Biodiversity Science ›› 2014, Vol. 22 ›› Issue (1): 88-96.doi: 10.3724/SP.J.1003.2014.13143

Special Issue: From Genome to Diversity

• Orginal Article • Previous Article     Next Article

A review on studies of speciation in the presence of gene flow: evolution of reproductive isolation

Zhonghu Li1, 2, *(), Zhanlin Liu2, Mali Wang2, Zengqiang Qian3, Peng Zhao2, Juan Zhu2, Yixin Yang2, Xiaohao Yan2, Yinjun Li2, Guifang Zhao2, *()   

  1. 1. Key Laboratory of Protection and Utilization of Biological Resources in Tarim Basin, Xinjiang Production & Construction Corps, Alaer, Xinjiang 843300
    2. Key Laboratory of Resource Biology and Biotechnology in Western China, Ministry of Education, College of Life Sciences, Northwest University, Xi’an 710069
    3. College of Life Sciences, Shaanxi Normal University, Xi’an 710119
  • Received:2013-06-22 Accepted:2014-01-22 Online:2014-02-10
  • Li Zhonghu,Zhao Guifang;

Speciation has long been a core issue in evolutionary biology and is of fundamental importance to the formation of biodiversity. The traditional view of allopatric speciation holds that geographic isolation is a major driver of speciation and that species divergence only occurs in circumstances where there is geographic isolation between populations. In recent years, with the development of population genomics and the advance of coalescent-based analytical methods, speciation with gene flow has become a topic of major interest in the field of evolutionary biology research. Does gene flow occur during the process of speciation? How does it affect species divergence? What are the reproductive isolation underlying the speciation in the presence of gene flow? All these questions are foci of attention in current speciation research. In this paper, we review the distribution patterns of temporal and spatial gene flow, and elucidate the effects of gene flow on speciation and the evolution of reproductive isolation. We conclude that speciation with gene flow could be common in nature.

Key words: gene flow, speciation, reproductive isolation, natural selection, divergent selection

[1] Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, Boughman J, Brelsford A, Buerkle CA, Buggs R, Butlin RK, Dieckmann U, Eroukhmanoff F, Grill A, Cahan SH, Hermansen JS, Hewitt G, Hudson AG, Jiggins C, Jones J, Keller B, Marczewski T, Mallet J, Martinez-Rodriguez P, Möst M, Mullen S, Nichols R, Nolte AW, Parisod C, Pfennig K, Rice AM, Ritchie MG, Seifert B, Smadja CM, Stelkens R, Szymura JM, Väinölä R, Wolf JBW, Zinner D (2013) Hybridization and speciation.Journal of Evolutionary Biology, 26, 229-246.
[2] Barton N, Bengtsson BO (1986) The barrier to genetic exchange between hybridising populations.Heredity, 57, 357-376.
[3] Bayes JJ, Malik HS (2009) Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science, 326, 1538-1541.
[4] Becquet C, Przeworski M (2007) A new approach to estimate parameters of speciation models with application to apes.Genome Research, 17, 1505-1519.
[5] Becquet C, Przeworski M (2009) Learning about modes of speciation by computational approaches.Evolution, 63, 2547-2562.
[6] Bell MA, Travis MP (2005) Hybridization, transgressive segregation, genetic covariation, and adaptive radiation.Trends in Ecology and Evolution, 20, 358-361.
[7] Bolnick DI, Fitzpatrick BM (2007) Sympatric speciation: models and empirical evidence. Annual Review of Ecology, Evolution, and Systematics, 38, 459-487.
[8] Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events.Nature, 422, 433-438.
[9] Brown WL, Wilson EO (1956) Character displacement.Systematic Zoology, 5, 49-64.
[10] Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland, MA.
[11] Darwin CR (1859) The Origin of Species, 6th edn. John Murray, London.
[12] Du FK, Petit RJ, Liu JQ (2009) More introgression with less gene flow: chloroplast vs. mitochondrial DNA in the Picea asperata complex in China, and comparison with other conifers.Molecular Ecology, 18, 1396-1407.
[13] Elias M, Faria R, Gompert Z, Hendry A (2012) Factors in?uencing progress toward ecological speciation.International Journal of Ecology, (2012), 1-7.
[14] Feder JL, Egan SP, Nosil P (2012) The genomics of speciation-with-gene-flow.Trends in Genetics, 28, 342-350.
[15] Flaxman SM, Feder JL, Nosil P (2013) Genetic hitchhiking and the dynamic buildup of genomic divergence during speciation with gene flow.Evolution, 67, 2577-2591.
[16] Gavrilets S (2004) Fitness Landscapes and the Origin of Species. Princeton University Press, Princeton, NJ.
[17] Grant PR, Grant BR, Petren K (2005) Hybridization in the recent past.The American Naturalist, 166, 56-67.
[18] Garant D, Forde SE, Hendry AP (2007) The multifarious effects of dispersal and gene flow on contemporary adaptation.Functional Ecology, 21, 434-443.
[19] Hey J (2006) Recent advances in assessing gene flow between diverging populations and species.Current Opinion in Genetics and Development, 16, 592-596.
[20] Hey J (2010a) Isolation with migration models for more than two populations.Molecular Biology and Evolution, 27, 905-920.
[21] 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.
[22] Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics.Proceedings of the National Academy of Sciences,USA, 104, 2785-2790.
[23] Knowlton N (1993) Sibling species in the sea.Annual Review of Ecology and Systematics, 24, 189-216.
[24] Leal M, Fleishman LJ (2004) Differences in visual signal design and detectability between allopatric populations of Anolis lizards.The American Naturalist, 163, 26-39.
[25] Lee YH, Lin CP (2012) Pleistocene speciation with and without gene flow in Euphaea damselflies of subtropical and tropical East Asian islands. Molecular Ecology, 21, 3739-3756.
[26] Levin DA, Francisco-Ortega J, Jansen RK (1996) Hybridization and the extinction of rare plant species.Conservation Biology, 10, 10-16.
[27] Li JW, Yeung CKL, Tsai PW, Lin RC, Yeh CF, Yao CT, Han LX, Hung LM, Ding P, Wang QS, Li SH (2010) Rejecting strictly allopatric speciation on a continental island: prolonged postdivergence gene ?ow between Taiwan (Leucodioptron taewanus, Passeriformes Timaliidae) and Chinese (L. canorum canorum) hwameis.Molecular Ecology, 19, 494-507.
[28] Li ZH, Zou JB, Mao KS, Lin K, Li HP, Liu JQ, Källman T, Lascoux M (2012) Population genetic evidence for complex evolutionary histories of four high altitude Juniper species in the Qinghai-Tibetan Plateau.Evolution, 66, 831-845.
[29] Mallet J (2007) Hybrid speciation.Nature, 446, 279-283.
[30] Matute DR (2012) Reinforcement of gametic isolation in Drosophila.PLoS Biology, 8, e1000341.
[31] Mayr E (1942) Systematics and the Origin of Species. Columbia University Press,New York.
[32] Mayr E (1963) Animal Species and Evolution,pp, 235-240. Belknap Press, Cambridge.
[33] Mayr E (1970) Populations, Species, and Evolution. Belknap Press, Massachusetts.
[34] McKinnon JS, Mori S, Blackman BK, David L, Kingsley DM, Jamieson L, Chou J, Schluter D (2004) Evidence for ecology’s role in speciation.Nature, 429, 294-298.
[35] Mendelson TC (2003) Sexual isolation evolves faster than hybrid inviability in a diverse and sexually dimorphic genus of fish (Percidae: Etheostoma).Evolution, 57, 317-327.
[36] Michel AP, Sim S, Powell THQ Taylor MS, Nosil P, Feder JL (2010) Widespread genomic divergence during sympatric speciation.Proceedings of the National Academy of Sciences, USA, 107, 9724-9729.
[37] Nadachowska K, Babik W (2009) Divergence in the face of gene flow: the case of two newts (Amphibia: Salamandridae).Molecular Biology and Evolution, 26, 829-841.
[38] Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment.Trends in Ecology and Evolution, 15, 278-285.
[39] Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach.Genetics, 158, 885-896.
[40] Niemiller ML, Fitzpatrick BM, Miller BT (2008) Recent divergence with gene ?ow in Tennessee cave salamanders (Plethodontidae, Gyrinophilus) inferred from gene genealogies.Molecular Ecology, 17, 2258-2275.
[41] Nosil P (2008) Speciation with gene flow could be common.Molecular Ecology, 17, 2103-2106.
[42] Nosil P, Funk DJ, Ortiz-Barrientos D (2009) Divergent selection and heterogeneous genomic divergence.Molecular Ecology, 18, 375-402.
[43] Nosil P, Gompert Z, Farkas TE, Comeault AA, Feder JL, Buerkle CA, Parchman TL (2012) Genomic consequences of multiple speciation processes in a stick insect.Proceedings of the Royal Society B: Biological Sciences, 279, 5058-5065.
[44] Nosil P, Schluter D (2011) The genes underlying the process of speciation.Trends in Ecology and Evolution, 26, 160-167.
[45] Ohshima I (2010) Host-associated pre-mating reproductive isolation between host races of Acrocercops transecta: mating site preferences and effect of host presence on mating.Ecological Entomology, 35, 253-257.
[46] Panova M, Hollander J, Johannesson K (2006) Site-specific genetic divergence in parallel hybrid zones suggests non-allopatric evolution of reproductive barriers.Molecular Ecology, 15, 4021-4031.
[47] Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations.Molecular Ecology, 14, 689-701.
[48] Rice WR, Hostert EE (1993) Laboratory experiments on speciation: what have we learned in 40 years.Evolution, 47, 1637-1653.
[49] Roux C, Castric V, Pauwels M, Wright SI, Saumitou-Laprade P, Vekemans X (2011) Does speciation between Arabidopsis halleri and Arabidopsis lyrata coincide with major changes in a molecular target of adaptation? PLoS ONE, 6, e26872.
[50] Rundle HD, Nosil P (2005) Ecological speciation.Ecology Letters, 8, 336-352.
[51] Schartl M (2008) Evolution of Xmrk: an oncogene, but also a speciation gene?BioEssays, 30, 822-832.
[52] Schluter D (2009) Evidence for ecological speciation and its alternative.Science, 323, 737-741.
[53] Servedio MR (2009) The role of linkage disequilibrium in the evolution of premating isolation.Heredity, 102, 51-56.
[54] Servedio MR, Saether SA, Saetre GP (2009) Reinforcement and learning.Evolutionary Ecology, 23, 109-123.
[55] Servedio MR, Van Doorn GS, Kopp M, Frame AM, Nosil P (2011) Magic traits in speciation: ‘magic’ but not rare?Trends in Ecology and Evolution, 26, 389-397.
[56] Shafer ABA, Wolf JBW (2013) Widespread evidence for incipient ecological speciation: a meta-analysis of isolation-by-ecology.Ecology Letters, 16, 940-950.
[57] Slatkin M (1987) Gene flow and the geographic structure of natural populations.Science, 236, 787-792.
[58] Smadja CM, Butlin RK (2011) A framework for comparing processes of speciation in the presence of gene ?ow.Molecular Ecology, 20, 5123-5140.
[59] Sobel JM, Chen JF, Watt LR, Schemske DW (2009) The biology of speciation. Evolution, 64, 295-315.
[60] Soons MB, Ozinga WA (2005) How important is long-distance seed dispersal for the regional survival of plant species?Diversity and Distributions, 11, 165-172.
[61] Strasburg JL, Rieseberg LH (2011) Interpreting the estimated timing of migration events between hybridizing species.Molecular Ecology, 20, 2353-2366.
[62] Takahashi A, Tsaur SC, Coyne JA, Wu CI (2001) The nucleotide changes governing cuticular hydrocarbon variation and their evolution in Drosophila melanogaster. Proceedings of the National Academy of Sciences,USA, 98, 3920-3925.
[63] Via S, Conte G, Mason-Foley C, Mills K (2012) Localizing FST outliers on a QTL map reveals evidence for large genomic regions of reduced gene exchange during speciation-with-gene-?ow.Molecular Ecology, 21, 5546-5560.
[64] Wang IJ, Glor RE, Losos JB, Adler F (2013a) Quantifying the roles of ecology and geography in spatial genetic divergence.Ecology Letters, 16, 175-182.
[65] Wang Q, Abbott RJ, Yu QS, Lin K, Liu JQ (2013b) Pleistocene climate change and the origin of two desert plant species, Pugionium cornutum and Pugionium dolabratum (Brassicaceae), in northwest China.New Phytologist, 199, 277-287.
[66] Won YJ, Hey J (2005) Divergence population genetics of chimpanzees.Molecular Biology and Evolution, 22, 297-307.
[67] Wu CI (2001) The genic view of the process of speciation.Journal of Evolutionary Biology, 14, 851-865.
[68] Wu CI, Ting CT (2004) Genes and speciation.Nature Reviews Genetics, 5, 114-122.
[69] Xiang QY, Soltis DE, Soltis PS, Steven, Manchester R, Crawford DJ (2000) Timing the eastern Asian-eastern North American floristic disjunction: molecular clocks confirm paleontological estimates.Molecular Phylogenetics and Evolution, 15, 462-472.
[70] Yang Z (2010) A likelihood ratio test of speciation with gene flow using genomic sequence data.Genome Biology and Evolution, 2, 200-211.
[71] Yang Z, Rannala B (2010) Bayesian species delimitation using multilocus sequence data. Proceedings of the National Academy of Sciences,USA, 107, 9264-9269.
[72] Zheng XM, Ge S (2010) Ecological divergence in the presence of gene flow in two closely related Oryza species (Oryza rufipogon and O. nivara).Molecular Ecology, 19, 2439-2454.
[73] Zhou YF, Abbott RJ, Jiang ZY, Du FK, Milne RI, Liu JQ (2010) Gene flow and species delimitation: a case study of two pine species with overlapping distributions in southeast China.Evolution, 64, 2342-2352.
[1] Chao Li Jin-jin Jin Jin-zhen Luo Chun-hui Wang Jun-jie Wang Jun JunZHAO. (2020) The genetic relationships of hatchery populations of Tanichthys albonubes and wild populations near Guangzhou . Biodiv Sci, 28(4): 474-484.
[2] FAN Zi-Teng, WU Yu-Ling, WANG Xin-Ju, LI Tai-Qiang, GAO Jiang-Yun. (2019) Effects of symbiotic fungi on seed germination of interspecific hybrid progenies in Orchidaceae . Chin J Plant Ecol, 43(4): 374-382.
[3] Hu Ying, Wang Xi, Zhang Xinxin, Zhou Wei, Chen Xiaoyang, Hu Xinsheng. (2019) Advancing phylogeography with chloroplast DNA markers . Biodiv Sci, 27(2): 219-234.
[4] Morigengaowa , Hui Shang, Baodong Liu, Ming Kang, Yuehong Yan. (2019) One or more species? GBS sequencing and morphological traits evidence reveal species diversification of Sphaeropteris brunoniana in China . Biodiv Sci, 27(11): 1196-1204.
[5] Jibao Jiang, Jiangping Qiu. (2018) Origin and evolution of earthworms belonging to the family Megascolecidae in China . Biodiv Sci, 26(10): 1074-1082.
[6] Xiaolong Zhang, Lihua Yang, Ming Kang. (2017) Post-pollination reproductive isolation of sympatric populations of Primulina eburnea and P. mabaensis (Gesneriaceae) . Biodiv Sci, 25(6): 615-620.
[7] Jian-Feng Mao, Yongpeng Ma, Renchao Zhou. (2017) Approaches used to detect and test hybridization: combining phylogenetic and population genetic analyses . Biodiv Sci, 25(6): 577-599.
[8] Linfeng Li, Bao Liu. (2017) The roles of epigenetic variation in plant hybridization and polyploidization . Biodiv Sci, 25(6): 600-607.
[9] Yuguo Wang. (2017) Natural hybridization and speciation . Biodiv Sci, 25(6): 565-576.
[10] Yingxiong Qiu,Qixiang Lu,Yonghua Zhang,Yanan Cao. (2017) Phylogeography of East Asia’s Tertiary relict plants: current progress and future prospects . Biodiv Sci, 25(2): 136-146.
[11] Chao JIANG, Ke TAN, Ming-Xun REN. (2017) Effects of monsoon on distribution patterns of tropical plants in Asia . Chin J Plan Ecolo, 41(10): 1103-1112.
[12] Jianquan Liu. (2016) “The integrative species concept” and “species on the speciation way” . Biodiv Sci, 24(9): 1004-1008.
[13] Dexing Zhang. (2016) Why is it so difficult to reach a consensus in species concept? . Biodiv Sci, 24(9): 1009-1013.
[14] Ping Xie. (2016) A brief review on the historical changes in the concept of species . Biodiv Sci, 24(9): 1014-1019.
[15] Zhenna Qian,Qianwan Meng,Mingxun Ren. (2016) Pollination ecotypes and herkogamy variation of Hiptage benghalensis (Malpighiaceae) with mirror-image flowers . Biodiv Sci, 24(12): 1364-1372.
Full text