Volume 13 Issue 1
Mar.  2022
Turn off MathJax
Article Contents
Zheng Li, Jie Zhou, Minzhi Gao, Wei Liang, Lu Dong. 2022: Parapatric speciation with recurrent gene flow of two sexual dichromatic pheasants. Avian Research, 13(1): 100031. doi: 10.1016/j.avrs.2022.100031
Citation: Zheng Li, Jie Zhou, Minzhi Gao, Wei Liang, Lu Dong. 2022: Parapatric speciation with recurrent gene flow of two sexual dichromatic pheasants. Avian Research, 13(1): 100031. doi: 10.1016/j.avrs.2022.100031

Parapatric speciation with recurrent gene flow of two sexual dichromatic pheasants

doi: 10.1016/j.avrs.2022.100031
More Information
  • Corresponding author: E-mail address: donglu@bnu.edu.cn (L. Dong)
  • Received Date: 13 Mar 2022
  • Accepted Date: 12 Apr 2022
  • Available Online: 07 Jul 2022
  • Publish Date: 20 Apr 2022
  • Understanding speciation has long been a fundamental goal of evolutionary biology. It is widely accepted that speciation requires an interruption of gene flow to generate strong reproductive isolation between species. The mechanism of how speciation in sexually dichromatic species operates in the face of gene flow remains an open question. Two species in the genus Chrysolophus, the Golden Pheasant (C. pictus) and Lady Amherst's Pheasant (C. amherstiae), both of which exhibit significant plumage dichromatism, are currently parapatric in southwestern China with several hybrid recordings in field. In this study, we estimated the pattern of gene flow during the speciation of the two pheasants using the Approximate Bayesian Computation (ABC) method based on data from multiple genes. Using a newly assembled de novo genome of Lady Amherst's Pheasant and resequencing of widely distributed individuals, we reconstructed the demographic history of the two pheasants by the PSMC (pairwise sequentially Markovian coalescent) method. The results provide clear evidence that the gene flow between the two pheasants was consistent with the predictions of the isolation with migration model during divergence, indicating that there was long-term gene flow after the initial divergence (ca. 2.2 million years ago). The data further support the occurrence of secondary contact between the parapatric populations since around 30 kya with recurrent gene flow to the present, a pattern that may have been induced by the population expansion of the Golden Pheasant in the late Pleistocene. The results of the study support the scenario of speciation between the Golden Pheasant and Lady Amherst's Pheasant with cycles of mixing-isolation-mixing, possibly due to the dynamics of geographical context in the late Pleistocene. The two species provide a good research system as an evolutionary model for testing reinforcement selection in speciation.


  • loading
  • Anderson, E.C., Thompson, E.A., 2002. A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160, 1217-1229 doi: 10.1093/genetics/160.3.1217
    Arrieta, R.S., Lijtmaer, D.A., Tubaro, P.L., 2013. Evolution of postzygotic reproductive isolation in galliform birds: analysis of first and second hybrid generations and backcrosses. Biol. J. Linn. Soc. 110, 528-542 doi: 10.1111/bij.12153
    Beaumont, M.A., 2010. Approximate Bayesian computation in evolution and ecology. Annu. Rev. Ecol. Evol. Syst. 41, 379-406 doi: 10.1146/annurev-ecolsys-102209-144621
    Beaumont, M.A., Zhang, W., Balding, D.J., 2002. Approximate Bayesian computation in population genetics. Genetics 162, 2025-2035 doi: 10.1093/genetics/162.4.2025
    Beaumont, O., Bonichon, N., Duchon, P., Eyraud-Dubois, L., Larcheveque, H., 2008. A distributed algorithm for resource clustering in large scale platforms. In: Baker, T.P., Bui, A., Tixeuil, S. (Eds), Principles of Distributed Systems. OPODIS 2008. Lecture Notes in Computer Science, vol 5401. Springer, Berlin, pp. 564-567
    Bertorelle, G., Benazzo, A., Mona, S., 2010. ABC as a flexible framework to estimate demography over space and time: some cons, many pros. Mol. Ecol. 19, 2609-2625 doi: 10.1111/j.1365-294X.2010.04690.x
    Blum, M.G.B., Francois, O., 2010. Non-linear regression models for Approximate Bayesian Computation. Stat. Comput. 20, 63-73 doi: 10.1007/s11222-009-9116-0
    Bolnick, D.I., Fitzpatrick, B.M., 2007. Sympatric speciation: models and empirical evidence. Annu. Rev. Ecol. Evol. Syst. 38, 459-487 doi: 10.1146/annurev.ecolsys.38.091206.095804
    Butler, J., MacCallum, I., Kleber, M., Shlyakhter, I.A., Belmonte, M.K., Lander, E.S., et al., 2008. ALLPATHS: de novo assembly of whole-genome shotgun microreads. Genome Res. 18, 810-820 doi: 10.1101/gr.7337908
    Cornejo-Romero, A., Vargas-Mendoza, C.F., Aguilar-Martinez, G.F., Medina-Sanchez, J., Rendon-Aguilar, B., Valverde, P.L., et al., 2017. Alternative glacial-interglacial refugia demographic hypotheses tested on Cephalocereus columna-trajani (Cactaceae) in the intertropical Mexican drylands. PLoS ONE 12, e0175905 doi: 10.1371/journal.pone.0175905
    Coyne, J.A., Orr, H.A., 2004. Speciation. Sinauer Associates, Sunderland
    Csillery, K., Francois, O., Blum, M.G.B., 2012. Abc: an R package for approximate Bayesian computation (ABC). Method. Ecol. Evol. 3, 475-479 doi: 10.1111/j.2041-210X.2011.00179.x
    Darriba, D., Taboada, G.L., Doallo, R., Posada, D., 2012. JModelTest 2: more models, new heuristics and parallel computing. Nat. Method. 9, 772 doi: 10.1038/nmeth.2109
    Deng, Q.X., 1974. A natural hybrid of Chrysolophus amherstiae and C. picus. Curr. Zool. 20, 106-107. (in Chinese)
    Don, R.H., Cox, P.T., Wainwright, B.J., Baker, K., Mattick, J.S., 1991. “Touchdown” PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res. 19, 4008 doi: 10.1093/nar/19.14.4008
    Dong, F., Hung, C.M., Li, X.L., Gao, J.Y., Zhang, Q., Wu, F., et al., 2017. Ice age unfrozen: severe effect of the last interglacial, not glacial, climate change on East Asian avifauna. BMC Evol. Biol. 17, 244 doi: 10.1186/s12862-017-1100-2
    Dong, L., Heckel, G., Liang, W., Zhang, Y., 2013. Phylogeography of Silver Pheasant (Lophura nycthemera L.) across China: aggregate effects of refugia, introgression and riverine barriers. Mol. Ecol. 22, 3376-3390 doi: 10.1111/mec.12315
    Drummond, A.J., Suchard, M.A., Xie, D., Rambaut, A., 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969-1973 doi: 10.1093/molbev/mss075
    Duchen, P., Zivkovic, D., Hutter, S., Stephan, W., Laurent, S., 2013. Demographic inference reveals African and European admixture in the North American Drosophila melanogaster population. Genetics 193, 291-301 doi: 10.1534/genetics.112.145912
    Fraser, C.I., Nikula, R., Ruzzante, D.E., Waters, J.M., 2012. Poleward bound: biological impacts of southern Hemisphere glaciation. Trends Ecol. Evol. 27, 462-471 doi: 10.1016/j.tree.2012.04.011
    Funk, D.J., Nosil, P., Etges, W.J., 2006. Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proc. Natl. Acad. Sci. U. S. A. 103, 3209-3213 doi: 10.1073/pnas.0508653103
    He, J.L., Wei, L., 1993. Note on some natural hybrids of Chrysolophus amherstiae and C. picus from Dayi County, Sichuan. Zool. Res. 14, 239-240. (in Chinese)
    Hewitt, G., 2000. The genetic legacy of the quaternary ice ages. Nature 405, 907-913 doi: 10.1038/35016000
    Hewitt, G.M., 2001. Speciation, hybrid zones and phylogeography - or seeing genes in space and time. Mol. Ecol. 10, 537-549
    Hewitt, G.M., 2004. Genetic consequences of climatic oscillations in the Quaternary. Philos. T. Roy. Soc. B. 359, 183-195 doi: 10.1098/rstb.2003.1388
    Hudson, R.R., Kreitman, M., Aguade, M., 1987. A test of neutral molecular evolution based on nucleotide data. Genetics 116, 153-159 doi: 10.1093/genetics/116.1.153
    Jean-Marie, C., Filipe, S., Mark, A.B., Christian, P.R., Jean-Michel, M., David, J.B., et al., 2008. Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24, 2713-2719 doi: 10.1093/bioinformatics/btn514
    Kirkpatrick, M., Servedio, M.R., 1999. The reinforcement of mating preferences on an island. Genetics 151, 865-884 doi: 10.1093/genetics/151.2.865
    Lambeck, K., Chappell, J., 2001. Sea level change through the last glacial cycle. Science 292, 679-686 doi: 10.1126/science.1059549
    Lamichhaney, S., Berglund, J., Almen, M.S., Maqbool, K., Grabherr, M., Martinez-Barrio, A., et al., 2015. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518, 371-375 doi: 10.1038/nature14181
    Li, H., 2013. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:1303.3997v2 [q-bio.GN]
    Li, H., Durbin, R., 2011. Inference of human population history from individual whole-genome sequences. Nature 475, 493-496 doi: 10.1038/nature10231
    Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., et al., 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078-2079 doi: 10.1093/bioinformatics/btp352
    Li, J.W., Yeung, C.K.L., Tsai, P.W., Lin, R.C., Yeh, C.F., Yao, C.T., et al., 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. Mol. Ecol. 19, 494-507 doi: 10.1111/j.1365-294X.2009.04494.x
    Librado, P., Rozas, J., 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451-1452 doi: 10.1093/bioinformatics/btp187
    Liu, Y., Liu, S., Yeh, C.F., Zhang, N., Chen, G., Que, P., et al., 2018. The first set of universal nuclear protein-coding loci markers for avian phylogenetic and population genetic studies. Sci. Rep. 8, 15723 doi: 10.1038/s41598-018-33646-x
    Lyu, N., Packert, M., Tietze, D.T., Sun, Y.H., 2015. Uncommon paleodistribution patterns of Chrysolophus pheasants in east Asia: explanations and implications. J. Avian Biol. 46, 528-537 doi: 10.1111/jav.00590
    Mayr, E., 1942. Systematics and the Origin of Species from the Viewpoint of a Zoologist. Columbia University Press, New York
    Nosil, P., 2012. Ecological Speciation. Oxford University Press, Oxford
    Nosil, P., 2008. Speciation with gene flow could be common. Mol. Ecol. 17, 2103-2106 doi: 10.1111/j.1365-294X.2008.03715.x
    Olsen, J.B., Crane, P.A., Flannery, B.G., Dunmall, K., Templin, W.D., Wenburg, J.K., 2011. Comparative landscape genetic analysis of three Pacific salmon species from subarctic North America. Conserv. Genet. 12, 223-241 doi: 10.1007/s10592-010-0135-3
    Pavlidis, P., Laurent, S., Stephan, W., 2010. MsABC: a modification of Hudson’s ms to facilitate multi-locus ABC analysis. Mol. Ecol. Resour. 10, 723-727 doi: 10.1111/j.1755-0998.2010.02832.x
    Peng, M.S., Wu, F., Murphy, R.W., Yang, X.J., Zhang, Y.P., 2016. An ancient record of an avian hybrid and the potential uses of art in ecology and conservation. Ibis 158, 444-445 doi: 10.1111/ibi.12354
    Poelstra, J.W., Vijay, N., Bossu, C.M., Lantz, H., Ryll, B., Muller, I., et al., 2014. The genomic landscape underlying phenotypic integrity in the face of gene flow in crows. Science 344, 1410-1414 doi: 10.1126/science.1253226
    Provan, J., Bennett, K.D., 2008. Phylogeographic insights into cryptic glacial refugia. Trends Ecol. Evol. 23, 564-571 doi: 10.1016/j.tree.2008.06.010
    Rambaut, A., Drummond, A.J., 2009. Tracer v 1.5. http://beast.bio.ed.ac.uk/Tracer
    R Core Team, 2020. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. URL https://www.R-project.org/
    Rice, W.R., Salt, G.W., 1988. Speciation via disruptive selection on habitat preference: experimental evidence. Am. Nat. 131, 911-917 doi: 10.1086/284831
    Rohling, E.J., Fenton, M., Jorissen, F.J., Bertrand, P., Ganssen, G., Caulet, J.P., 1998. Magnitudes of sea-level lowstands of the past 500,000 years. Nature 394, 162-165 doi: 10.1038/28134
    Servedio, M.R., 2000. Reinforcement and the genetics of nonrandom mating. Evolution 54, 21-29 doi: 10.1111/j.0014-3820.2000.tb00003.x
    Servedio, M.R., 2004. The what and why of research on reinforcement. PLoS Biol. 2, e420 doi: 10.1371/journal.pbio.0020420
    Servedio, M.R., 2011. Limits to the evolution of assortative mating by female choice under restricted gene flow. P. Roy. Soc. B. Biol. Sci. 278, 179-187 doi: 10.1098/rspb.2010.1174
    Servedio, M.R., 2012. The relationship between sexual selection and speciation. Curr. Zool. 58, 413-415 doi: 10.1093/czoolo/58.3.413
    Servedio, M.R., 2016. Geography, assortative mating, and the effects of sexual selection on speciation with gene flow. Evol. Appl. 9, 91-102 doi: 10.1111/eva.12296
    Servedio, M.R., Burger, R., 2014. The counterintuitive role of sexual selection in species maintenance and speciation. Proc. Natl. Acad. Sci. U. S. A. 111, 8113-8118 doi: 10.1073/pnas.1316484111
    Servedio, M.R., Kirkpatrick, M., 1997. The effects of gene flow on reinforcement. Evolution 51, 1764-1772 doi: 10.1111/j.1558-5646.1997.tb05100.x
    Servedio, M.R., Noor, M.A.F., 2003. The role of reinforcement in speciation: theory and data. Annu. Rev. Ecol. Evol. Syst. 34, 339-364 doi: 10.1146/annurev.ecolsys.34.011802.132412
    Shafer, A.B.A., Cullingham, C.I., Cote, S.D., Coltman, D.W., 2010. Of glaciers and refugia: A decade of study sheds new light on the phylogeography of northwestern North America. Mol. Ecol. 19, 4589-4621 doi: 10.1111/j.1365-294X.2010.04828.x
    Shi, X.Y., Fu, Q., Wang, L., Jiang, Z.Y., Shi, X.G., Li, S., 2018. Note on the natural hybridization of Golden Pheasant (Chrysolophus pictus) and Lady Amherst’s Pheasant (C. amherstiae) in Anzihe Nature Reserve, Sichuan Province. Chinese J Zool. 53, 660-663. (in Chinese)
    Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585-595 doi: 10.1093/genetics/123.3.585
    Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729 doi: 10.1093/molbev/mst197
    Thompson, J.D., Higgins, D.G., Gibson, T.J., 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680 doi: 10.1093/nar/22.22.4673
    Wang, P., Liu, Y., Liu, Y., Chang, Y., Wang, N., Zhang, Z., 2017. The role of niche divergence and geographic arrangement in the speciation of Eared Pheasants (Crossoptilon, Hodgson 1938). Mol. Phylogenet. Evol. 113, 1-8 doi: 10.1016/j.ympev.2017.05.003
    Wang, P., Yeh, C., Chang, J., Yao, H., Fu, Y., Yao, C., et al., 2021. Multilocus phylogeography and ecological niche modeling suggest speciation with gene flow between the two Bamboo Partridges. Avian Res. 12, 17 doi: 10.1167/iovs.62.14.17
    Wang, W., Dai, C., Alstrom, P., Zhang, C., Qu, Y., Li, S.H., et al., 2014. Past hybridization between two East Asian long-tailed tits (Aegithalos bonvaloti and A. fuliginosus). Front. Zool. 11, 40 doi: 10.1186/1742-9994-11-40
    Wasserman, T.N., Cushman, S.A., Schwartz, M.K., Wallin, D.O., 2010. Spatial scaling and multi-model inference in landscape genetics: martes americana in northern Idaho. Landscape Ecol. 25, 1601-1612 doi: 10.1007/s10980-010-9525-7
    Wei, C., Dong, L., Li, S.H., Alstrom, P., Liu, Y., Xia, C., et al., 2019. From the Himalayas to a continental Island: Integrative species delimitation in the Brownish-flanked Bush Warbler Horornis fortipes complex. Mol. Phylogenet. Evol. 131, 219-227 doi: 10.1016/j.ympev.2018.10.009
    Zhang, D., Tang, L., Cheng, Y., Hao, Y., Xiong, Y., Song, G., et al., 2019. “Ghost Introgression” as a cause of deep mitochondrial divergence in a bird species complex. Mol. Biol. Evol. 36, 2375-2386 doi: 10.1093/molbev/msz170
    Zhang, G., Li, C., Li, Q., Li, B., Larkin, D.M., Lee, C., et al., 2014. Comparative genomics reveals insights into avian genome evolution and adaptation. Science 346, 1311-1320 doi: 10.1126/science.1251385
    Zhou, S.Z., Jijun, L., Zhang, S.Q., Zhao, J.D., Cui, J.X., 2004. Quaternary glaciations in China. Dev. Quat. Sci. 2, 105-113
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(3)  / Tables(1)

    Article Metrics

    Article views (48) PDF downloads(2) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint