Voles and lemmings (subfamily Arvicolinae) remain some of the most difficult groups for disentangling phylogenetic relations owing to recent and very fast explosive radiation. The rapid radiation events are challenging for phylogenetic analysis and produce bushes of various shapes that are impossible to resolve with a straightforward approach using individual loci. Here using the quaddRAD-seq technique and transcriptomes, we tested whether data from the nuclear genome are consistent with trees inferred earlier from individual loci and from mitogenomes in topology and divergence dating. Both the transcriptome and quaddRAD-seq data convincingly place Arvicola as the earliest derivative within Arvicolini. This result is in agreement with the fossil record and conventional taxonomy. For the first time, whole-genome sequencing data resolved relations within the third radiation wave of the subfamily’s taxa, namely the tribes Arvicolini, Lagurini, and Ellobiusini, which have formed polytomy in mitochondrial trees in earlier articles. This study indicates that divergence dating is highly dependent on the number and position of calibration points in a tree and on taxa sampling. In terms of phylogenetic inference, the position of nodes with insufficient taxa representation is the most susceptible to errors.

True lemmings (genus Lemmus) underwent substantial range shifts during the Late Pleistocene and the Pleistocene-Holocene transition, but the impact of these events on present-day diversity remains poorly understood. Here, we used whole-genome sequencing data from modern and ancient samples across the Palearctic range to address this knowledge gap. Reconstruction of autosomal phylogeny revealed that Palearctic true lemmings exhibit relatively shallow genetic structure, contrasting with the deep divergence inferred from mitochondrial genomes. Genetic variation largely follows an isolation-by-distance pattern, and no elevated nuclear divergence was detected between the major mitochondrial lineages. Window-based phylogenetic analyses identified several peripheral populations with high concordance factors, including Norway and Amur lemmings. The high degree of phylogenetic concordance along the genome in these populations is likely a consequence of postglacial bottlenecks and isolation, as indicated by reduced heterozygosity and the presence of runs of homozygosity in them. Overall, our results indicate that the modern genomic structure of Palearctic lemmings was shaped primarily by range fragmentation and population isolation following the broad distribution of the genus during the Last Glacial Maximum. Thus, the current genetic structure appears to represent only a fraction of the Late Pleistocene true lemming diversity. This is illustrated by a genetically distinct ancient specimen (~40 ka BP) from the Indigirka River basin that does not cluster with any modern lineage. From a taxonomic perspective, these findings do not support strong species-level differentiation among the major Palearctic lineages and highlight the discrepancy between mitochondrial and nuclear patterns of diversity within the genus.

The voles and lemmings (subfamily Arvicolinae) remain one of the most difficult groups for disentangling phylogenetic relationships due to recent and very fast explosive radiation. The rapid radiations are challenging for phylogenetic analysis producing bushes of various forms impossible to resolve with a straightforward approach using individual loci. Here using quaddRADseq technique and comprehensive sample and transcriptomes on a limited sample we test whether the data from the nuclear genome are consistent with the trees inferred earlier in topology and divergence dating and evaluate the relative influence of sample number versus number of molecular markers. The study demonstrates that most plausible and reliable dated phylogeny of Arvicolinae at the supraspecies level is given by nuclear data. At the same time, the divergence dating is highly dependent on the number and position of calibration points at the tree and sample number. The most vulnerable for phylogenetic inference is the position of nodes with insufficient taxa sample. The challenge of rapid radiation in phylogeny reconstruction is easier to overcome when the number of recent taxa is not less than the number of extinctions. The robust resolution may be achieved only by accounting both the number of molecular markers and the sample size.