Evolutionary History of Apocheima Cinerarius (Lepidoptera: Geometridae), a Female flightless Moth in Northern China
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Zoologica Scripta Evolutionary history of Apocheima cinerarius (Lepidoptera: Geometridae), a female flightless moth in northern China SHUXIAN LIU,NAN JIANG,DAYONG XUE,RUI CHENG,YANHUA QU,XINXIN LI,FUMIN LEI & HONGXIANG HAN Submitted: 6 May 2015 Liu, S. X., Jiang, N., Xue, D. Y., Cheng, R., Qu, Y. H., Li, X. X., Lei, F. M. & Han, H. X. Accepted: 30 September 2015 (2016). Evolutionary history of Apocheima cinerarius (Lepidoptera: Geometridae), a female doi:10.1111/zsc.12147 flightless moth in northern China. — Zoologica Scripta, 45, 160–174. The alterations in the phylogeographical structures of insects in response to the uplift of the Qinghai–Tibet Plateau and the Quaternary glaciations in eastern Asia, particularly in north- ern China, remain largely unknown. In this study, we selected Apocheima cinerarius, a moth with flightless females, using molecular data (complete mitochondrial genomes and nuclear data) and ecological niche modelling (ENM) to investigate the effects of paleoclimatic changes on the evolutionary history of insects in the area of northern China. The phyloge- netic tree of complete mitochondrial genomes indicated that there were two lineages, the western and eastern lineages. The nuclear gene analyses also detected unique haplotypes in each lineage. Time of the most recent common ancestor (TMRCA) of the two lineages was approximately in Early–Middle Pleistocene. Bayesian skyline plots revealed that the western lineage underwent a population expansion event after the Last Glacial Maximum, whereas the eastern lineage underwent expansion between the Last Interglacial and the Last Glacial Maximum. Our results suggest that A. cinerarius expanded eastward from western sites until the moth was distributed across the entire region of northern China. Then, A. cinerarius underwent contraction into isolated glacial refugia followed by subsequent expansion driven by Pleistocene climate changes, which established a narrow sympatric area. Our results indi- cate that the Quaternary environmental fluctuations had profound influences on the diversifi- cation and demography of an insect in northern China, and the same species in north- western China and north-eastern China have different demographic histories. Corresponding author: Hongxiang Han and Fumin Lei, Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China. E-mails: [email protected]; [email protected] Shuxian Liu, Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101 China and University of the Chinese Academy of Sciences, Beijing, 100049 China. E-mail: [email protected] Nan Jiang, and Dayong Xue, Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101 China. E-mail: [email protected], xuedy@ ioz.ac.cn Rui Cheng, Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101 China and University of the Chinese Academy of Sciences, Beijing, 100049 China. E-mail: [email protected] Yanhua Qu, Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101 China. E-mail: [email protected] Xinxin Li, Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101 China and University of the Chinese Academy of Sciences, Beijing, 100049 China. E-mail: [email protected] Fumin Lei, and Hongxiang Han, Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101 China. E-mail: [email protected], hanhx@ ioz.ac.cn Shuxian Lu and Nan Jiang contributed equally to the present paper. 160 ª 2015 Royal Swedish Academy of Sciences, 45, 2, March 2016, pp 160–174 S. Liu et al. Evolutionary history of Apocheima cinerarius Introduction in climatic conditions during the Pleistocene (Haring et al. Animal phylogeography and patterns of distribution related 2007; Zink et al. 2008, 2009; Olsson et al. 2010; Zhang to geological events and climate change in the temperate et al. 2012). In addition, several studies also indicated that a zone of the Northern Hemisphere have long fascinated geographical gap between the eastern and western ranges biologists and naturalists. The uplift of the Qinghai–Tibet of the azure-winged magpie (Cyanopica cyanus) might be the Plateau (QTP) was the largest geological event in the east- subdivision of a former continuous range during the Pleis- ern Asia and caused dramatic climatic and ecological shifts tocene (Cooper 2000; Palomino et al. 2011). Comparative (Zhang 2000). The uplift of the QTP and the Quaternary phylogeography of two widespread magpies (Cyanopica cya- glaciations are key factors that influence the phylogeo- nus and Pica pica) indicate that bird species with different graphical structure of species in eastern Asia (Cao et al. life histories (e.g. habitat preference and breeding beha- 2012; Lei et al. 2014). viour) might respond differently to fluctuations in the envi- Previous studies have shown that the uplift of the QTP ronment (Zhang et al. 2012). from 1.7 to 3.6 Ma changed the surrounding geography Apocheima cinerarius (Erschoff) is a geometrid moth with and environment, which facilitated the speciation of many wingless females and is distributed from Maracanda east- species in eastern Asia (Li et al. 2001; Qu et al. 2009, 2010; ward across the entire region of northern China to the Cao et al. 2012; Lei et al. 2014). The uplift of the QTP Amur district. This area is in an arid climate zone in the increased the desertification of northern China, and this East Asia monsoon region. The adults of A. cinerarius process had a large effect on the biodiversity of the area emerge from overwintered pupae in soils between the end (Shi et al. 1998; Liu et al. 2001). For example, desertifica- of February and April, when the winter monsoon is strong tion shaped the current biodiversity and distribution pat- and the temperature is very low (Chu 1981; Sattler 1991). tern of a perennial herb (Lagochilus ilicifolius) (Meng & The weak ability for movement, wide distribution and Zhang 2011). The uplift of the plateau also triggered the unique life history make this inactive litter-layer insect an onset of the monsoon circulation, which intensified begin- excellent model organism to study the phylogeographical ning 2.6 Ma, particularly within 0.9–1.2 Ma (Sun et al. pattern and to test the demographic hypothesis of the 2003). However, the effects of the monsoon circulation on insects in northern China. the phylogeographical patterns of the local fauna remain In this study, we combined the mitochondrial genomes unknown. (13 PCGs + 2 rRNAs) and two nuclear genes [translation The Quaternary glaciations led to the extinction or elongation factor 1-alpha (EF1a) as well as the second migration of species, with some surviving in refugia during internal transcribed spacer (ITS2)] and integrated with an the glacial periods and subsequently expanding after the ecological niche model to analyse the phylogeographical glaciation, thus contributing to the current genetic struc- pattern of A. cinerarius. The aims of the study were (i) to ture and distribution (Hewitt 1999, 2000, 2004; Lin et al. investigate the phylogeographical structures of this moth; 2014). Previous studies revealed that the demographic his- (ii) to infer the possible origins, migration routes and tories of most European species are ‘post-LGM expansion’ expansion force of this moth; and (iii) to test whether the mode (Hewitt 1999, 2000, 2004; Kvist et al. 2003). How- demographic history of this moth corresponds to the ‘pre- ever, East Asia, including China, Japan, the Korean Penin- LGM expansion’ mode like other eastern Asian animals. sula and Mongolia, was not completely covered with a widespread ice sheet, which is different from North Amer- Materials and methods ica and Europe (Rost 1994; Ju et al. 2007; Igea et al. 2013). Specimen sampling Many East Asian birds have been hypothesized to undergo We searched for adult specimens on the appropriate host a pre-glacial population expansion, thus considered to fol- plants (Populus, Salix and Elaeagnus). In total, 211 adult low a ‘pre-LGM expansion’ mode (Dai et al. 2011; Qu specimens of A. cinerarius from 31 sampling sites were col- et al. 2011; Zhao et al. 2012; Wang et al. 2013a). For spe- lected across the entire range of this species in China cies that were widely distributed on the Eurasian continent, (Table S1). The specimens were preserved in anhydrous multiple isolated glacial refugia occurred in their area of ethanol at À20 °C and were deposited at the Institute of distribution during the Quaternary glaciations. These refu- Zoology, Chinese Academy of Sciences, Beijing, China gia would have facilitated the differentiation of species (IZCAS). (Qian & Ricklefs 2000; Hu et al. 2013). Previous studies revealed that many bird species distributed across the Eura- DNA extraction, PCR amplification and sequencing sian continent have concordant patterns of ‘western vs. The DNA was extracted using the Qiagen DNeasy Blood eastern lineage divergence’ that resulted from the changes & Tissue Kits (Qiagen, Beijing, China). In all, 27 mitogen- ª 2015 Royal Swedish Academy of Sciences, 45, 2, March 2016, pp 160–174 161 Evolutionary history of Apocheima cinerarius S. Liu et al. omes from representative sampling sites were obtained with Bank