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Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Exploring the diversity of Asian Cryptocercus (Blattodea : Cryptocercidae): species delimitation based on chromosome numbers, morphology and molecular analysis

Qikun Bai A , Lili Wang A , Zongqing Wang A , Nathan Lo B and Yanli Che A C
+ Author Affiliations
- Author Affiliations

A College of Plant Protection, Southwest University, Beibei, Chongqing 400716, P.R. China.

B School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW 2006, Australia.

C Corresponding author. Email: shirleyche2000@126.com

Invertebrate Systematics 32(1) 69-91 https://doi.org/10.1071/IS17003
Submitted: 10 January 2017  Accepted: 1 June 2017   Published: 9 January 2018

Abstract

Woodroaches from the genus Cryptocercus Scudder, 1862 are known to display low levels of morphological divergence, yet significant genetic divergence and variability in chromosome number. Compared with Cryptocercus taxa from North America, the diversity of the genus in Asia has received relatively little attention. We performed morphological and karyotypic examinations of multiple taxa from several previously unsampled mountainous areas of central and south-western China, and identified nine candidate species primarily on the basis of chromosome number. We then investigated diversity across all Asian Cryptocercus, through phylogenetic analyses of 135 COI sequences and 74 28S rRNA sequences from individuals of 28 localities, including species delimitation analysis in General Mixed Yule Coalescent (GMYC) and Automatic Barcode Gap Discovery (ABGD). Phylogenetic results indicated that individuals from the same locality constituted well supported clades. The congruence of GMYC and ABGD results were in almost perfect accord, with 28 candidate species described on the basis of karyotypes (including the nine identified in this study). We provide evidence that each valley population in the Hengduan Mountains contains a separate evolving lineage. We conclude that the principal cause of the rich Cryptocercus diversity in China has been the uplift of the Qinghai-Tibet Plateau.

Additional keywords: ABGD, biogeography, DNA barcode, GMYC, Hengduan Mountains, woodroach


References

Aldrich, B. T., Zolnerowich, G., and Kambhampati, S. (2004). Interspecific morphological variation in the wood-feeding cockroach, Cryptocercus (Dictyoptera: Cryptocercidae). Arthropod Structure & Development 33, 443–451.
Interspecific morphological variation in the wood-feeding cockroach, Cryptocercus (Dictyoptera: Cryptocercidae).Crossref | GoogleScholarGoogle Scholar |

Allégre, C. J., Courtillot, V., Tapponnier, P., Hirn, A., Mattauer, M., Coulon, C., Jaeger, J. J., Achache, J., Schärer, U., and Marcoux, J. (1984). Structure and evolution of the Himalaya–Tibet orogenic belt. Nature 307, 17–22.
Structure and evolution of the Himalaya–Tibet orogenic belt.Crossref | GoogleScholarGoogle Scholar |

Bey-Bienko, G. (1935). Descriptions of six new species of Palearctic Blattodea. Konowia: Zeitschrift für systematische Insektenkunde 14, 117–134.

Bey-Bienko, G. (1938). On some new or interesting Asiatic Blattodea. Annals & Magazine of Natural History 1, 230–238.
On some new or interesting Asiatic Blattodea.Crossref | GoogleScholarGoogle Scholar |

Burnside, C. A., Smith, P. T., and Kambhampati, S. (1999). Three new species of the wood roach, Cryptocercus (Blattodea: Cryptocercidae), from the eastern United States. Journal of the Kansas Entomological Society 72, 361–378.

Cameron, S. L., Lo, N., Bourguignon, T., Svenson, G. J., and Evans, T. A. (2012). A mitochondrial genome phylogeny of termites (Blattodea: Termitoidae): robust support for interfamilial relationships and molecular synapomorphies define major clades. Molecular Phylogenetics and Evolution 65, 163–173.
A mitochondrial genome phylogeny of termites (Blattodea: Termitoidae): robust support for interfamilial relationships and molecular synapomorphies define major clades.Crossref | GoogleScholarGoogle Scholar |

Caterino, M. S., Cho, S., and Sperling, F. A. (2000). The current state of insect molecular systematics: a thriving Tower of Babel. Annual Review of Entomology 45, 1–54.
The current state of insect molecular systematics: a thriving Tower of Babel.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVequrg%3D&md5=08e70b013b2b69af184bf4304f997c65CAS |

Che, Y. L., Wang, D., Shi, Y., Du, X. H., Zhao, Y. Q., Lo, N., and Wang, Z. Q. (2016). A global molecular phylogeny and timescale of evolution for Cryptocercus woodroaches. Molecular Phylogenetics Evolution 98, 201–209.

Che, Y. L., Gui, S. H., Lo, N., Ritchie, A., and Wang, Z. Q. (2017). Species delimitation and phylogenetic relationships in ectobiid cockroaches (Dictyoptera, Blattodea) from China. PLoS One 12, e0169006.
Species delimitation and phylogenetic relationships in ectobiid cockroaches (Dictyoptera, Blattodea) from China.Crossref | GoogleScholarGoogle Scholar |

Desalle, R. (2006). Species discovery versus species identification in DNA barcoding efforts: response to Rubinoff. Conservation Biology 20, 1545–1547.
Species discovery versus species identification in DNA barcoding efforts: response to Rubinoff.Crossref | GoogleScholarGoogle Scholar |

Drummond, A. J., and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.
BEAST: Bayesian evolutionary analysis by sampling trees.Crossref | GoogleScholarGoogle Scholar |

Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=9f0ae72ae0dad8d77ae7a57341dd73f7CAS |

Elliott, M. C. (2000). The limits of Tartary: Manchuria in imperial and national geographies. The Journal of Asian Studies 59, 603–646.
The limits of Tartary: Manchuria in imperial and national geographies.Crossref | GoogleScholarGoogle Scholar |

Evangelista, D. A., Bourne, G., and Ware, J. L. (2014). Species richness estimates of Blattodea s.s. (Insecta: Dictyoptera) from northern Guyana vary depending upon methods of species delimitation. Systematic Entomology 39, 150–158.
Species richness estimates of Blattodea s.s. (Insecta: Dictyoptera) from northern Guyana vary depending upon methods of species delimitation.Crossref | GoogleScholarGoogle Scholar |

Everaerts, C., Maekawa, K., Farine, J. P., Shimada, K., Luykx, P., Brossut, R., and Nalepa, C. A. (2008). The Cryptocercus punctulatus species complex (Dictyoptera: Cryptocercidae) in the eastern United States: comparison of cuticular hydrocarbons, chromosome number, and DNA sequences. Molecular Phylogenetics and Evolution 47, 950–959.
The Cryptocercus punctulatus species complex (Dictyoptera: Cryptocercidae) in the eastern United States: comparison of cuticular hydrocarbons, chromosome number, and DNA sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtlyhu74%3D&md5=bf02b8a880c1697ca12dd22740b7f760CAS |

Ezard, T., Fujisawa, T., and Barraclough, T. (2009). Splits: species’ limits by threshold statistics. R package version 1.0–11/r29.

Fujisawa, T., and Barraclough, T. G. (2013). Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Systematic Biology 62, 707–724.
Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets.Crossref | GoogleScholarGoogle Scholar |

Grandcolas, P. (2000). Cryptocercus matilei n. sp., du Sichuan de Chine [Dictyoptera, Blattaria, Polyphaginae]. Revue Francaise d’Entomologie 22, 223–226.

Grandcolas, P., Park, Y. C., Choe, J. C., Piulachs, M. D., Bellés, X., D’Haese, C., Farine, J. P., Brossut, R., and Farine, J. P. (2001). What does Cryptocercus kyebangensis, n. sp. (Dictyoptera, Blattaria, Polyphagidae) from Korea reveal about Cryptocercus evolution? A study in morphology, molecular phylogeny, and chemistry of tergal glands. Proceedings. Academy of Natural Sciences of Philadelphia 151, 61–79.
What does Cryptocercus kyebangensis, n. sp. (Dictyoptera, Blattaria, Polyphagidae) from Korea reveal about Cryptocercus evolution? A study in morphology, molecular phylogeny, and chemistry of tergal glands.Crossref | GoogleScholarGoogle Scholar |

Grandcolas, P., Legendre, F., Park, Y. C., Belles, X., Murienne, J., and Pellens, R. (2005). The genus Cryptocercus in East Asia: distribution and new species (Insecta, Dictyoptera, Blattaria, Polyphagidae). Zoosystema 27, 725–732.

Hausmann, A., Haszprunar, G., and Hebert, P. D. N. (2011). DNA barcoding the geometrid fauna of Bavaria (Lepidoptera): successes, surprises, and questions. PLoS One 6, e17134.
DNA barcoding the geometrid fauna of Bavaria (Lepidoptera): successes, surprises, and questions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisFSrs74%3D&md5=e84e7d181d44973bf731db86ae0a8203CAS |

Hebert, P. D. N., Cywinska, A., Ball, S. L., and deWaard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B, Biological Sciences 270, 313–321.
Biological identifications through DNA barcodes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktVWiu7g%3D&md5=c0443b02dbd64e2f00e8510254878405CAS |

Hebert, P. D. N., Stoeckle, M. Y., Zemlak, T. S., and Francis, C. M. (2004). Identification of birds through DNA barcodes. PLoS Biology 2, e312.
Identification of birds through DNA barcodes.Crossref | GoogleScholarGoogle Scholar |

Inward, D. J., Vogler, A. P., and Eggleton, P. (2007). A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology. Molecular Phylogenetics and Evolution 44, 953–967.
A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1als7g%3D&md5=418daabe8c78c034a0ff31b5406d6886CAS |

Kambhampati, S. (1996). Phylogenetic relationship among cockroach families inferred from mitochondrial 12S rRNA gene sequence. Systematic Entomology 21, 89–98.

Kambhampati, S., Luykx, P., and Nalepa, C. A. (1996). Evidence for sibling species in Cryptocercus punctulatus, the wood roach, from variation in mitochondrial DNA and karyotype. Heredity 76, 1–12.

Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.
A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXmtFSktg%3D%3D&md5=cdf76744b4b364eb254b209d02ea7b1aCAS |

Klass, K. D., and Meier, R. (2006). A phylogenetic analysis of Dictyoptera (Insecta) based on morphological characters. Entomologische Abhandlungen 63, 3–50.

Knebelsberger, T., and Miller, M. A. (2007). Revision and phylogeny of the subaptera-group of Phyllodromica (Blattoptera: Blattellidae: Ectobiinae), including a parthenogenetic species and the evaluation of COI sequences for species identification (DNA barcoding). Zootaxa 1522, 1–68.

Lanfear, R., Calcott, B., Ho, S. Y., and Guindon, S. (2012). Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnt1ehsbg%3D&md5=26f6e036355c63beec261d5ea5725683CAS |

Li, Y., Wang, Z. Q., and Che, Y. L. (2013). A comparative study of the oothecae and female genitalia of seven species of Blattodea. Acta Zootaxonomica Sinica 38, 16–26.

Liu, J., Moller, M., Provan, J., Gao, L. M., Poudel, R. C., and Li, D. Z. (2013). Geological and ecological factors drive cryptic speciation of yews in a biodiversity hotspot. New Phytologist 199, 1093–1108.
Geological and ecological factors drive cryptic speciation of yews in a biodiversity hotspot.Crossref | GoogleScholarGoogle Scholar |

Liu, J. Q., Duan, Y. W., Hao, G., Ge, X. J., and Sun, H. (2014). Evolutionary history and underlying adaptation of alpine plants on the Qinghai–Tibet Plateau. Journal of Systematics and Evolution 52, 241–249.
Evolutionary history and underlying adaptation of alpine plants on the Qinghai–Tibet Plateau.Crossref | GoogleScholarGoogle Scholar |

Lo, N., Tokuda, G., Watanabe, H., Rose, H., Slaytor, M., Maekawa, K., Bandi, C., and Noda, H. (2000). Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Current Biology 10, 801–804.
Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkslSiurs%3D&md5=4e811f0ebaf79b1e65d001850583d8edCAS |

Lo, N., Luykx, P., Santoni, R., Beninati, T., Bandi, C., Casiraghi, M., Wen-hua, L., Zakharov, E. V., and Nalepa, C. A. (2006). Molecular phylogeny of Cryptocercus wood-roaches based on mitochondrial COII and 16S sequences, and chromosome numbers in Palearctic representatives. Zoological Science 23, 393–398.
Molecular phylogeny of Cryptocercus wood-roaches based on mitochondrial COII and 16S sequences, and chromosome numbers in Palearctic representatives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xnt1Citb4%3D&md5=814aa296daf76f0ff8b9a2f72bc55adfCAS |

Lo, N., Beninati, T., Stone, F., Walker, J., and Sacchi, L. (2007). Cockroaches that lack Blattabacterium endosymbionts: the phylogenetically divergent genus Nocticola. Biology Letters 3, 327–330.
Cockroaches that lack Blattabacterium endosymbionts: the phylogenetically divergent genus Nocticola.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnt1Glu7c%3D&md5=63546633a722ff2f9997140a3fa54154CAS |

Luykx, P. (1983). XO:XX sex chromosomes and Robertsonian variation in the autosomes of the wood-roach Cryptocercus punctulatus (Dictyoptera: Blattaria: Cryptocercidae). Annals of the Entomological Society of America 76, 518–522.
XO:XX sex chromosomes and Robertsonian variation in the autosomes of the wood-roach Cryptocercus punctulatus (Dictyoptera: Blattaria: Cryptocercidae).Crossref | GoogleScholarGoogle Scholar |

McKittrick, F. A. (1964). Evolutionary studies of cockroaches. Cornell Univ. Agric. Exp. Sta., N. Y. State Coll. Of Agric. Mem. 389, 197 pp., Pls. 1–64.

Monaghan, M. T., Wild, R., Elliot, M., Fujisawa, T., Balke, M., Inward, D. J., Lees, D. C., Ranaivosolo, R., Eggleton, P., Barraclough, T. G., and Vogler, A. P. (2009). Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Systematic Biology 58, 298–311.
Accelerated species inventory on Madagascar using coalescent-based models of species delineation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1Wqu7%2FO&md5=9df7e3be72f42089712f2470b98012faCAS |

Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A., and Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
Biodiversity hotspots for conservation priorities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhs1Olsr4%3D&md5=b98e58fd361c7bffff31e39f583c5580CAS |

Nalepa, C. A. (1984). Colony composition, protozoan transfer and some life history characteristics of the woodroach Cryptocercus punctulatus Scudder (Dictyoptera: Cryptocercidae). Behavioral Ecology and Sociobiology 14, 273–279.
Colony composition, protozoan transfer and some life history characteristics of the woodroach Cryptocercus punctulatus Scudder (Dictyoptera: Cryptocercidae).Crossref | GoogleScholarGoogle Scholar |

Nalepa, C., Byers, G., Bandi, C., and Sironi, M. (1997). Description of Cryptocercus clevelandi (Dictyoptera: Cryptocercidae) from the northwestern United States, molecular analysis of bacterial symbionts in its fat body, and notes on biology, distribution, and biogeography. Annals of the Entomological Society of America 90, 416–424.
Description of Cryptocercus clevelandi (Dictyoptera: Cryptocercidae) from the northwestern United States, molecular analysis of bacterial symbionts in its fat body, and notes on biology, distribution, and biogeography.Crossref | GoogleScholarGoogle Scholar |

Park, Y. C., and Choe, J. C. (2003). Life history and population dynamics of Korean woodroach (Cryptocercus kyebangensis) populations. Korean Journal of Biological Sciences 7, 111–117.
Life history and population dynamics of Korean woodroach (Cryptocercus kyebangensis) populations.Crossref | GoogleScholarGoogle Scholar |

Park, Y. C., Maekawa, K., Matsumoto, T., Santoni, R., and Choe, J. C. (2004). Molecular phylogeny and biogeography of the Korean woodroaches Cryptocercus spp. Molecular Phylogenetics and Evolution 30, 450–464.
Molecular phylogeny and biogeography of the Korean woodroaches Cryptocercus spp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjtVGitw%3D%3D&md5=4701ebf733a669e00de764d167d30972CAS |

Pons, J., Barraclough, T., Gomez-Zurita, J., Cardoso, A., Duran, D., Hazell, S., Kamoun, S., Sumlin, W., and Vogler, A. (2006). Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55, 595–609.
Sequence-based species delimitation for the DNA taxonomy of undescribed insects.Crossref | GoogleScholarGoogle Scholar |

Puillandre, N., Lambert, A., Brouillet, S., and Achaz, G. (2012). ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.
ABGD, Automatic Barcode Gap Discovery for primary species delimitation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38zlsFeltQ%3D%3D&md5=dea740a238d308acb00905d2cd6b7936CAS |

R Core Team (2013) ‘R: a Language and Environment for Statistical Computing.’ (R Foundation for Statistical Computing: Vienna, Austria.)

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar |

Royden, L. H., Burchfiel, B. C., and van der Hilst, R. D. (2008). The geological evolution of the Tibetan Plateau. Science 321, 1054–1058.
The geological evolution of the Tibetan Plateau.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVSitrfP&md5=704e07d34fd664a0393d5b42f416663bCAS |

Scudder, S. H. (1862). Materials for a monograph of the North American Orthoptera. Boston Journal of Natural History 7, 409–480.
Materials for a monograph of the North American Orthoptera.Crossref | GoogleScholarGoogle Scholar |

Smith, M. A., Fisher, B. L., and Hebert, P. D. N. (2005). DNA barcoding for effective biodiversity assessment of a hyperdiverse arthropod group: the ants of Madagascar. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 360, 1825–1834.
DNA barcoding for effective biodiversity assessment of a hyperdiverse arthropod group: the ants of Madagascar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlSjsrjP&md5=bf745a2e2546b1fec06d03885d5eb9a2CAS |

Spicer, R. A., Harris, N. B., Widdowson, M., Herman, A. B., Guo, S., Valdes, P. J., Wolfe, J. A., and Kelley, S. P. (2003). Constant elevation of southern Tibet over the past 15 million years. Nature 421, 622–624.
Constant elevation of southern Tibet over the past 15 million years.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovFKmsg%3D%3D&md5=3cce1476fd722dae5d2cd8a6e6822ea5CAS |

Stamatakis, A., Hoover, P., and Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57, 758–771.
A rapid bootstrap algorithm for the RAxML web servers.Crossref | GoogleScholarGoogle Scholar |

Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
MEGA6: Molecular Evolutionary Genetics Analysis version 6.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=213a455e206e1c198319858e32755a17CAS |

Wan, F. (2012). Geological and geomorphological evolution history of Changbai Mountain of Jilin Province. Jilin Geology 31, 21–23.

Wang, X., Zhang, L., and Fang, J. (2004). Geographical differences in alpine timberline and its climatic interpretation in China. Acta Geographica Sinica 59, 871–879.

Wang, Z. Q., Li, Y., Che, Y. L., and Wang, J. J. (2015). The wood-feeding genus Cryptocercus (Blattodea: Cryptocercidae), with description of two new species based on female genitalia. The Florida Entomologist 98, 260–271.
The wood-feeding genus Cryptocercus (Blattodea: Cryptocercidae), with description of two new species based on female genitalia.Crossref | GoogleScholarGoogle Scholar |

Ware, J. L., Litman, J., Klass, K. D., and Spearman, L. A. (2008). Relationships among the major lineages of Dictyoptera: the effect of outgroup selection on dictyopteran tree topology. Systematic Entomology 33, 429–450.
Relationships among the major lineages of Dictyoptera: the effect of outgroup selection on dictyopteran tree topology.Crossref | GoogleScholarGoogle Scholar |

Wei, H. Q., Wang, Y., Jin, J. Y., Gao, L., Yun, S. H., and Jin, B. (2007). Timescale and evolution of the intracontinental Tianchi volcanic shield and ignimbrite-forming eruption, Changbaishan, Northeast China. Lithos 96, 315–324.
| 1:CAS:528:DC%2BD2sXlsFehtLg%3D&md5=c5d049fbc95a45ed8aac434a90e31cf9CAS |

Wen, J., Zhang, J. Q., Nie, Z. L., Zhong, Y., and Sun, H. (2014). Evolutionary diversifications of plants on the Qinghai–Tibetan Plateau. Frontiers in Genetics 5, 4.
Evolutionary diversifications of plants on the Qinghai–Tibetan Plateau.Crossref | GoogleScholarGoogle Scholar |

Wu, Y., Colwell, R. K., Rahbek, C., Zhang, C., Quan, Q., Wang, C., Lei, F., and Burns, K. C. (2013). Explaining the species richness of birds along a subtropical elevational gradient in the Hengduan Mountains. Journal of Biogeography 40, 2310–2323.
Explaining the species richness of birds along a subtropical elevational gradient in the Hengduan Mountains.Crossref | GoogleScholarGoogle Scholar |

Yin, A., and Harrison, T. M. (2000). Geologic evolution of the Himalayan-Tibetan Orogen. Annual Review of Earth and Planetary Sciences 28, 211–280.
Geologic evolution of the Himalayan-Tibetan Orogen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsFOnt7s%3D&md5=103d50daa6250ecd28e73f3aa494003dCAS |