1 Major research interests
Species are the units of biodiversity. Our research is focused on investigating the biodiversity of spiders and amphipods. Based on broad collections, we will publish the species new to science and revise the known species. Further, we explore the origin of the diversity, specially the spatio-temporal patterns of diversification, based on genetic data and phylogenomics. The key region studied in our laboratory is the Tethys, which vanished during uplifting of the Qinghai-Tibet Plateau (see figure 1).
Figure 1. The vanished Tethys and the uprising of the Qinghai-Tibet Plateau.
2 Background
Tethys is named after the sea goddess of Greek myth who was the daughter of Gaia and mother of great rivers. The Tethys began to form some 260 million years ago (Ma) and vanished 5.5 Ma. Tethyan changes have great impacted the fauna and flora in adjacent areas. However, recent advances in molecular systematics facilitate further possibilities and details.
3 Major Research Achievements
3.1 Field investigation on the spiders and amphipods in Eurasian continent
Field investigation forms the basis of our current studies. The fieldwork yielded many specimens from Europe and Asia. The specimens are deposited in a refrigerator which allows their use in molecular studies for many years. These specimens will also assist the next generation of researchers because resources are being destroyed rapidly.
3.2 Major findings
(1) Eocene habitat shift from saline to freshwater promoted Tethyan amphipod diversification: Current theory predicts that a shift to a new habitat would increase the rate of diversification, while as lineages evolve into multiple species, intensified competition would decrease the rate of diversification. We used Holarctic amphipods of the genus Gammarus to test this hypothesis. We sequenced four genes (5,088 bp) for 289 samples representing 115 species of Gammarus. A phylogenetic analysis showed that Gammarus originated in the Paleocene from the Tethyan region and, thus, it has a saline ancestry. In the Middle Eocene it colonized freshwater habitats. Ancestral range reconstruction and diversification mode analyses combined with paleogeological and paleoclimatic evidence suggested that the habitat shift from saline to freshwater led to an increased diversification rate. The saline lineage of Gammarus dispersed to both sides of the Atlantic at 55 Ma because of the few barriers between the Tethys and the Atlantic. It diversified throughout its evolutionary history with a constant diversification rate of 0.04 species per million years (sp/My). The freshwater Gammarus, however, underwent a rapid diversification phase (0.11 sp/My) until the Middle Miocene and lineages successively diversified across Eurasia via vicariance likely driven by changes of the Tethys and landmasses. In particular, freshwater Gammarus lacustris and G. balcanicus had a relatively high diversification shift, corresponding to the regression of the Paratethys Sea and the continentalization of Eurasian lands during the Miocene. Subsequently (14 Ma), the diversification rate of the freshwater Gammarus decreased to 0.05 and again to 0.01 sp/My. The genus Gammarus provides an excellent aquatic case supporting the hypothesis that ecological opportunities promote diversification.
(2) Phylogenetic analyses of Gammaridae crustaceans reveal different diversification patterns among sister lineages in the Tethyan region: The Gammaridae shows the greatest disparity in species diversity and distribution pattern in the Amphipoda, with some genera ranging from the Palearctic to Nearctic, while others are limited to the Mediterranean region or ancient Tethyan margins. We presented the first molecular phylogenetic analysis of the Gammaridae to investigate its evolutionary history using four genetic markers and a comprehensive set of taxa representing 198 species. The results revealed that the Gammaridae originated from the Tethyan region in the Cretaceous, and split into three morphologically and geographically distinct lineages by the end of the Paleocene. Diversification analysis combined with paleogeological evidence suggested that the Tethyan changes induced by sea-level fluctuation and tectonic uplift triggered different diversification modes and range expansions for the three lineages. Gammarus underwent an early rapid radiation across Eurasia and North America, then declined towards modern species. Pontogammarids maintained stable diversification with restricted distributions around the Tethyan basin, whereas sarothrogammarids experienced evolutionary stasis by stranding on the ancient Tethyan margins. Our findings suggested that environmental changes have played important roles in the diversification of Gammaridae.
(3) Marine incursion into East Asia- a forgotten driving force of biodiversity: Episodic marine incursion has been a major driving force in the formation of present-day diversity. Marine incursions are considered to be one of the most productive ‘species pumps’ particularly because of its division and coalescence effects. Marine incursion events and their impacts on diversity are well documented from South America, North America and Africa. In contrast, little is known regarding their history and impacts in continental East Asia. We proposed a marine incursion scenario occurring in East Asia during the Miocene epoch, 10–17 Ma. Our molecular phylogenetic analysis of Platorchestia talitrids revealed that continental terrestrial populations (P. japonica) form a monophyletic group that is the sister group to the Northwest Pacific coastal species P. pacifica. The divergence between the two species coincides with Middle Miocene high global sea levels. We suggested that the inland form arose as a consequence of a marine incursion event. This is the first solid case documenting the impact of marine incursion on extant biodiversity in continental East Asia. We believe that such incursion event has had major impacts on other organisms and has played an important role in the formation of biodiversity patterns in the region.
(4) A spider species complex revealed high cryptic diversity in South China caves: Cryptic species, which are an important component of biodiversity, have rarely been studied in South China karst. We investigated cryptic diversity in the cave species complex Telema cucurbitina, which has a narrow niche but widespread distribution among multiple caves. We sampled 15 populations (caves) in addition to the type locality. Phylogenetic results indicated that individuals from the same cave constituted well-supported clades. Species diversity within this species complex was assessed in a coalescent framework, first with a Bayesian extension of the general mixed Yule coalescent (bGMYC) model and a Bayesian species delimitation method (BPP). Both species delimitation methods identified each cave population as a separate species. We proposed that each cave population within this species complex was a separate evolving lineage and therefore 16 OTUs were recovered based on our molecular data despite their high levels of morphological similarity. We also proposed that the unrecognized organism’s diversity within South China caves might be extremely large considering our case. Further, our work revealed that species discovery of cave organisms by morphological data has a high probability of underestimating hidden diversity. Our work also highlights the need for conservation strategies to protect this largely neglected diversity of cave organisms.
(5) Ancient lineage, young troglobites—recent colonization of caves by Nesticella spiders: The evolution and origin of cave organisms is a recurring theme in evolutionary biology, but analyses are often hindered by the inaccessibility of caves, convergent morphological adaptation, and complex colonization processes. We investigated the evolutionary history of Nesticella cave spiders, which mainly occur in the Yunnan–Guizhou Plateau, China. Our comprehensive sampling and phylogenetic and coalescent-based analyses, allow investigations into the tempo and mode of diversification and the origins of these troglobites. We also determine which factors have driven the diversification of this little-known group. Coalescent-based species delimitations validated the 18 species recognized by morphological inspection and also suggested the existence of cryptic lineages. Estimated divergence times suggested that our troglobtic Nesticella constitute a monophyletic clade that originated in the middle Miocene (11.1–18.6 Ma). Although the Yunnan–Guizhou Plateau clade was composed exclusively of troglobites, suggesting an ancient common subterranean ancestor, we favor the scenario of multiple, independent, Pleistocene cave colonizations over a single ancient cave colonization event. The diversification of Nesticella has been greatly influenced by the sequential uplift of the plateau. It is likely that multiple cave colonizations by epigean ancestors occurred over time during periods of glaciation. Although plateau troglobitic Nesticella are ancient, young lineages invaded caves only recently. The absence of extant epigean relatives and nearly complete isolation among caves supports they are relict taxa. Our work highlights the importance of comprehensive sampling for studies of subterranean diversity and the evolution of cave organisms. The existence of potentially cryptic species and the relict status of Nesticella highlight the need to conserve these cave spiders.
3.3 Contribution of our work in our field of research
Morphological taxonomy: In all, 2361 spider species belonging to 450 genera and 56 families were known from China in 1999 (Song et al 1999). Now, 4385 species of spiders belonging to 650 genera and 68 families are known. Most of this increase in diversity (>80%) was published by my laboratory. In the last few years alone, we described 410 species new species. This effort accounts for almost 0.3% of all the known Chinese biota.
Molecular systematics: The uprising of Qinghai-Tibet Plateau is a main geological event in the history of China. The orogenesis greatly effects in the current fauna of Asia and Europe. However, early studies mainly focused on the Qinghai-Tibet Plateau itself. Our molecualr systematics studies are more comprehensive in following the evolutionary footprint of spiders and amphipods from Africa and Europe to Asia. This helps clarify the origin of the Chinese fauna.
4 Current Research and Future Directions
Our studies focus on the systematics of spiders and amphipods. Morphological species descriptions are a direct means of documenting biodiversity. Molecular systematics trace the trail of speciation on a large scale. Using phylogenomics, we are establishing the evolutionary relationships of haplogyne spiders, which includes ca. 30 families, most of which live in caves. We are planning to use phylogenomics to predict gene functions and identify those involved in adaptions to troglodytic lifestyles.
