Zhixin Wen

Evolutionary History of Lagomorphs in Response to Global Environmental Change

Although species within Lagomorpha are derived from a common ancestor, the distribution range and body size of its two extant groups, ochotonids and leporids, are quite differentiated. It is unclear what has driven their disparate evolutionary history. In this study, we compile and update all fossil records of Lagomorpha for the first time, to trace the evolutionary processes and infer their evolutionary history using mitochondrial genes, body length and distribution of extant species. We also compare the forage selection of extant species, which offers an insight into their future prospects. The earliest lagomorphs originated in Asia and later diversified in different continents. Within ochotonids, more than 20 genera occupied the period from the early Miocene to middle Miocene, whereas most of them became extinct during the transition from the Miocene to Pliocene. The peak diversity of the leporids occurred during the Miocene to Pliocene transition, while their diversity dramatically decreased in the late Quaternary. Mantel tests identified a positive correlation between body length and phylogenetic distance of lagomorphs. The body length of extant ochotonids shows a normal distribution, while the body length of extant leporids displays a non-normal pattern. We also find that the forage selection of extant pikas features a strong preference for C3 plants, while for the diet of leporids, more than 16% of plant species are identified as C4 (31% species are from Poaceae). The ability of several leporid species to consume C4 plants is likely to result in their size increase and range expansion, most notably in Lepus. Expansion of C4 plants in the late Miocene, the so-called ‘nature’s green revolution’, induced by global environmental change, is suggested to be one of the major ‘ecological opportunities’, which probably drove large-scale extinction and range contraction of ochotonids, but inversely promoted diversification and range expansion of leporids.

Molecular phylogeny and the underestimated species diversity of the endemic white-bellied rat (Rodentia: Muridae: Niviventer) in Southeast Asia and China

The white‐bellied rat, Niviventer, is a genus endemic to Southeast Asia and China. However, the interspecific phylogenetic relationships and species diversity of this genus remain poorly understood. In the present study, single and multi‐locus analyses were performed. Phylogenetic reconstruction on Cytochrome b (512 individuals, including data from Genbank) revealed five major clades with approximately 35 operational taxonomic units (OTUs), a number twice the existing taxonomy. The first clade (N. langbianis species group) was the earliest diverged. The second clade (N. fulvescens species group) diverged in Southeast Asia, the south and lower altitude regions of the Hengduan Mountains, and Southeast China. The third clade (the N. eha species group) is endemic to high altitudes in Northwest Yunnan and the central region of Himalaya. The fourth clade (the N. andersoni species group), is mainly confined to alpine regions of the Hengduan Mountains. The fifth clade (N. confucianus species group) is mainly distributed in the north and higher altitude regions of eastern Himalaya, the Hengduan Mountains and Taiwan, with the complex also invading central and northern China. Results from the combined dataset of four genes (Cytochrome b, Cytochrome oxidase subunit I, the D‐loop sequence of the mitochondrial genome and the first exon of the nuclear interphotoreceptor retinoid binding protein) for 82 representative individuals from China generally coincide with the result of the single gene, with 12 OTUs identified. These results provide a preliminary framework for the existing classification of this highly diversified genus. The divergence time of Niviventer based on the four gene topology was dated to the late Miocene ~6.41 Ma. Significant differences were detected in the general body form changes among these units based on voucher specimens. Moreover, geometric morphometric analysis of the cranium shape of voucher specimens indicated significant differences among five major species groups. Shape divergence of the cranium among several OTUs within the N. confucinaus complex is also significant. Our results provide further evidence for rapid and highly underestimated diversification of Niviventer both in genetics and morphology.

Continental Refugium in the Mongolian Plateau during Quaternary Glacial Oscillations: Phylogeography and Niche Modelling of the Endemic Desert Hamster, Phodopus roborovskii.

The Mongolian Plateau (MP), which is situated in the interior of Asia and possesses a typical continental climate, experienced harsh climatic conditions during the Quaternary glacial fluctuations. Although these events likely had huge impacts on the local animal populations, the current effects have hardly been explored. To investigate whether the MP supported a refugium along an oceanic-continental gradient (ROCG), and whether this refugium was glacial or interglacial, we investigated the demographic and phylogeographic history of an endemic mammal species, the desert hamster Phodopus roborovskii. We reconstructed the demographic variation, the phylogeographic diffusion, and modelled the potential habitat during historical periods. The genetic diversity in the MP was the highest among all the localities, and the MP was a suitable habitat throughout the modelled historical periods. A phylogeographic diffusion analysis emphasized the importance of the MP as the centre of origin, preservation and spread for P. roborovskii. The homogeneous landscape provided the opportunity for a wide gene flow, which resulted in low resolution of the phylogenetic relationships. Moreover, P. roborovskii was favoured by the interglacial condition, with both its demographical and geographical ranges expanded within the interglacial periods. The range variation from the Last Glacial Maximum to the current condition reflects a distinct longitudinal shift, while both ranges largely contracted from that of the Last Interglacial. Our results support that the MP served as a refugium and spread centre for P. roborovskii during the Quaternary climate fluctuations. The interglacial expansion and the longitudinal shifts highlighted the important effects of precipitations on the distribution range of species adapted to arid and semi-arid during glacial oscillations.

Dispersal, niche, and isolation processes jointly explain species turnover patterns of nonvolant small mammals in a large mountainous region of China

Abstract Understanding the mechanisms that govern the spatial patterns of species turnover (beta diversity) has been one of the fundamental issues in biogeography. Species turnover is generally recognized as strong in mountainous regions, but the way in which different processes (dispersal, niche, and isolation) have shaped the spatial turnover patterns in mountainous regions remains largely unexplored. Here, we explore the directional and elevational patterns of species turnover for nonvolant small mammals in the Hengduan Mountains of southwest China and distinguish the relative roles of geographic distance, environmental distance, and geographic isolation on the patterns. The spatial turnover was assessed using the halving distance (km), which was the geographic distance that halved the similarity (Jaccard similarity) from its initial value. The halving distance was calculated for the linear, logarithmic, and exponential regression models between Jaccard similarity and geographic distance. We found that the east–west turnover is generally faster than the south–north turnover for high‐latitudinal regions in the Hengduan Mountains and that this pattern corresponds to the geographic structure of the major mountain ranges and rivers that mainly extend in a south–north direction. There is an increasing trend of turnover toward the higher‐elevation zones. Most of the variation in the Jaccard similarity could be explained by the pure effect of geographic distance and the joint effects of geographic distance, environmental distance, and average elevation difference. Our study indicates that dispersal, niche, and isolation processes are all important determinants of the spatial turnover patterns of nonvolant small mammals in the Hengduan Mountains. The spatial configuration of the landscape and geographic isolation can strongly influence the rate of species turnover in mountainous regions at multiple spatial scales.

An endemic rat species complex is evidence of moderate environmental changes in the terrestrial biodiversity centre of China through the late Quaternary

The underlying mechanisms that allow the Hengduan Mountains (HDM), the terrestrial biodiversity centre of China, to harbour high levels of species diversity remain poorly understood. Here, we sought to explore the biogeographic history of the endemic rat, Niviventer andersoni species complex (NASC), and to understand the long-term persistence of high species diversity in this region. In contrast to previous studies that have proposed regional refuges in eastern or southern of the HDM and emphasized the influence of climatic oscillations on local vertebrates, we found that HDM as a whole acted as refuge for the NASC and that the historical range shifts of NASC mainly occurred in the marginal regions. Demographic analyses revealed slight recent population decline in Yunnan and south-eastern Tibet, whereas of the populations in Sichuan and of the entire NASC were stable. This pattern differs greatly from classic paradigms of temperate or alpine and holarctic species. Interestingly, the mean elevation, area and climate of potential habitats of clade a (N. excelsior), an alpine inhabitant, showed larger variations than did those of clade b (N. andersoni), a middle-high altitude inhabitant. These species represent the evolutionary history of montane small mammals in regions that were less affected by the Quaternary climatic changes.

Heterogeneous distributional responses to climate warming: evidence from rodents along a subtropical elevational gradient

BackgroundUnderstanding whether species’ elevational range is shifting in response to directional changes in climate and whether there is a predictable pattern in that response is one of the major challenges in ecology. However, so far very little is known about the distributional responses of subtropical species to climate change, especially for small mammals. In this study, we examined the elevational range shifts at three range points (upper and lower range limits and abundance-weighted range centre) of rodents over a 30-year period (1986 to 2014–2015), in a subtropical forest of Southwest China. We also examined the influences of four ecological traits (body mass, habitat breadth, diet and daily activity pattern) on the upslope shifts in species’ abundance-weighted range centres.ResultsDespite the warming trend between 1986 and 2015, the 11 rodent species in analysis displayed heterogeneous dynamics at each of the three range points. Species which have larger body sizes and narrower habitat breadths, show both diurnal and nocturnal activities and more specialized dietary requirements, are more likely to exhibit upslope shifts in abundance-weighted range centres.ConclusionsSpecies’ distributional responses can be heterogeneous even though there are directional changes in climate. Our study indicates that climate-induced alleviation of competition and lag in response may potentially drive species’ range shift, which may not conform to the expectation from climate change. Difference in traits can lead to different range dynamics. Our study also illustrates the merit of multi-faceted assessment in studying elevational range shifts.

The roles of environment, space, and phylogeny in determining functional dispersion of rodents (Rodentia) in the Hengduan Mountains, China

Abstract The recently described trait‐based approach is becoming widely popular for a mechanistic understanding of species coexistence. However, the greatest challenge in functional analyses is decomposing the contributions of different ecological and evolutionary processes (e.g., niche‐based process, neutral process, and evolutionary process) in determining trait structure. Taking rodents (Rodentia) in the Hengduan Mountains as our study model, we aim to (1) quantify the vertical patterns of functional structure for head–body length (HL), tail/body ratio (TR), animal component in diet (ACD), and all traits; (2) disentangle the relative importance of different assembly processes (environment, space, and phylogeny) in structuring trait dispersion; and (3) assess the feasibility of Bergmanns rule and Allens rule along elevational gradient. Our results have suggested that the vertical functional structure pattern varied across these three traits, indicating distinct functional roles in the community assembly process. These nonrandom vertical patterns of HL, TR, and terminal ACD have demonstrated these traits were dominated by different ecological process along environmental gradient. In variance partitioning, high proportion of the spatial variations in trait dispersion was explained by environmental and spatial models, which have provided supporting strong evidence for niche‐based and neutral processes in leading species coexistence. Although the three traits all exhibited apparent phylogenetic signals, phylogenetic relationship within community failed to predict the spatial variations of functional dispersion, confirming the enormous inference of phylogenetic signals in predicting trait structure. By assessing the vertical patterns of HL and TR at order and family levels, we argued that functional adaptation along an environmental gradient is a surrogate of series of complex processes (e.g., environmental filtering, interspecific interaction, and neutral dispersal) acting on multiple functional axes, which results in inconsistence with the empirical rules along elevational gradient.

Phylogeny and taxonomic reassessment of jerboa, Dipus (Rodentia, Dipodinae), in inland Asia

Deserts and arid regions are perceived to have low biological and genetic diversity, which has partially influenced the identification of psammophilic species, especially taxonomic inferences based on morphology alone. Recent studies of Dipus sagitta have revealed clear, deep genetic divergence beyond the species level within this monotypic genus. To clarify the taxonomy of Dipus, we examined a morphometric dataset consisting of 191 voucher specimens covering nearly the entire distribution of the genus to explore skull variation using traditional morphological measurements and geometric morphometric analysis. Phylogenetic relationships within Dipus using two mitochondrial genes (n = 383) and six nuclear genes (n = 106) were assessed by Bayesian inference and maximum‐likelihood procedures. We used a “candidate species approach” with the divergent mtDNA phylogenetic groups and subspecies identified in previous studies as the starting point and analysed the candidates using five species delimitation methods and two validation methods. Our findings indicate that Dipus can be divided into four phylogenetic groups that include two species: the Deasyi group (D. deasyi), Sagitta group, Sowerbyi group and Turanicus group (D. sagitta). According to the morphological analyses and the examined specimens, pelage colour varies significantly with season and age, making it unsuitable as a diagnostic characteristic of the subspecies. Furthermore, measurements of body size and skull size require a large number of specimens to reach statistical significance and obtain reliable results. Geographical distributions should be considered first when identifying species or subspecies due to the disjunct habitats of Dipus. Our molecular analyses revealed the long‐neglected potential diversity in arid regions and improved the efficiency of species/subspecies identification. We also found that individuals from more humid areas or higher altitudes were larger, whereas individuals from drier areas possessed longer appendages and larger tympanic bulla.

Abundance–occupancy and abundance–body mass relationships of small mammals in a mountainous landscape

ContextMountainous landscapes are characterized by strong spatial heterogeneity, leading to increasing geographical isolation and decreasing area with elevation. Consequently, the colonization rate decreases from the low to high elevation zone, while the extinction rate shows the opposite.ObjectivesDue to such changes, we test whether (1) species occur at a declining number of sites (mountains) and have a less positive abundance–occupancy relationship (AOR) in a higher elevation zone; (2) a lower proportion of rare large-bodied species (less resistant to extinction) and a more positive abundance–body mass relationship (ABR) emerge in a higher elevation zone.MethodsUsing the data of small mammals from 20 elevational gradients in the Mountainous Region of Southwest China, we compared the AORs and ABRs among the low, middle and high elevation zones. The AOR and ABR were fitted with linear and polynomial regression models. We compared endemic ratios among the different elevation zones.ResultsThe AOR was best characterized by a linear model and positive in all elevation zones. Its slope decreased from the low to high elevation zone. The quadratic model performed the best in fitting the ABR in each zone. When fitted with linear models, both the R2 and slope of the ABR increased towards the high elevation zone. The endemic ratios were significantly higher in the middle and high elevation zones.ConclusionsBoth the AOR and ABR in mountainous landscapes are strongly elevation-dependent. The increasing geographical isolation and decreasing area with elevation can have a high impact on macroecological patterns and processes.

Evolutionary Genetics of Hypoxia and Cold Tolerance in Mammals

Low oxygen and fluctuant ambient temperature pose serious challenges to mammalian survival. Physiological adaptations in mammals to hypoxia and low temperatures have been intensively investigated, yet their underlying molecular mechanisms need further exploration. Independent invasions of high-altitude plateaus, subterranean burrows and marine environments by different mammals provide opportunities to conduct such analyses. Here, we focused on six genes in the hypoxia inducible factor (HIF) pathway and two non-shivering thermogenesis (NST)-related genes [PPAR co-activator 1 (PGC-1) and uncoupling protein 1 (UCP1)] in representative species of pikas and other mammals to understand whether these loci were targeted by natural selection during independent invasions to conditions characterized by hypoxia and temperature fluctuations by high-altitude, subterranean and marine mammals. Our analyses revealed pervasive positive selection signals in the HIF pathway genes of mammals occupying high-altitude, subterranean and aquatic ecosystems; however, the mechanisms underlying their independent adaptations to hypoxic environments varied by taxa, since different genes were positively selected in each taxon and expression levels of individual genes varied among species. Additionally, parallel amino acid substitutions were also detected in hypoxia-tolerant mammals, indicating that convergent evolution may play a role in their independent adaptations to hypoxic environments. However, divergent evolutionary histories of NST-related genes were noted, since significant evidence of positive selection was observed in PGC-1 and UCP1 in high-altitude species and subterranean rodents; however, UCP1 may have already lost its function in diving cetaceans, which may be related to the thick blubber layer of adipose and connective tissue in these mammals.