Pikas are widely distributed in the Northern Hemisphere and are highly adapted to cold and alpine environments. They are one of the most complex and problematic groups in mammalian systematics, and the origin and evolutionary history of extant pikas remain controversial. In this study, we sequenced the whole coding sequences of 105 pika samples (29 named species and 1 putative new species) and obtained DNA data for more than 10,000 genes. Our phylogenomic analyses recognized four subgenera of extant pikas: Alienauroa, Conothoa, Ochotona, and Pika. The interrelationships between the four subgenera were strongly resolved as (Conothoa, (Alienauroa, (Ochotona, Pika))), with the mountain group Conothoa being the sister group of all other pikas. Our divergence time and phylogeographic analyses indicated that the last common ancestor of extant pikas first occurred on in the middle Miocene, ∼14 Ma. The emergence of opportunities related to the climate, food supply, and spreading paths in concert promoted the dispersal of pikas from the Qinghai-Tibetan Plateau (QTP) to other parts of Eurasia and North America. We found that the genes that were positively selected in the early evolution of pikas were most concentrated in functional categories related to cold tolerance. These results suggest that the QTP may have served as a training ground for cold tolerance in early pikas, which gives pikas a great advantage when the climate continued to cool after the middle Miocene. Our study highlights the importance of the QTP as a center of origin for many cold-adapted animals.

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Pheromones are chemical cues released and sensed by individuals of the same species, which are of major importance in regulating reproductive and social behaviors of mammals. Generally, they are detected by the vomeronasal system (VNS). Here, we first investigated and compared an essential genetic component of vomeronasal chemoreception, that is, TRPC2 gene, of four marine mammals varying the degree of aquatic specialization and related terrestrial species in order to provide insights into the evolution of pheromonal olfaction in the mammalian transition from land to water. Our results based on sequence characterizations and evolutionary analyses, for the first time, show the evidence for the ancestral impairment of vomeronasal pheromone signal transduction pathway in fully aquatic cetaceans, supporting a reduced or absent dependence on olfaction as a result of the complete adaptation to the marine habitat, whereas the amphibious California sea lion was found to have a putatively functional TRPC2 gene, which is still under strong selective pressures, reflecting the reliance of terrestrial environment on chemical recognition among the semiadapted marine mammals. Interestingly, our study found that, unlike that of the California sea lion, TRPC2 genes of the harbor seal and the river otter, both of which are also semiaquatic, are pseudogenes. Our data suggest that other unknown selective pressures or sensory modalities might have promoted the independent absence of a functional VNS in these two species. In this respect, the evolution of pheromonal olfaction in marine mammals appears to be more complex and confusing than has been previously thought. Our study makes a useful contribution to the current understanding of the evolution of pheromone perception of mammals in response to selective pressures from an aquatic environment.

The monophyletic group Caniformia (dog-like carnivores) in the order Carnivora comprises 9 families. Except for the general consensus for the earliest divergence of Canidae and the grouping of Procyonidae and Mustelidae, conflicting phylogenetic hypotheses exist for the other caniformian families. In the present study, a data set comprising > 22 kb of 22 nuclear intron loci from 16 caniformian species is used to investigate the phylogenetic utility of nuclear introns in resolving the interfamilial relationships of Caniformia. Our phylogenetic analyses support Ailuridae as the sister taxon to a clade containing Procyonidae and Mustelidae, with Mephitinae being the sister taxon to all of them. The unresolved placements of Ursidae and Pinnipeds here emphasize a need to add more data and include more taxa to resolve this problem. The present study not only resolves some of the ambiguous relationships in Caniformia phylogeny but also shows that the noncoding nuclear markers can offer powerful complementary data for estimating the species tree. None of the newly developed introns here have previously been used for phylogeny reconstruction, thus increasing the spectrum of molecular markers available to mammalian systematics. Interestingly, all the newly developed intron data partitions exhibit intraindividual allele heterozygotes (IIAHs). There are 115 cases of IIAHs in total. The incorporation of IIAHs into phylogenetic analysis not only provides insights into the interfamilial relationships of Caniformia but also identifies two potential hybridization events occurred within Ursidae and Otariidae, respectively. Finally, the powers and pitfalls of phylogenetics using nuclear introns as markers are discussed in the context of Caniformia phylogeny.

The leptin gene has received intensive attention and scientific investigation for its importance in energy homeostasis and reproductive regulation in mammals. Furthermore, study of the leptin gene is of crucial importance for public health, particularly for its role in obesity, as well as for other numerous physiological roles that it plays in mammals. In the present work, we report the identification of novel leptin genes in 4 species of Cetacea, and a comparison with 55 publicly available leptin sequences from mammalian genome assemblies and previous studies. Our study provides evidence for positive selection in the suborder Odontoceti (toothed whales) of the Cetacea and the family Phocidae (earless seals) of the Pinnipedia. We also detected positive selection in several leptin gene residues in these two lineages. To test whether leptin and its receptor evolved in a coordinated manner, we analyzed 24 leptin receptor gene (LPR) sequences from available mammalian genome assemblies and other published data. Unlike the case of leptin, our analyses did not find evidence of positive selection for LPR across the Cetacea and Pinnipedia lineages. In line with this, positively selected sites identified in the leptin genes of these two lineages were located outside of leptin receptor binding sites, which at least partially explains why co-evolution of leptin and its receptor was not observed in the present study. Our study provides interesting insights into current understanding of the evolution of mammalian leptin genes in response to selective pressures from life in an aquatic environment, and leads to a hypothesis that new tissue specificity or novel physiologic functions of leptin genes may have arisen in both odontocetes and phocids. Additional data from other species encompassing varying life histories and functional tests of the adaptive role of the amino acid changes identified in this study will help determine the factors that promote the adaptive evolution of the leptin genes in marine mammals.

China has 26 species in the tribe Arvicolini. The taxonomic status of these voles remains controversial despite much effort. Herein, we evaluate the taxonomic position of 22 species plus 2 unidentified taxa using mitochondrial DNA gene sequences (cytb + CO1). We also evaluate 18 species and 2 unidentified taxa using morphological data. Phylogenetic analyses of cytb resolve monophyly for the genera Alexandromys, Lasiopodomys, Microtus, Neodon, Proedromys, and Volemys with strong support. Stenocranius clusters with Chionomys but with very weak support. Analyses of concatenated cytb + CO1 resolve the same genera with strong support, but the topology of the tree differs from that of cytb in that Chionomys roots at the base of the tree independent of Stenocranius, which forms the sister-group of Lasiopodomys in a more terminal position. The matrilineal genealogy excludes the type species Arvicola amphibius from the rest of the Arvicolini. This species forms the sister-group of Ondatra with high support. Neodon includes N. irene, N. linzhiensis, N. fuscus, N. leucurus, N. sikimensis, Microtus clarkei, and 2 unidentified specimens. Alexandromys includes the former species Microtus oeconomus, M. kikuchii, M. limnophilus, M. fortis, and M. maximowiczii. Finally, Microtus has the subgenera Blanfordimys, Microtus, Mynomes, Pedomys, Pitymys, and Terricola, which includes the Chinese species M. agrestis, M. arvalis, and Blanfordimys juldaschi. General mixed Yule-coalescent species delimitation modeling demarcates 6 currently recognized species and 2 new species of Neodon. A principal component analysis of the morphological data among 7 matrilines shows that all variables have positive loadings of high magnitude on the 1st component. Canonical discriminant analysis for Neodon (including M. clarkei and 2 unidentified species) correctly classifies 93.0% of specimens. Overall, our analyses support the recognition of Alexandromys, Lasiopodomys, Microtus, Neodon, Proedromys, and Volemys as genera. Stenocranius includes Microtus gregalis, and the genealogical position of Stenocranius remains uncertain. The status of Arvicola requires further study. We assign M. clarkei to Neodon and describe 2 new species of Neodon.

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