Based on mtDNA, the geographically isolated subspecies (M. b. sphagnicola) was found to be divergent from all other specimens. The remainder of the species exhibited shallow intra-specific differentiation in mtDNA, however, nuclear data supports genetic distinction consistent with four geographic subspecies. Recent coalescence of all northern bog lemmings (except for M. b. sphagnicola) reflects divergence in multiple refugia through the last glacial cycle, including a well-known coastal center of endemism and multiple regions south of continental ice sheets. Regional lineages across North America suggest strong latitudinal displacement with global climate change, coupled with isolation-reconnection dynamics. This taxon suffers from a lack of modern samples through most of its distribution, severely limiting the interpretation of ongoing evolutionary processes, particularly in southern portions of the species’ range. Limited voucher specimen sampling of vulnerable populations could aid in rigorous conservation decision-making.