Regional drivers of diversification in the late Quaternary in a widely distributed generalist species, the common pheasant Phasianus colchicus
Simin Liu
State Key Laboratory of Biocontrol, School of Ecology/School of Life Sciences, Sun Yat-sen University, Guangzhou, China
Search for more papers by this authorCorresponding Author
Yang Liu
State Key Laboratory of Biocontrol, School of Ecology/School of Life Sciences, Sun Yat-sen University, Guangzhou, China
Correspondence
Yang Liu, State Key Laboratory of Biocontrol, School of Ecology/School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China.
Email: [email protected]
Search for more papers by this authorEdouard Jelen
World Pheasant Association-France, Merville, France
Search for more papers by this authorMansour Alibadian
Research Department of Zoological Innovation, Institute of Applied Zoology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran
Search for more papers by this authorCheng-Te Yao
High Altitude Experimental Station, Endemic Species Research Institute, Nantou, Taiwan, China
Search for more papers by this authorXintong Li
State Key Laboratory of Biocontrol, School of Ecology/School of Life Sciences, Sun Yat-sen University, Guangzhou, China
Search for more papers by this authorNasrin Kayvanfar
Research Department of Zoological Innovation, Institute of Applied Zoology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran
Search for more papers by this authorYutao Wang
School of Life and Geographic Science, Kashi University, Kashi, China
Search for more papers by this authorFarhad S. M. Vahidi
Department of Animal Biotechnology, Agricultural Biotechnology Research Institute of Iran, Agricultural Research, Education, and Extension Organization, Karaj, Iran
Search for more papers by this authorJian-Lin Han
CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, China
International Livestock Research Institute (ILRI), Nairobi, Kenya
Search for more papers by this authorGombobaatar Sundev
National University of Mongolia and Mongolian Ornithological Society, Ulaanbaatar, Mongolia
Search for more papers by this authorZhengwang Zhang
Key Laboratory for Biodiversity Sciences and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, China
Search for more papers by this authorManuel Schweizer
Naturhistorisches Museum Bern, Bern, Switzerland
Institute of Ecology and Evolution, University of Bern, Bern, Switzerland
Search for more papers by this authorSimin Liu
State Key Laboratory of Biocontrol, School of Ecology/School of Life Sciences, Sun Yat-sen University, Guangzhou, China
Search for more papers by this authorCorresponding Author
Yang Liu
State Key Laboratory of Biocontrol, School of Ecology/School of Life Sciences, Sun Yat-sen University, Guangzhou, China
Correspondence
Yang Liu, State Key Laboratory of Biocontrol, School of Ecology/School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China.
Email: [email protected]
Search for more papers by this authorEdouard Jelen
World Pheasant Association-France, Merville, France
Search for more papers by this authorMansour Alibadian
Research Department of Zoological Innovation, Institute of Applied Zoology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran
Search for more papers by this authorCheng-Te Yao
High Altitude Experimental Station, Endemic Species Research Institute, Nantou, Taiwan, China
Search for more papers by this authorXintong Li
State Key Laboratory of Biocontrol, School of Ecology/School of Life Sciences, Sun Yat-sen University, Guangzhou, China
Search for more papers by this authorNasrin Kayvanfar
Research Department of Zoological Innovation, Institute of Applied Zoology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran
Search for more papers by this authorYutao Wang
School of Life and Geographic Science, Kashi University, Kashi, China
Search for more papers by this authorFarhad S. M. Vahidi
Department of Animal Biotechnology, Agricultural Biotechnology Research Institute of Iran, Agricultural Research, Education, and Extension Organization, Karaj, Iran
Search for more papers by this authorJian-Lin Han
CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, China
International Livestock Research Institute (ILRI), Nairobi, Kenya
Search for more papers by this authorGombobaatar Sundev
National University of Mongolia and Mongolian Ornithological Society, Ulaanbaatar, Mongolia
Search for more papers by this authorZhengwang Zhang
Key Laboratory for Biodiversity Sciences and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, China
Search for more papers by this authorManuel Schweizer
Naturhistorisches Museum Bern, Bern, Switzerland
Institute of Ecology and Evolution, University of Bern, Bern, Switzerland
Search for more papers by this authorHandling Editor: Fumin Lei
Abstract
Aim
Pleistocene climate and associated environmental changes have influenced phylogeographic patterns of many species. These not only depend on a species’ life history but also vary regionally. Consequently, populations of widespread species that occur in several biomes might display different evolutionary trajectories. We aimed to identify regional drivers of diversification in the common pheasant, a widely distributed ecological generalist.
Location
Asia.
Taxon
Common pheasant Phasianus colchicus.
Methods
Using a comprehensive geographical sampling of 204 individuals from the species’ entire range genotyped at seven nuclear and two mitochondrial loci, we reconstructed spatio-temporal diversification and demographic history of the common pheasant. We applied Bayesian phylogenetic inference to describe phylogeographic structure, generated a species tree and inferred demographic history within and migration between lineages. Moreover, to establish a taxonomic framework, we conducted a species delimitation analysis.
Results
The common pheasant diversified during the Late Pleistocene into eight distinct lineages. It originated at the edge of the Qinghai–Tibetan plateau and spread to East and Central Asia. Only the widely distributed lowland lineage of East Asia displayed recent range expansion. Greater phylogeographic structure was identified elsewhere, with lineages showing no sign of recent demographic changes. One lineage in south-central China is the result of long-term isolation within a climatically stable but topographically complex region. In lineages from arid Central Asia and China, range expansions were impeded by repeated population fragmentation during dry glacial periods and by recent aridification.
Main conclusions
Spatio-temporal phylogeographic frameworks of widespread taxa such as the common pheasant provide valuable opportunities to identify divergent drivers of regional diversification. Our results suggest that diversification and population histories in the eight distinct evolutionary lineages were shaped by regionally variable effects of past climate and associated environmental changes. The evolutionary history of the common pheasant is best reflected by its being split into three species.
Open Research
DATA AVAILABILITY STATEMENT
Detailed sample localities and GenBank accession numbers of (MT840913 - MT842838) of deposited DNA sequences are available in Table S1 in Supporting information. Input files for BEAST, IMa and BP&P analyses are available on DRYAD (https://doi.org/10.5061/dryad.1rn8pk0r9).
Supporting Information
| Filename | Description |
|---|---|
| jbi13964-sup-0001-Supinfo.docWord document, 1.3 MB | Supplementary Material |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Alaei Kakhki, N., Aliabadian, M., Förschler, M. I., Ghasempouri, S. M., Kiabi, B. H., Verde Arregoitia, L. D., & Schweizer, M. (2018). Phylogeography of the Oenanthe hispanica–pleschanka–cypriaca complex (Aves, Muscicapidae: Saxicolinae): Diversification history of open-habitat specialists based on climate niche models, genetic data, and morphometric data. Journal of Zoological Systematics and Evolutionary Research, 56, 408–427.https://doi.org/10.1111/jzs.12206.
- Bielejec, F., Rambaut, A., Suchard, M. A., & Lemey, P. (2011). SPREAD: Spatial phylogenetic reconstruction of evolutionary dynamics. Bioinformatics, 27, 2910–2912. https://doi.org/10.1093/bioinformatics/btr481
- Bouckaert, R., & Heled, J. (2014). DensiTree 2: Seeing trees through the forest. bioRxiv 012401.
- Bouckaert, R., Heled, J., Kuhnert, D., Vaughan, T., Wu, C. H., Xie, D., … Drummond, A. J. (2014). BEAST 2: A software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 10, e1003537. https://doi.org/10.1371/journal.pcbi.1003537
- Cai, T. L., Fjeldsa, J., Wu, Y. J., Shao, S. M., Chen, Y. H., Quan, Q., … Lei, F. M. (2018). What makes the Sino-Himalayan mountains the major diversity hotspots for pheasants? Journal of Biogeography, 45, 640–651. https://doi.org/10.1111/jbi.13156
- Dai, C., Zhao, N., Wang, W., Lin, C., Gao, B., Yang, X., … Lei, F. (2011). Profound climatic effects on two East Asian black-throated tits (Ave: Aegithalidae), revealed by ecological niche models and phylogeographic analysis. PLoS ONE, 6, e29329. https://doi.org/10.1371/journal.pone.0029329
- Delacour, J. (1977). The pheasants of the world (2nd revised edition). Lamarsh, UK: Spur Publications.
- Dong, F., Hung, C.-M., Li, X.-L., Gao, J.-Y., Zhang, Q., Wu, F., … Yang, X.-J. (2017). Ice age unfrozen: Severe effect of the last interglacial, not glacial, climate change on East Asian avifauna. BMC Evolutionary Biology, 17, 244. https://doi.org/10.1186/s12862-017-1100-2
- Drovetski, S. V., Semenov, G., Red'kin, Y. A., Sotnikov, V. N., Fadeev, I. V., & Koblik, E. A. (2015). Effects of asymmetric nuclear introgression, introgressive mitochondrial sweep, and purifying selection on phylogenetic reconstruction and divergence estimates in the Pacific clade of Locustella warblers. PLoS ONE, 10, e0122590. https://doi.org/10.1371/journal.pone.0122590
- Drummond, A. J., & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214. https://doi.org/10.1186/1471-2148-7-214
- Edwards, S. V., & Beerli, P. (2000). Perspective: Gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Evolution, 54, 1839–1854. https://doi.org/10.1111/j.0014-3820.2000.tb01231.x
- Garcia, J. T., Manosa, S., Morales, M. B., Ponjoan, A., de la Morena, E. L. G., Bota, G., … Davila, J. A. (2011). Genetic consequences of interglacial isolation in a steppe bird. Molecular Phylogenetics and Evolution, 61, 671–676. https://doi.org/10.1016/j.ympev.2011.07.017
- Gombobaatar, S., Monks, E. M., Seidler, R., Sumiya, D., Tseveenmyadag, N., Bayarkhuu, S., …Uuganbayar, C. H. (2011). Regional Red List Series, Vol. 7. Birds. Zoological Society of London, National University of Mongolia and Mongolian Ornithological Society. 1036 pp.
- Heled, J., & Drummond, A. J. (2010). Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution, 27, 570–580. https://doi.org/10.1093/molbev/msp274
- Hennache, A., & Ottaviani, M. (2019). Monographie des faisans, mise à jour 2018, 157, pages, ed. France: France: W.P.A.
- Hewitt, G. (2000). The genetic legacy of the Quaternary ice ages. Nature, 405, 907–913. https://doi.org/10.1038/35016000
- Hey, J. (2010a). Isolation with migration models for more than two populations. Molecular Biology and Evolution, 27, 905–920. https://doi.org/10.1093/molbev/msp296
- Hey, J. (2010b). The divergence of Chimpanzee species and subspecies as revealed in multipopulation isolation-with-migration analyses. Molecular Biology and Evolution, 27, 921–933. https://doi.org/10.1093/molbev/msp298
- Hillis, D. M., & Bull, J. J. (1993). An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology, 42, 182–192. https://doi.org/10.1093/sysbio/42.2.182
- Huang, X. L., Qiao, G. X., & Lei, F. M. (2010). Use of parsimony analysis to identify areas of endemism of Chinese birds: Implications for conservation and biogeography. International Journal of Molecular Sciences, 11, 2097–2108. https://doi.org/10.3390/ijms11052097
- Hung, C. M., Drovetski, S. V., & Zink, R. M. (2017). The roles of ecology, behaviour and effective population size in the evolution of a community. Molecular Ecology, 26, 3775–3784. https://doi.org/10.1111/mec.14152
- Huson, D. H., & Bryant, D. (2006). Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23, 254–267. https://doi.org/10.1093/molbev/msj030
- Johansson, U. S., Alstrom, P., Olsson, U., Ericson, P. G. R., Sundberg, P., & Price, T. D. (2007). Build-up of the Himalayan avifauna through immigration: A biogeographical analysis of the Phylloscopus and Seicercus warblers. Evolution, 61, 324–333. https://doi.org/10.1111/j.1558-5646.2007.00024.x.
- Kamp, L., Pasinelli, G., Milanesi, P., Drovetski, S. V., Kosinski, Z., Kossenko, S., … Schweizer, M. (2019). Significant Asia-Europe divergence in the middle spotted woodpecker (Aves, Picidae). Zoologica Scripta, 48, 17–32. https://doi.org/10.1111/zsc.12320
- Kayvanfar, N., Aliabadian, M., Niu, X. J., Zhang, Z. W., & Liu, Y. (2017). Phylogeography of the common pheasant phasianus colchicus. Ibis, 159, 430–442. https://doi.org/10.1111/ibi.12455
- Lei, F., Qu, Y., Song, G., Alström, P., & Fjeldså, J. (2015). The potential drivers in forming avian biodiversity hotspots in the East Himalaya-Mountains of Southwest China. Integrative Zoology, 10, 171–181. https://doi.org/10.1111/1749-4877.12121
- Leigh, J. W., & Bryant, D. (2015). POPART: Full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6, 1110–1116. https://doi.org/10.1111/2041-210X.12410.
- Lemey, P., Rambaut, A., Drummond, A. J., & Suchard, M. A. (2009). Bayesian phylogeography finds its roots. PLoS Computational Biology, 5, 16. https://doi.org/10.1371/journal.pcbi.1000520
- Leroy, S. A. G., Marret, F., Gibert, E., Chalie, F., Reyss, J. L., & Arpe, K. (2007). River inflow and salinity changes in the Caspian Sea during the last 5500 years. Quaternary Science Reviews, 26, 3359–3383. https://doi.org/10.1016/j.quascirev.2007.09.012
- Li, J. W., Yeung, C. K. L., Tsai, P. W., Lin, R. C., Yeh, C. F., Yao, C. T., … Li, S. H. (2010). Rejecting strictly allopatric speciation on a continental island: Prolonged postdivergence gene flow between Taiwan (Leucodioptron taewanus, Passeriformes Timaliidae) and Chinese (L. canorum canorum) hwameis. Molecular Ecology, 19, 494–507. https://doi.org/10.1111/j.1365-294X.2009.04494.x.
- Liu, Y., Hu, J. H., Li, S. H., Duchen, P., Wegmann, D., & Schweizer, M. (2016). Sino-Himalayan mountains act as cradles of diversity and immigration centres in the diversification of parrotbills (Paradoxornithidae). Journal of Biogeography, 43, 1488–1501. https://doi.org/10.1111/jbi.12738
- Liu, Y., Liu, S., Zhang, N., Chen, D. E., Que, P., Liu, N., … Wang, B. (2019). Genome assembly of the Common Pheasant Phasianus colchicus: A model for speciation and ecological genomics. Genome Biology and Evolution, 11, 3326–3331. https://doi.org/10.1093/gbe/evz249
- Liu, Y., Zhan, X. J., Wang, N., Chang, J., & Zhang, Z. W. (2010). Effect of geological vicariance on mitochondrial DNA differentiation in Common Pheasant populations of the Loess Plateau and eastern China. Molecular Phylogenetics and Evolution, 55, 409–417. https://doi.org/10.1016/j.ympev.2009.12.026
- Madge, S. C., McGowan, P. J. K., & Kirwan, G. M. (2002). Pheasants, partridges and grouse: a guide to the pheasants, partridges, quails, grouse, guineafowl, buttonquails and sandgrouse of the world. London: A & C Black Publishers Ltd.
- Maslin, M. A., Brierley, C. M., Milner, A. M., Shultz, S., Trauth, M. H. & Wilson, K. E. (2014). East African climate pulses and early human evolution. Quaternary Science Reviews, 101, 1–17.
- McGowan, P. J. K., & Kirwan, G. M. (2019). Common pheasant (<em>Phasianus colchicus</em>). In J. Hoyo, A. Elliot, J. Sargatal, D. A. Christie, & E. Juana (Eds.), Handbook of the Birds of the World Alive (pp. 542–543). Barcelona: Lynx Edicions.
- Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic treesi. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA pp. 1–8.
- Owen, L. A., Caffee, M. W., Finkel, R. C., & Seong, Y. B. (2008). Quaternary glaciation of the Himalayan-Tibetan orogen. Journal of Quaternary Science, 23, 513–531. https://doi.org/10.1002/jqs.1203.
- Päckert, M., Martens, J., Sun, Y. H., Severinghaus, L. L., Nazarenko, A. A., Ting, J., … Tietze, D. T. (2012). Horizontal and elevational phylogeographic patterns of Himalayan and Southeast Asian forest passerines (Aves: Passeriformes). Journal of Biogeography, 39, 556–573. https://doi.org/10.1111/j.1365-2699.2011.02606.x
- Päckert, M., Martens, J., Sun, Y.-H., & Tietze, D. (2015). Evolutionary history of passerine birds (Aves: Passeriformes) from the Qinghai-Tibetan plateau: From a pre-Quarternary perspective to an integrative biodiversity assessment. Journal of Ornithology, 156(Suppl. 1), S355–S365. https://doi.org/10.1007/s10336-015-1185-6
- Price, T. (2008). Speciation in birds. Greenwood Village CO: Roberts and Company.
- Price, T. D., Hooper, D. M., Buchanan, C. D., Johansson, U. S., Tietze, D. T., Alström, P., … Mohan, D. (2014). Niche filling slows the diversification of Himalayan songbirds. Nature, 509, 222–225. https://doi.org/10.1038/nature13272
- Pyron, R. A., & Burbrink, F. T. (2009). Lineage diversification in a widespread species: Roles for niche divergence and conservatism in the common kingsnake, <em>Lampropeltis getula</em>. Molecular Ecology, 18, 3443–3457. https://doi.org/10.1111/j.1365-294X.2009.04292.x.
- Qu, H. W., Qu, J. Y., Wang, Y. H., Guo, C. H., Shi, B. Y., & Liu, N. F. (2017). Subspecies boundaries and recent evolution history of the common pheasant (Phasianus colchicus) across China. Biochemical Systematics and Ecology, 71, 155–162. https://doi.org/10.1016/j.bse.2017.02.001
- Qu, J. Y., Liu, N. F., Bao, X. K., & Wang, X. L. (2009). Phylogeography of the ring-necked pheasant (Phasianus colchicus) in China. Molecular Phylogenetics and Evolution, 52, 125–132. https://doi.org/10.1016/j.ympev.2009.03.015
- Qu, Y. H., Ericson, P. G. P., Quan, Q., Song, G., Zhang, R. Y., Gao, B., & Lei, F. M. (2014). Long-term isolation and stability explain high genetic diversity in the Eastern Himalaya. Molecular Ecology, 23, 705–720. https://doi.org/10.1111/mec.12619
- Rambaut, A. (2008) FigTree 1.4, published by the author. Retrieved from http://tree.bio.ed.ac.uk/software/figtree/
- Rambaut, A., Suchard, M. A., & Drummond, A. J. (2013) Tracer v 1.6, Retrieved from http://tree.bio.ed.ac.uk/software/tracer/.
- Rannala, B., & Yang, Z. H. (2013). Improved reversible jump algorithms for Bayesian species delimitation. Genetics, 194, 245–253. https://doi.org/10.1534/genetics.112.149039
- Sangster, G. (2018) Integrative taxonomy of birds: The nature and delimitation of species. In D. T. Tietze (Eds.), Bird species, (pp. 9–38). Cham, Switzerland: Springer Nature. https://doi.org/10.1007/978-3-319-91689-7.
10.1007/978-3-319-91689-7_2 Google Scholar
- Solokha, A. V. (1994) On the evolution of pheasants (Pasianus colchicus L.) in Middle Asia. In V. Fet & K. I. Atamuradov (Eds.), Biogeography and ecology of turkmenistan (pp. 295–306). Netherlands: Kluwer Academic Publishers.
10.1007/978-94-011-1116-4_18 Google Scholar
- Song, G., Zhang, R. Y., Alstrom, P., Irestedt, M., Cai, T. L., Qu, Y. H., … Lei, F. M. (2018). Complete taxon sampling of the avian genus Pica (magpies) reveals ancient relictual populations and synchronous Late-Pleistocene demographic expansion across the Northern Hemisphere. Journal of Avian Biology, 49, e01612. https://doi.org/10.1111/jav.01612.
- Stamatakis, A. (2014). RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
- Statham, M. J., Murdoch, J., Janecka, J., Aubry, K. B., Edwards, C. J., Soulsbury, C. D., … Sacks, B. N. (2014). Range-wide multilocus phylogeography of the red fox reveals ancient continental divergence, minimal genomic exchange and distinct demographic histories. Molecular Ecology, 23, 4813–4830. https://doi.org/10.1111/mec.12898
- Stein, R. W., Brown, J. W., & Mooers, A. O. (2015). A molecular genetic time scale demonstrates Cretaceous origins and multiple diversification rate shifts within the order Galliformes (Aves). Molecular Phylogenetics and Evolution, 92, 155–164. https://doi.org/10.1016/j.ympev.2015.06.005
- Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729. https://doi.org/10.1093/molbev/mst197
- Weir, J. T., & Schluter, D. (2004). Ice sheets promote speciation in boreal birds. Proceedings of the Royal Society of London Series B-Biological Sciences, 271, 1881–1887. https://doi.org/10.1098/rspb.2004.2803
- Weir, J. T., & Schluter, D. (2008). Calibrating the avian molecular clock. Molecular Ecology, 17, 2321–2328. https://doi.org/10.1111/j.1365-294X.2008.03742.x
- Xing, Y. W., & Ree, R. H. (2017). Uplift-driven diversification in the Hengduan Mountains, a temperate biodiversity hotspot. Proceedings of the National Academy of Sciences of the United States of America, 114, E3444–E3451. https://doi.org/10.1073/pnas.1616063114
- Yamagishi, Y., Yanaka, H., Suzuki, K., Tsuboi, S., Isse, T., Obayashi, M., … Nagao, H. (2010). Visualization of geoscience data on Google Earth: Development of a data converter system for seismic tomographic models. Computers & Geosciences, 36, 373–382. https://doi.org/10.1016/j.cageo.2009.08.007
- Yang, Z. H. (2015). The BPP program for species tree estimation and species delimitation. Current Zoology, 61, 854–865. https://doi.org/10.1093/czoolo/61.5.854
- Yang, Z. H., & Rannala, B. (2010). Bayesian species delimitation using multilocus sequence data. Proceedings of the National Academy of Sciences of the United States of America, 107(20), 9264–9269. https://doi.org/10.1073/pnas.0913022107.
- Zhao, H. F., Lei, F. M., Qu, Y. H., & Lu, J. L. (2007). Conservation priority based on avian subspecific differentiation of endemic species. Acta Zoologica Sinica, 53, 378–382. https://doi.org/10.1360/crad20071213.
10.1360/crad20071213 Google Scholar
- Zhao, M., Chang, Y. B., Kimball, R. T., Zhao, J., Lei, F. M., & Qu, Y. H. (2019). Pleistocene glaciation explains the disjunct distribution of the Chestnut-vented Nuthatch (Aves, Sittidae). Zoologica Scripta, 48, 33–45. https://doi.org/10.1111/zsc.12327
- Zhao, Y., Liu, Y. L., Guo, Z. T., Fang, K. Y., Li, Q., & Cao, X. Y. (2017). Abrupt vegetation shifts caused by gradual climate changes in central Asia during the Holocene. Science China-Earth Sciences, 60, 1317–1327. https://doi.org/10.1007/s11430-017-9047-7
