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Xiu-Qin Lin, Yin-Meng Hou, Wei-Zhao Yang, Sheng-Chao Shi, Pu-Yang Zheng, Chung-Kun Shih, Jian-Ping Jiang, Feng Xie. A wide hybrid zone mediated by precipitation contributed to confused geographical structure of Scutiger boulengeri. Zoological Research, 2023, 44(1): 3-19. doi: 10.24272/j.issn.2095-8137.2022.108
Citation: Xiu-Qin Lin, Yin-Meng Hou, Wei-Zhao Yang, Sheng-Chao Shi, Pu-Yang Zheng, Chung-Kun Shih, Jian-Ping Jiang, Feng Xie. A wide hybrid zone mediated by precipitation contributed to confused geographical structure of Scutiger boulengeri. Zoological Research, 2023, 44(1): 3-19. doi: 10.24272/j.issn.2095-8137.2022.108

A wide hybrid zone mediated by precipitation contributed to confused geographical structure of Scutiger boulengeri

doi: 10.24272/j.issn.2095-8137.2022.108
Funds:  This study was supported by the Second Tibetan Plateau Scientific Expedition and Research Program (STEP, 2019QZKK05010503), Biodiversity Survey and Assessment Project of the Ministry of Ecology and Environment, China (2019HJ2096001006), Construction of Basic Conditions Platform of Sichuan Science and Technology Department (2019JDPT0020), and China Biodiversity Observation Networks (Sino BON)
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  • Corresponding author: E-mail: xiefeng@cib.ac.cn
  • Received Date: 2022-06-07
  • Accepted Date: 2022-09-19
  • Published Online: 2022-09-20
  • Confused geographical structure of a population and mitonuclear discordance are shaped by a combination of rapid changes in population demographics and shifts in ecology. In this study, we generated a time-calibrated phylogeny of Scutiger boulengeri, an endemic Xizang alpine toad occurring in mountain streams on the Qinghai-Xizang (Tibet) Plateau (QTP). Based on three mitochondrial DNA (mtDNA) genes, eight clades were assigned to three deeply divergent lineages. Analysis of nuclear DNA (nuDNA) genes revealed three distinct clusters without geographic structure, indicating significantly high rates of gene flow. Coalescent theory framework analysis (approximate Bayesian computation model DIYABC and Migrate-N) suggested that divergence of the main intraspecific clusters was the result of hybridization after secondary contact in the Holocene around 0.59 million years ago (Ma). The ratio of mtDNA FST (fixation index) to nuDNA FST was 2.3, thus failing to show male-biased dispersal. Geographic cline analysis showed that a wide hybrid zone was initially established in southwestern China, without significant reproductive isolation but with strong introgression in S. boulengeri, suggesting high hybrid fitness. Furthermore, mtDNA genes exhibited isolation by distance (IBD) while nuDNA genes exhibited significant isolation by environment (IBE). Results suggested that mitonuclear discordance may have initially been caused by geographic isolation, followed by precipitation-mediated hybridization, producing a wide hybrid zone and geographic structure confusion of nuDNA genes in S. boulengeri. This study indicated that complicated historical processes may have led to specific genetic patterns, with a specific climate factor facilitating gene flow in the system.
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  • [1]
    Auguie B, Antonov A. 2017. Miscellaneous functions for "Grid" graphics (Version 2.3). https://cran.r-project.org/web/packages/gridExtra/gridExtra.pdf.
    Banta J. 2020. How to convert a FASTA file to a STRUCTURE file [Video]. YouTube.https://www.youtube.com/watch?v=EO6AtZPgz1g.
    Barton NH, Hewitt GM. 1985. Analysis of hybrid zones. Annual Review of Ecology and Systematics, 16: 113−148. doi: 10.1146/annurev.es.16.110185.000553
    Barton NH, Hewitt GM. 1989. Adaptation, speciation and hybrid zones. Nature, 341(6242): 497−503. doi: 10.1038/341497a0
    Beerli P, Mashayekhi S, Sadeghi M, Khodaei M, Shaw K. 2019. Population genetic inference with MIGRATE. Current Protocols in Bioinformatics, 68(1): e87.
    Blanquart F, Gandon S, Nuismer SL. 2012. The effects of migration and drift on local adaptation to a heterogeneous environment. Journal of Evolutionary Biology, 25(7): 1351−1363. doi: 10.1111/j.1420-9101.2012.02524.x
    Boaratti AZ, Da Silva FR. 2015. Relationships between environmental gradients and geographic variation in the intraspecific body size of three species of frogs (Anura). Austral Ecology, 40(8): 869−876. doi: 10.1111/aec.12267
    Bohonak AJ. 1999. Dispersal, gene flow, and population structure. The Quarterly Review of Biology, 74(1): 21−45. doi: 10.1086/392950
    Bonnet E, Van de Peer Y. 2002. zt: a sofware tool for simple and partial mantel tests. Journal of Statistical Software, 7(10): 1−12.
    Broquet T, Petit EJ. 2009. Molecular estimation of dispersal for ecology and population genetics. Annual Review of Ecology, Evolution, and Systematics, 40: 193−216. doi: 10.1146/annurev.ecolsys.110308.120324
    Bruen TC, Philippe H, Bryant D. 2006. A simple and robust statistical test for detecting the presence of recombination. Genetics, 172(4): 2665−2681. doi: 10.1534/genetics.105.048975
    Brumfield RT, Jernigan RW, Mcdonald DB, Braun MJ. 2001. Evolutionary implications of divergent clines in an avian (Manacus: Aves) hybrid zone. Evolution, 55(10): 2070−2087. doi: 10.1111/j.0014-3820.2001.tb01322.x
    Bryant D, Moulton V. 2004. Neighbor-Net: an agglomerative method for the construction of phylogenetic networks. Molecular Biology and Evolution, 21(2): 255−265.
    Buggs RJA. 2007. Empirical study of hybrid zone movement. Heredity, 99(3): 301−312. doi: 10.1038/sj.hdy.6800997
    Chen W, Bi K, Fu JZ. 2009. Frequent mitochondrial gene introgression among high elevation Tibetan megophryid frogs revealed by conflicting gene genealogies. Molecular Ecology, 18(13): 2856−2876. doi: 10.1111/j.1365-294X.2009.04258.x
    Cornuet JM, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M, Leblois R, et al. 2014. DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics, 30(8): 1187−1189. doi: 10.1093/bioinformatics/btt763
    Cornuet JM, Santos F, Beaumont MA, Robert CP, Marin JM, Balding DJ, et al. 2008. Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics, 24(23): 2713−2719. doi: 10.1093/bioinformatics/btn514
    Crease TJ, Lynch M, Spitze K. 1990. Hierarchical analysis of population genetic variation in mitochondrial and nuclear genes of Daphnia pulex. Molecular Biology and Evolution, 7(5): 444–458.
    Derryberry EP, Derryberry GE, Maley JM, Brumfield RT. 2014. HZAR: hybrid zone analysis using an R software package. Molecular Ecology Resources, 14(3): 652−663. doi: 10.1111/1755-0998.12209
    Després L. 2019. One, two or more species? Mitonuclear discordance and species delimitation. Molecular Ecology, 28(17): 3845−3847. doi: 10.1111/mec.15211
    Drummond AJ, Suchard MA, Xie D, Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29(8): 1969−1973. doi: 10.1093/molbev/mss075
    Dufresnes C, Pribille M, Alard B, Gonçalves H, Amat F, Crochet PA, et al. 2020. Integrating hybrid zone analyses in species delimitation: lessons from two anuran radiations of the Western Mediterranean. Heredity, 124(3): 423−438. doi: 10.1038/s41437-020-0294-z
    Edwards S, Bensch S. 2009. Looking forwards or looking backwards in avian phylogeography? A comment on Zink and Barrowclough 2008. Molecular Ecology, 18(14): 2930−2933. doi: 10.1111/j.1365-294X.2009.04270.x
    Evanno G, Regnaut S, Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14(8): 2611−2620. doi: 10.1111/j.1365-294X.2005.02553.x
    Everson KM, Gray LN, Jones AG, Lawrence NM, Foley ME, Sovacool KL, et al. 2021. Geography is more important than life history in the recent diversification of the tiger salamander complex. Proceedings of the National Academy of Sciences of the United States of America, 118(17): e2014719118. doi: 10.1073/pnas.2014719118
    Excoffier L, Foll M, Petit RJ. 2009. Genetic consequences of range expansions. Annual Review of Ecology, Evolution, and Systematics, 40: 481−501. doi: 10.1146/annurev.ecolsys.39.110707.173414
    Fei L, Ye CY, Huang YZ, Jiang JP, Xie F. 2005. Chapter 2: taxonomic terms and metrics of amphibians. In: An Illustrated key to Chinese Amphibians. Sichuan Publishing House of Science and Technology, 3–5. (in Chinese)
    Fick SE, Hijmans RJ. 2017. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37(12): 4302−4315. doi: 10.1002/joc.5086
    Francis RM. 2017. POPHELPER: an R package and web app to analyse and visualize population structure. Molecular Ecology Resources, 17(1): 27−32. doi: 10.1111/1755-0998.12509
    Funk DJ, Omland KE. 2003. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution, and Systematics, 34: 397−423. doi: 10.1146/annurev.ecolsys.34.011802.132421
    García-Girón J, García P, Fernández-Aláez M, Bécares E, Fernández-Aláez C. 2019. Bridging population genetics and the metacommunity perspective to unravel the biogeographic processes shaping genetic differentiation of Myriophyllum alterniflorum DC. Scientific Reports, 9(1): 18097. doi: 10.1038/s41598-019-54725-7
    Han WX, Fang XM, Ye CC, Teng XH, Zhang T. 2014. Tibet forcing Quaternary stepwise enhancement of westerly jet and central Asian aridification: carbonate isotope records from deep drilling in the Qaidam salt playa, NE Tibet. Global and Planetary Change, 116: 68−75. doi: 10.1016/j.gloplacha.2014.02.006
    Head MJ, Gibbard PL. 2015. Early–Middle Pleistocene transitions: linking terrestrial and marine realms. Quaternary International, 389: 7−46. doi: 10.1016/j.quaint.2015.09.042
    Hewitt GM. 1988. Hybrid zones-natural laboratories for evolutionary studies. Trends in Ecology & Evolution, 3(7): 158−167.
    Hijmans RJ, Karney C, Williams E, Vennes C. 2021. Geosphere: spherical trigonometry.https://rdrr.io/cran/geosphere/.
    Hofmann S, Stöck M, Zheng YC, Ficetola FG, Li JT, Scheidt U, et al. 2017. Molecular phylogenies indicate a Paleo-Tibetan origin of himalayan lazy toads (Scutiger). Scientific Reports, 7(1): 3308. doi: 10.1038/s41598-017-03395-4
    Hudson RR, Turelli M. 2003. Stochasticity overrules the “three-times rule”: genetic drift, genetic draft, and coalescence times for nuclear loci versus mitochondrial DNA. Evolution, 57(1): 182−190.
    Huson DH, Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23(2): 254−267. doi: 10.1093/molbev/msj030
    Huson DH, Bryant D. 2008. User manual for SplitsTree4 V4.10. http://nebc.nerc.ac.uk/bioinformatics/documentation/splitstree/manual.pdf.
    Huson DH, Kloepper TH. 2005. Computing recombination networks from binary sequences. Bioinformatics, 21(S2): ii159−ii165.
    Jiang FC, Wu XH. 1998. Late cenozoic tectonic movement in geomorphologic boundary belt of southeastern Qinghai-Xizang Plateau. Journal of Chengdu University of Technology, 25(2): 162−168. (in Chinese)
    Jombart T, Collins C. 2015. A tutorial for discriminant analysis of principal components (DAPC) using adegenet 2.0. 0.https://adegenet.r-forge.r-project.org/files/tutorial-dapc.pdf.
    Jombart T, Devillard S, Balloux F. 2010. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics, 11: 94.
    Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14(6): 587−589. doi: 10.1038/nmeth.4285
    Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: molecular evolutionary genetics Analysis across computing platforms. Molecular Biology and Evolution, 35(6): 1547−1549. doi: 10.1093/molbev/msy096
    Larson EL, White TA, Ross CL, Harrison RG. 2014. Gene flow and the maintenance of species boundaries. Molecular Ecology, 23(7): 1668−1678. doi: 10.1111/mec.12601
    Legendre P, Fortin MJ. 2010. Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data. Molecular Ecology Resources, 10(5): 831−844. doi: 10.1111/j.1755-0998.2010.02866.x
    Li R, Chen W, Tu LH, Fu JZ. 2009. Rivers as barriers for high elevation amphibians: a phylogeographic analysis of the alpine stream frog of the Hengduan Mountains. Journal of Zoology, 277(4): 309−316. doi: 10.1111/j.1469-7998.2008.00543.x
    Lin XQ, Shih CK, Hou YM, Shu XX, Zhang MH, Hu JH, et al. 2021. Climatic-niche evolution with key morphological innovations across clades within Scutiger boulengeri (Anura: Megophryidae). Ecology and Evolution, 11(15): 10353−10368. doi: 10.1002/ece3.7838
    López-Uribe MM, Jha S, Soro A. 2019. A trait-based approach to predict population genetic structure in bees. Molecular Ecology, 28(8): 1919−1929. doi: 10.1111/mec.15028
    Major EI, Höhn M, Avanzi C, Fady B, Heer K, Opgenoorth L, et al. 2021. Fine-scale spatial genetic structure across the species range reflects recent colonization of high elevation habitats in silver fir (Abies alba Mill. ). Molecular Ecology, 30(20): 5247−5265. doi: 10.1111/mec.16107
    Marko PB, Hart MW. 2011. The complex analytical landscape of gene flow inference. Trends in Ecology & Evolution, 26(9): 448−456.
    McQuillan MA, Rice AM. 2015. Differential effects of climate and species interactions on range limits at a hybrid zone: potential direct and indirect impacts of climate change. Ecology and Evolution, 5(21): 5120−5137. doi: 10.1002/ece3.1774
    Medina R, Wogan GOU, Bi K, Termignoni-García F, Bernal MH, Jaramillo-Correa JP, et al. 2021. Phenotypic and genomic diversification with isolation by environment along elevational gradients in a neotropical treefrog. Molecular Ecology, 30(16): 4062−4076. doi: 10.1111/mec.16035
    Menon M, Bagley JC, Friedline CJ, Whipple AV, Schoettle AW, Leal-Sàenz A, et al. 2018. The role of hybridization during ecological divergence of southwestern white pine (Pinus strobiformis) and limber pine (P. flexilis). Molecular Ecology, 27(5): 1245−1260. doi: 10.1111/mec.14505
    Ottaviani D, Cairns SC, Oliverio M, Boitani L. 2006. Body mass as a predictive variable of home-range size among Italian mammals and birds. Journal of Zoology, 269(3): 317−330. doi: 10.1111/j.1469-7998.2006.00060.x
    Parins-Fukuchi C, Stull GW, Smith SA. 2021. Phylogenomic conflict coincides with rapid morphological innovation. Proceedings of the National Academy of Sciences of the United States of America, 118(19): e2023058118. doi: 10.1073/pnas.2023058118
    Pereira RJ, Singhal S. 2022. A lizard with two tales: what diversification within Sceloporus occidentalis teaches us about species formation. Molecular Ecology, 31(2): 407−410. doi: 10.1111/mec.16321
    Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics, 155(2): 945−959. doi: 10.1093/genetics/155.2.945
    Prugnolle F, de Meeus T. 2002. Inferring sex-biased dispersal from population genetic tools: a review. Heredity, 88(3): 161−165. doi: 10.1038/sj.hdy.6800060
    Rambaut A, Drummond A. 2012. FigTree v1.4. Molecular evolution, phylogenetics and epidemiology. http://tree.bio.ed.ac.uk/software/figtree/.
    Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67(5): 901−904. doi: 10.1093/sysbio/syy032
    Sexton JP, Hangartner SB, Hoffmann AA. 2014. Genetic isolation by environment or distance: which pattern of gene flow is most common?. Evolution, 68(1): 1−15. doi: 10.1111/evo.12258
    Shen XX, Liang D, Feng YJ, Chen MY, Zhang P. 2013. A versatile and highly efficient toolkit including 102 nuclear markers for vertebrate phylogenomics, tested by resolving the higher level relationships of the caudata. Molecular Biology and Evolution, 30(10): 2235−2248. doi: 10.1093/molbev/mst122
    Shu XX, Hou YM, Cheng MY, Shu GC, Lin XQ, Wang B, et al. 2022. Rapid genetic divergence and mitonuclear discordance in the Taliang knobby newt (Liangshantriton taliangensis, Salamandridae, Caudata) and their driving forces. Zoological Research, 43(1): 129−146. doi: 10.24272/j.issn.2095-8137.2021.299
    Song ZM, Huang DM, Chang C. 1990. On the development and population age structure of Scutiger boulengeri tadpoles. Acta Zoologica Sinica, 36(2): 187−193. (in Chinese)
    Stevens VM, Trochet A, Blanchet S, Moulherat S, Clobert J, Baguette M. 2013. Dispersal syndromes and the use of life-histories to predict dispersal. Evolutionary Applications, 6(4): 630−642. doi: 10.1111/eva.12049
    Szymura JM, Barton NH. 1991. The genetic structure of the hybrid zone between the fire-bellied toads Bombina Bombina and B. Variegata: comparisons between transects and between loci. Evolution, 45(2): 237−261.
    Taylor SA, Larson EL, Harrison RG. 2015. Hybrid zones: windows on climate change. Trends in Ecology & Evolution, 30(7): 398−406.
    Toews DPL, Brelsford A. 2012. The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology, 21(16): 3907−3930. doi: 10.1111/j.1365-294X.2012.05664.x
    Tsuda Y, Nakao K, Ide Y, Tsumura Y. 2015. The population demography of Betula maximowicziana, a cool-temperate tree species in Japan, in relation to the last glacial period: its admixture-like genetic structure is the result of simple population splitting not admixing. Molecular Ecology, 24(7): 1403−1418. doi: 10.1111/mec.13123
    Twyford AD, Wong ELY, Friedman J. 2020. Multi-level patterns of genetic structure and isolation by distance in the widespread plant Mimulus guttatus. Heredity, 125(4): 227–239.
    Urquhart J, Wang YZ, Fu JZ. 2009. Historical vicariance and male-mediated gene flow in the toad-headed lizards Phrynocephalus przewalskii. Molecular Ecology, 18(17): 3714–3729.
    Valenzuela-Sánchez A, Cunningham AA, Soto-Azat C. 2015. Geographic body size variation in ectotherms: effects of seasonality on an anuran from the southern temperate forest. Frontiers in Zoology, 12: 37. doi: 10.1186/s12983-015-0132-y
    Wang IJ. 2013. Examining the full effects of landscape heterogeneity on spatial genetic variation: a multiple matrix regression approach for quantifying geographic and ecological isolation. Evolution, 67(12): 3403−3411. doi: 10.1111/evo.12134
    Wang K, Lenstra JA, Liu L, Hu QJ, Ma T, Qiu Q, et al. 2018. Incomplete lineage sorting rather than hybridization explains the inconsistent phylogeny of the wisent. Communications Biology, 1(1): 169. doi: 10.1038/s42003-018-0176-6
    Wen GN, Fu JZ. 2021. Isolation and reconnection: demographic history and multiple contact zones of the green odorous frog (Odorrana margaretae) around the Sichuan Basin. Molecular Ecology, 30(16): 4103−4117. doi: 10.1111/mec.16021
    Wilson GA, Rannala B. 2003. Bayesian inference of recent migration rates using multilocus genotypes. Genetics, 163(3): 1177−1191. doi: 10.1093/genetics/163.3.1177
    Xing YW, Ree RH. 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(17): E3444−E3451.
    Yang WZ, Feiner N, Pinho C, While GM, Kaliontzopoulou A, Harris DJ, et al. 2021. Extensive introgression and mosaic genomes of Mediterranean endemic lizards. Nature Communications, 12(1): 2762. doi: 10.1038/s41467-021-22949-9
    Zhang D, Gao FL, Jakovlić I, Zou H, Zhang J, Li WX, et al. 2020. PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecology Resources, 20(1): 348−355. doi: 10.1111/1755-0998.13096
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