Deyan Ge

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.

Anti-predator defence drives parallel morphological evolution in flea beetles

Complex morphological or functional traits are frequently considered evolutionarily unique and hence useful for taxonomic classification. Flea beetles (Alticinae) are characterized by an extraordinary jumping apparatus in the usually greatly expanded femur of their hind legs that separates them from the related Galerucinae. Here, we examine the evolution of this trait using phylogenetic analysis and a time-calibrated tree from mitochondrial (rrnL and cox1) and nuclear (small subunits and large subunits) genes, as well as morphometrics of femora using elliptic Fourier analysis. The phylogeny strongly supports multiple independent origins of the metafemoral spring and therefore rejects the monophyly of Alticinae, as defined by this trait. Geometric outline analysis of femora shows the great plasticity of this structure and its correlation with the type and diversity of the metafemoral springs. The recognition of convergence in jumping apparatus now resolves the long-standing difficulties of Galerucinae–Alticinae classification, and cautions against the value of trait complexity as a measure of taxonomic significance. The lineage also shows accelerated species diversification rates relative to other leaf beetles, which may be promoted by the same ecological factors that also favour the repeated evolution of jumping as an anti-predation mechanism.

Tracing the Origin and Diversification of Dipodoidea (Order: Rodentia): Evidence from Fossil Record and Molecular Phylogeny

Dipodoidea are a diverse rodent group whose earliest known record is from the Middle Eocene. The evolution and diversification of this superfamily have been documented by fossils and comparative morphology, but have not yet been studied from the perspective of molecular phylogeny. This study is the first attempt to reconstruct an extensive phylogeny of Dipodidae and estimate divergence times based on a nuclear gene coding for interphotoreceptor retinoid-binding protein. We found that there is a wide measure of agreement with the fossil record. Each of the three ecological groups of the extant Dipodoidea (sicistines, zapodines, and jerboas) has its distinctive distribution; the distribution patterns have been shaped by the dispersal events. The key events of paleogeographic distribution coincided with major paleoenvironmental events in the Cenozoic. The first important diversification phase occurred during the period from the Oligocene to Early Miocene, when global climate underwent major changes beginning with the Eocene/Oligocene boundary. The second adaptive radiation occurred within jerboas and was associated with the expansion of open habitat starting with the late Middle Miocene. The diversification of jerboas can be correlated with habitat changes in response to global and regional climatic events.

Suprageneric systematics of flea beetles (Chrysomelidae: Alticinae) inferred from multilocus sequence data

Recent phylogenetic studies of flea beetles (Alticinae) based on morphological or molecular data have focused on the relationship and possible paraphyly with respect to the closely related Galerucinae, while the supra-generic classification mainly dates back to the 19th century. Here, phylogenetic analysis was performed on DNA sequences for two mitochondrial (rrnL and cox1) and two nuclear (SSU and LSU rRNA) genes from 158 genera and 165 species that cover most suprageneric groups of flea beetles proposed in the older literature. Various alignment strategies and tree search methods were used to test the stability of major clades. Besides confirmation of the placement of several alticine lineages within Galerucinae, a preliminary framework for classification of the main alticine clades was obtained. It is proposed to recognize 18 groups of genera based on well-supported nodes. These include the Altica, Amphimela, Aphthona, Blepharida, Chabria, Chaetocnema, Dibolia, Disonycha, Griva, Lactica, Longitarsus, Manobia, Monoplatus, Nisotra, Oedionychis, Pentamesa, Phygasia and Pseudodera groups. These groups provide a novel perspective to the existing classification. The analysis of 14 morphological characters used in the traditional classification of Alticinae and Galerucinae revealed high levels of homoplasy with respect to the DNA-based tree, but significant hierarchical structure in most of them. Even if not unique to any particular group of genera, these traits largely corroborate the groupings established with DNA sequences.

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.

The Evolution and Paleobiogeography of Flying Squirrels (Sciuridae, Pteromyini) in Response to Global Environmental Change

Flying squirrels are strictly arboreal squirrels adopting a special gliding form of locomotion. This group of animals has a long history that has mirrored the vicissitude of forests. The discrepancy in the distribution between fossils and extant species indicates a mysterious evolution history requiring further exploration. This study compiles the worldwide fossils of Pteromyini to the species level in order to reproduce the spatiotemporal distribution pattern of flying squirrels and deduce the ancestral distribution according to dispersal-vicariance analysis of a phylogeny of the extant species. In addition, we reconstruct the paleoenvironmental background and find that flying squirrels probably originated in the Oligocene–Miocene transition from Europe and immediately dispersed to Asia and North America. Influenced by glaciation, CO2 reduction, geologic movements and the Paratethys retreat, the Northern Hemisphere underwent climate deterioration and grassland expansion during the late Miocene, and thus the diversity of Pteromyini dramatically decreased. The uplift of the Tibet Plateau in addition to the strengthened Asian monsoons intensified the aridity in central Asia, but brought sufficient water to the densely forested regions of South and Southeast Asia. These forests are likely both refugia and diversification center for flying squirrels during glacial periods in the Quarternary. The subsequent connection and separation events among these heterogeneous habitats has probably been a driving force in the speciation of flying squirrels. Based on this work, we predict a bleak future for the flying squirrels, one which is closely associated with the fate of forests in Asia.

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.

Climatic niche conservatism and ecological opportunity in the explosive radiation of arvicoline rodents (Arvicolinae, Cricetidae)

Climatic niche conservatism shapes patterns of diversity in many taxonomic groups, while ecological opportunity (EO) can trigger rapid speciation that is less constrained by the amount of time a lineage has occupied a given habitat. These two processes are well studied, but limited research has considered their joint and relative roles in shaping diversity patterns. We characterized climatic and biogeographic variables for 102 species of arvicoline rodents (Arvicolinae, Cricetidae), testing the effects of climatic niche conservatism and EO on arvicoline diversification as lineages transitioned between biogeographic regions. We found that the amount of time a lineage has occupied a precipitation niche is positively correlated with diversity along a precipitation gradient, suggesting climatic niche conservatism. In contrast, shift in diversification rate explained diversity patterns along a temperature gradient. Our results suggest that an indirect relationship exists between temperature and diversification that is associated with EO as arvicoline rodents colonized warm Palearctic environments. Climatic niche conservatism alone did not fully explain diversity patterns under density‐dependence, highlighting the additional importance of EO‐related processes in promoting the explosive radiation in arvicoline rodents and shaping diversity pattern among biogeographic regions and along climatic gradients.

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.