Journal of Biogeography (J. Biogeogr.) (2016) 43, 691–702 ORIGINAL The influence of geological movements ARTICLE on the population differentiation of Biston panterinaria (Lepidoptera: Geometridae) Rui Cheng1,2, Nan Jiang1, Xiushuai Yang1, Dayong Xue1, Shuxian Liu1,2 and Hongxiang Han1* 1Key Laboratory of Zoological Systematics and ABSTRACT Evolution, Institute of Zoology, Chinese Aim East Asia is known for its exceptionally high levels of biodiversity, which Academy of Sciences, Beijing 100101, China, 2 is connected to its high level of species differentiation. Geological movements University of Chinese Academy of Sciences, Shijingshan District, Beijing 100049, China are the most important factor promoting the species differentiation in East Asia. In this paper, we choose Biston panterinaria, a moth species widely dis- tributed in East Asia, to study the relative contributions of geographical isola- tion and glaciation cycles to its current genetic constitution. Location East Asia. Methods Phylogenetic analyses were based on three data sets. beast was used to estimate the divergence time and reconstruct the maximum clade credibility tree. Mismatch distribution and Bayesian skyline plots (BSP) were used to infer historical population fluctuations. maxent was used to predict the potential species distributions during two periods: the present day and the Last Glacial Maximum (LGM). Results The phylogenetic tree and the median joining network strongly sup- ported four reciprocally monophyletic lineages: northern, Yunnan-Tibet, south- ern and Yunnan-SE. The estimates of divergence time suggested that three differentiation processes occurred at approximately 1.17, 0.76 and 0.67 Ma. Within the northern and southern lineages, lineage divergence occurred at approximately 0.17 and 0.16 Ma. Mismatch distribution and BSP suggested that the northern and southern lineages experienced one expansion after the LGM, and this result was consistent with the result of the ecological niche model. Main conclusions Our results suggested that B. panterinaria experienced three fragmentations of wide-ranging ancestral populations, and that mountain bar- rier isolation induced by geological movements is the main driver of lineage dif- ferentiation. Climatic oscillations during the Pleistocene affected the population differentiation within both the northern and southern lineages. The distribution of the four lineages of B. panterinaria is generally consistent with the zoogeo- graphical regionalization of China. This study provides direct evidence for the importance of mountain barriers in promoting population differentiation. *Correspondence: Hongxiang Han, Institute of Keywords Zoology, Chinese Academy of Sciences, No. 1 East Asia, ecological stability, Gaoligong Mountains, Himalaya-Hengduan Beichen West Road, Chaoyang District, Beijing Mountains, Kunlun-Yellow River Movement, mountain barrier, penultimate 100101, China. E-mail: [email protected] glaciation and simplest types of speciation in animals (Mayr, 1942, INTRODUCTION 1970; Futuyma & Mayer, 1980). Geographical isolation sepa- It has been widely accepted that allopatric speciation (specia- rates populations, prevents gene flow, and produces genetic tion by geographical isolation) is one of the most important differentiation, which results in the evolution of new species. ª 2015 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/jbi 691 doi:10.1111/jbi.12676 R. Cheng et al. Examples of allopatric speciation can be found in almost all glaciations in East Asia (Shi et al., 2006; Zhou et al., 2006). animal groups, such as mammals (Ci et al., 2009), birds (Qu The development of both modern and Quaternary glacia- et al., 2014), frogs (Che et al., 2010) and butterflies (Habel tions was reliant on mountains, and the coupling of the et al., 2008). Geographical barriers may comprise many types mountain uplift and a global cooling was the ultimate cause of geological features, including mountains, rivers, straits and of glacier development around the QTP and its surrounding deserts. Mountain barriers may play a particularly important mountains (Shi et al., 2006; Zhou et al., 2006). Glacial role in shaping animal communities in East Asia by promot- oscillations are also an important factor affecting species ing speciation and maintaining high levels of endemism differentiation and the present distribution of several plants (Zhao et al., 2007; Ci et al., 2009; Huang et al., 2010; Lei and animals (Hewitt, 1996, 2004), particularly in central et al., 2015). and eastern China, where isolation due to geographical bar- The Himalaya-Hengduan Mountains (HHM) are the riers is not a factor. most important mountain system in China and are consid- The drivers of diversification for species living at different ered the ‘evolutionary powerhouse’ of Chinese avifauna (Li, altitudes are often different. Species living at high altitudes 1988; Zhao et al., 2007; Lei et al., 2015). Several previous appear to have experienced colonization via dispersal fol- studies have confirmed that geographical isolation with lowed by isolation and divergence. In contrast, species living mountain barriers was responsible for the lineage diversifi- at low altitudes appear to have experienced fragmentation of cation of multiple intra-specific genetic lineages of several wide-ranging ancestral populations (Lu et al., 2012). There bird species in the Hengduan Mountains (Lei et al., 2007; are many studies examining how species living at different Song et al., 2009; Qu et al., 2014). The complex topogra- altitudes cope with geological movements and climatic fluc- phy and glacial oscillations may have contributed to shap- tuations (Kullman, 1987; Lu et al., 2012; Qu et al., 2014). ing the high genetic diversity and endemism of the HHM The primary aim of this study is to explore how geographical (Rahbek & Graves, 2000; Fjeldsa et al., 2012). Previous events are responsible for population differentiation of spe- studies have shown that Pleistocene glaciations were cies living at low altitudes. For this study, we selected Biston restricted to high altitudes (> 2000 m) around the HHM, panterinaria (Bremer & Grey, 1853), a moth species with a unlike the situation in nearby central China, which was wide distribution at low altitudes, typically below 1500 m, extensively covered in ice (Li et al., 1991; Liu et al., 2002). through East and South Asia (including the HHM, central Apart from glaciation factors, the HHM constitute an ideal and eastern China), similar to the distribution of its host natural area for studying speciation and population differ- broad leaved trees (Liu, 1981; Li et al., 2008a). Biston pan- entiation by geographical isolation, particularly for species terinaria has many intraspecific morphological variations, living at low altitudes (Craw et al., 2008). Among the vari- involving for instance wing markings and male genitalia ous constituents of the HHM, the Gaoligong Mountains (Sato, 1996; Jiang et al., 2011). (GLGM), which constitute the extreme western section of the Hengduan Mountains, may play a particularly impor- MATERIALS AND METHODS tant role in driving species differentiation in the HHM. However, research testing this hypothesis is lacking, with Sampling and sequence data the exception of some studies on the species richness of different altitudes and slopes of the GLGM (Xu et al., A total of 271 specimens of B. panterinaria were collected 2001a,b; Li et al., 2008b). from 56 sampling sites throughout much of the distribution The HHM, an important part of the Qinghai-Tibet Pla- range of this species. We pooled the 56 sampling sites into teau (QTP), were formed by a series of geological move- 28 geographical locations (the abbreviations of sampling ments, which resulted in the strong uplift of the whole sites, see Appendix S1 in Supporting Information and QTP over the past 3.6 Myr (Li & Fang, 1998; Li, 1999). Fig. 1). Samples for DNA extraction were preserved in 100% The QTP region had an altitude of approximately 1000 m ethanol and stored at À20 °C. DNA was extracted using the before the Pliocene (Li et al., 1979) and experienced a DNeasy Tissue kit (Qiagen, Beijing, China) and vouchers strong uplift caused by the Himalayan Orogeny during the were deposited at the Museum of IZCAS (the Institute of Pliocene. During the strong uplift of the QTP, three main Zoology, Chinese Academy of Sciences, Beijing, China). geological movements took place: the Qinghai-Tibet Move- Three mitochondrial and three nuclear genes were obtained, ment (3.6–1.4 Ma), the Kunlun-Yellow River Movement including COI, CYTB, 16S, EF-1a, wg and ITS2 genes, (1.2–0.6 Ma) and the Gonghe Movement (0.15–0 Ma) (Li, through Polymerase Chain Reaction (PCR) amplification. 1999; Zhao et al., 2011). Each movement played an impor- The three mtDNA loci were amplified as described in Yang tant role in shaping the terrain of the plateau and promot- et al. (2013). The three nuDNA loci, were amplified as ing species differentiation, for instance, the Qinghai-Tibet described in Yamamoto & Sota (2007), Brower & DeSalle Movement, is thought to have led to the emergence of (1998) and Ji et al. (2003). Sequences of all primers used in Homo habilis and the speciation of three ancient elephants this study are listed in Table 1. Sequences were deposited in (Vrba, 1985; Wang et al., 2013). Geological movements in GenBank; the accession numbers are provided in the QTP were also essential for shaping the Quaternary Appendix S1. 692 Journal of Biogeography 43, 691–702 ª 2015 John Wiley