Historical introgression and the persistence of ghost alleles in the intermediate horseshoe bat (Rhinolophus affinis)

Molecular Ecology

Volumn 22, Issue 4, 2013, Pages 1035-1050

  Mao, Xiuguang ^a,b   He, Guimei ^a   Hua, Panyu ^a   Jones, Gareth ^c   Zhang, Shuyi ^a   Rossiter, Stephen J ^b  

^a EAST CHINA NORMAL UNIVERSITY   (China)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

asymmetric introgression; hybridization; phylogenetic discordance; speciation

Indexed keywords

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

ALLELE; ANIMAL; ARTICLE; BAT; BAYES THEOREM; BIOLOGICAL MODEL; CELL NUCLEUS; CHINA; CLASSIFICATION; DNA SEQUENCE; ECHOLOCATION; GENE FLOW; GENETIC VARIABILITY; GENETICS; HAPLOTYPE; HYBRIDIZATION; ISLAND (GEOLOGICAL); MOLECULAR EVOLUTION; PHYLOGENY; POPULATION GENETICS;

ALLELES; ANIMALS; BAYES THEOREM; CELL NUCLEUS; CHINA; CHIROPTERA; DNA, MITOCHONDRIAL; ECHOLOCATION; EVOLUTION, MOLECULAR; GENE FLOW; GENETIC VARIATION; GENETICS, POPULATION; HAPLOTYPES; HYBRIDIZATION, GENETIC; ISLANDS; MICROSATELLITE REPEATS; MODELS, GENETIC; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

RHINOLOPHUS AFFINIS;

EID: 84873076950     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12154     Document Type: Article

References (111)

1. Anderson EC, Thompson EA, (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics, 160, 1217-1229.
2. Arnold ML, Sapir Y, Martin NH, (2008) Genetic exchange and the origin of adaptations: prokaryotes to primates. Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 2813-2820.
3. Bachtrog D, Thornton K, Clark A, Andolfatto P, (2006) Extensive introgression of mitochondrial DNA relative to nuclear genes in the Drosophila yakuba species group. Evolution, 60, 292-302.
4. Ballard JWO, Whitlock MC, (2004) The incomplete natural history of mitochondria. Molecular Ecology, 13, 729-744.
5. Barton NH, Hewitt GM, (1985) Analysis of hybrid zones. Annual Review of Ecology and Systematics, 16, 113-148.
6. Barton NH, Hewitt GM, (1989) Adaptation, speciation and hybrid zones. Nature, 341, 497-503.
7. Beaumont MA, Balding DJ, (2004) Identifying adaptive genetic divergence among populations from genome scans. Molecular Ecology, 13, 969-980.
8. Beaumont MA, Zhang W, Balding DJ, (2002) Approximate Bayesian computation in population genetics. Genetics, 162, 2025-2035.
9. Beysard M, Perrin N, Jaarola M, Heckel G, Vogel P, (2012) Asymmetric and differential gene introgression at a contact zone between two highly divergent lineages of field voles (Microtus agrestis). Journal of Evolutionary Biology, 25, 400-408.
10. Bossu CM, Near TJ, (2009) Gene trees reveal repeated instances of mitochondrial introgression in orangethroat darters (Percidae: Etheostoma). Systematic Biology, 58, 114-129.
11. Brumfield RT, Beerli P, Nickerson DA, Edwards SV, (2003) The utility of single nucleotide polymorphisms in inferences of population history. Trends in Ecology and Evolution, 18, 249-256.
12. Carstens BC, Knowles LL, (2007) Shifting distributions and speciation: species divergence during rapid climate change. Molecular Ecology, 16, 619-627.
13. Castric V, Bechsgaard J, Schierup MH, Vekemans X, (2008) Repeated adaptive introgression at a gene under multiallelic balancing selection. PLoS Genetics, 4, e1000168.
14. Chen S-F, Rossiter SJ, Faulkes CG, Jones G, (2006) Population genetic structure and demographic history of the endemic Formosan lesser horseshoe bat (Rhinolophus monoceros). Molecular Ecology, 15, 1643-1656.
15. Chen C, Durand E, Forbes F, François O, (2007) Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Molecular Ecology Notes, 7, 747-756.
16. 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, 2856-2876.
17. Clement M, Posada D, Crandall KA, (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657-1660.
18. Corander J, Marttinen P, (2006) Bayesian identification of admixture events using multilocus molecular markers. Molecular Ecology, 15, 2833-2843.
19. Cornuet JM, Santos F, Beaumont MA, et al,. (2008) Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics, 24, 2713-2719.
20. Cornuet JM, Ravigné A, Estoup A, (2010) Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v. 1.0). BMC Bioinformatics, 11, 401.
21. Crandall KA, Templeton AR, (1993) Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics, 134, 959-969.
22. Currat M, Ruedi M, Petit RJ, Excoffier L, (2008) The hidden side of invasions: massive introgression by local genes. Evolution, 62, 1908-1920.
23. Doi A, Suzuki H, Matsuura ET, (1999) Genetic analysis of temperature-dependent transmission of mitochondrial DNA in Drosophila. Heredity, 82, 555-560.
24. Dopman EB, Perez L, Bogdanowicz SM, Harrison RG, (2005) Consequences of reproductive barriers for genealogical discordance in the European corn borer. Proceedings of the National Academy of Sciences of the United States of America, 102, 14706-14711.
25. Drummond AJ, Rambaut A, (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
26. Duenez-Guzman EA, Mavarez J, Vose MD, Gavrilets S, (2009) Case studies and mathematical models of ecological speciation. 4. Hybrid speciation in butterflies in a jungle. Evolution, 63, 2611-2626.
27. Excoffier L, Laval LG, Schneider S, (2005) ARLEQUIN version. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47-50.
28. Excoffier L, Foll M, Petit RJ, (2009) Genetic consequences of range expansions. Annual Review of Ecology, Evolution, and Systematics, 40, 481-501.
29. Flanders J, Jones G, Benda P, et al,. (2009) Phylogeography of the greater horseshoe bat, Rhinolophus ferrumequinum: contrasting results from mitochondrial and microsatellite data. Molecular Ecology, 18, 306-318.
30. Flanders J, Wei L, Rossiter SJ, Zhang SY, (2011) Identifying the effects of the Pleistocene on the greater horseshoe bat‚ Rhinolophus ferrumequinum‚ in East Asia using ecological niche modelling and phylogenetic analyses. Journal of Biogeography, 38, 439-452.
31. Fu YX, (1997) Statistical test of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915-925.
32. 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.
33. Gompert Z, Buerkle CA, (2011) Bayesian estimate of genomic clines. Molecular Ecology, 20, 2111-2127.
34. Gompert Z, Forister ML, Fordyce JA, Nice CC, (2008) Widespread mito-nuclear discordance with evidence for introgressive hybridization and selective sweeps in Lycaeides. Molecular Ecology, 17, 5231-5244.
35. Goodman SN, (1999) Toward evidence-based medical statistics. 2: The Bayes factor. Annals of International Medicine, 130, 1005-1013.
36. Goudet J, (1995) FSTAT version 1.2: a computer program to calculate F-statistics. Journal of Heredity, 86, 485-486.
37. Grant PR, Grant BR, (1992) Hybridization of bird species. Science, 256, 193-197.
38. Hall TA, (1999) BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95-98.
39. Harpending HC, (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology, 66, 591-600.
40. Hedin M, Wood DA, (2002) Genealogical exclusivity in geographically proximate populations of Hypochilus thorelli Marx (Araneae, Hypochilidae) on Cumberland Plateau of North America. Molecular Ecology, 11, 1975-1988.
41. Hewitt GM, (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society, 58, 247-276.
42. Hewitt GM, (2004) Genetic consequences of climatic oscillations in the Quaternary. Proceedings of the Royal Society of London, Series B: Biological Sciences, 359, 183-195.
43. Hey J, Nielsen R, (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics, 167, 747-760.
44. Hua PY, Guo TT, Liu WC, Zhang SY, Rossiter SJ,. (2009) Isolation and characterization of 13 microsatellite loci in Rhinolophus pusillus (least horseshoe bat) with cross-amplification in five related species. Conservation Genetics, 10, 597-600.
45. Hudson RR, Kaplan N, (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics, 111, 147-164.
46. Hudson RR, Kreitman M, Aguade M, (1987) A test of neutral molecular evolution based on nucleotide data. Genetics, 116, 153-159.
47. Hulva P, Fornuskova A, Chudarkova A, et al,. (2010) Mechanisms of radiation in a bat group from the genus Pipistrellus inferred by phylogeography, demography and population genetics. Molecular Ecology, 19, 5417-5431.
48. Jaarola M, Searle JB, (2004) A highly divergent mitochondrial DNA lineage of Microtus agrestis in southern Europe. Heredity, 92, 228-234.
49. Jakobsson M, Rosenberg NA, (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23, 1801-1806.
50. Jiggins CD, Mallet J, (2000) Bimodal hybrid zones and speciation. Trends in Ecology and Evolution, 15, 250-255.
51. Jones G, Siemers BM, (2011) The communicative function of bat echolocation calls. Journal of Comparative Physiology A, 197, 447-457.
52. Kim M, Cui ML, Cubas P, et al,. (2008) Regulatory genes control a key morphological and ecological trait transferred between species. Science, 322, 1116-1119.
53. Kingston T, Rossiter SJ, (2004) Harmonic-hopping in Wallacea's bats. Nature, 429, 654-657.
54. Kingston T, Lara MC, Jones G, Akbar Z, Kunz TH, Schneider CJ, (2001) Acoustic divergence in two cryptic Hipposideros species: a role for social selection? Proceedings of the Royal Society of London, Series B: Biological Sciences, 268, 1381-1386.
55. Kotlík P, Marková S, Choleva L, Bogutskaya NG, Ekmekçi FG, Ivanova PP, (2008) Divergence with gene flow between Ponto-Caspian refugia in an anadromous cyprinid Rutilus frisii revealed by multiple gene phylogeography. Molecular Ecology, 17, 1076-1088.
56. Kuhner MK, Smith LP, (2007) Comparing likelihood and Bayesian coalescent estimation of population parameters. Genetics, 175, 155-165.
57. Larsen PA, Marchan-Rivadeneira MR, Baker RJ, (2010) Natural hybridization generates mammalian lineage with species characteristics. Proceedings of the National Academy of Sciences of the United States of America, 107, 11447-11452.
58. Lewis PO, Zaykin D, (2001) GENETIC DATA ANALYSIS: Computer Program for the Analysis of Allelic Data, Version 1.0 (d16c). University of Connecticut, Storrs, Connecticut.
59. Linnen CR, Farrell BD, (2007) Mitonuclear discordance is caused by rampant mitochondrial introgression in Neodiprion (Hymenoptera: Diprionidae) sawflies. Evolution, 61, 1417-1438.
60. Mallet J, (2005) Hybridization as an invasion of the genome. Trends in Ecology and Evolution, 20, 229-237.
61. Mao XG, Liu Y, Zhou YY, He BB, Zhang SY, (2009) Development of 19 polymorphic microsatellite loci for the intermediate horseshoe bat, Rhinolophus affinis (Rhinolophidae, Chiroptera). Conservation Genetics, 10, 709-711.
62. Mao XG, Zhu GJ, Zhang SY, Rossiter SJ, (2010a) Pleistocene climatic cycling drives intra-specific diversification in the intermediate horseshoe bat (Rhinolophus affinis) in Southern China. Molecular Ecology, 19, 2754-2769.
63. Mao XG, Zhang JP, Zhang SY, Rossiter SJ, (2010b) Historical male-mediated introgression in horseshoe bats revealed by multi-locus DNA sequence data. Molecular Ecology, 19, 1352-1366.
64. Martinsen GD, Whitham TG, Turek RJ, Keim P, (2001) Hybrid populations selectively filter gene introgression between species. Evolution, 55, 1325-1335.
65. McDonald JH, Kreitman M, (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature, 351, 652-654.
66. Melo-Ferreira J, Boursot P, Suchentrunk F, Ferrand N, Alves PC, (2005) Invasion from the cold past: extensive introgression of mountain hare (Lepus timidus) mitochondrial DNA into three other hare species in Northern Iberia. Molecular Ecology, 14, 2459-2464.
67. Melo-Ferreira J, Boursot P, Randi E, et al,. (2007) The rise and fall of the mountain hare (Lepus timidus) during Pleistocene glaciations: expansion and retreat with hybridization in the Iberian Peninsula. Molecular Ecology, 16, 605-618.
68. Mishmar D, Ruiz-Pesini E, Golik P, et al,. (2003) Natural selection shaped regional mtDNA variation in humans. Proceedings of the National Academy of Sciences of the United States of America, 100, 171-176.
69. Morgan K, Linton Y, Somboon P, et al,. (2010) Inter-specific gene flow dynamics during the Pleistocene-dated speciation of forest-dependent mosquitoes in Southeast Asia. Molecular Ecology, 19, 2269-2285.
70. Nielsen R, Wakeley J, (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics, 158, 885-896.
71. Niki Y, Chigusa SI, Matsuura ET, (1989) Complete replacement of mitochondrial DNA in Drosophila. Nature, 341, 551-552.
72. Nunes MDS, Orozco-Ter Wengel P, Kreissl M, Schlötterer C, (2010) Multiple hybridization events between Drosophila simulans and Drosophila mauritiana are supported by mtDNA introgression. Molecular Ecology, 19, 4695-4707.
73. Paetkau D, Slade R, Burden M, Estoup A, (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Molecular Ecology, 13, 55-65.
74. Palumbi SR, Cipriano F, Hare MP, (2001) Predicting nuclear gene coalescence from mitochondrial data: the three-times rule. Evolution, 55, 859-868.
75. Petit E, Excoffier L, Mayer F, (1999) No evidence of bottleneck in the postglacial recolonization of Europe by the noctule bat (Nyctalus noctula). Evolution, 53, 1247-1258.
76. Piry S, Alapetite A, Cornuet JM, Baudouin PL, Estoup A, (2004) GENECLASS 2: a software for genetic assignment and first generation migrants detection. Journal of Heredity, 95, 536-539.
77. Posada D, Crandall KA, (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817-818.
78. Posada D, Crandall KA, (2001) Intraspecific gene genealogies: trees grafting into networks. Trends in Ecology and Evolution, 16, 37-45.
79. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
80. Rambaut A, Drummond AJ, (2007) Tracer Version 1.4. Available from http://tree.bio.ed.ac.uk/software/tracer.
81. Rannala B, Mountain JL, (1997) Detecting immigration by using multilocus genotypes. Proceedings of the National Academy of Sciences of the United States of America, 94, 9197-9201.
82. Raymond M, Rousset F, (1995) GENEPOP (version 1.2): population genetics software for exact test and ecumenicism. Journal of Heredity, 86, 248-249.
83. Rieseberg LH, (2009) Evolution: replacing genes and traits through hybridization. Current Biology, 19, R119-R122.
84. Rieseberg LH, Whitton J, Gardner K, (1999) Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics, 152, 713-727.
85. Rogers AR, Harpending H, (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution, 9, 552-569.
86. Rogers AR, Fraley AE, Bamshad MJ, Watkins WS, Jorde LB, (1996) Mitochondrial mismatch analysis is insensitive to the mutational process. Molecular Biology Evolution, 13, 895-902.
87. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572-1574.
88. Rosenberg NA, (2004) DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes, 4, 137-138.
89. Rossiter SJ, Benda P, Dietz C, Zhang S, Jones G, (2007) Rangewide phylogeography in the greater horseshoe bat inferred from microsatellites: implications for population history, taxonomy and conservation. Molecular Ecology, 16, 4699-4714.
90. Rozas J, Sanchez-De I, Barrio JC, Messeguer X, Rozas R, (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics, 19, 2496-2497.
91. Salgueiro P, Coelho MM, Palmeirim JM, Ruedi M, (2004) Mitochondrial DNA variation and population structure of the island endemic Azorean bat (Nyctalus azoreum). Molecular Ecology, 13, 3357-3366.
92. Schwartz MK, Mckelvey KS, (2009) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conservation Genetics, 10, 441-452.
93. Shaw KL, (2002) Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation: What mtDNA reveals and conceals about modes of speciation in Hawaiian crickets. Proceedings of the National Academy of Sciences of the United States of America, 99, 16122-16127.
94. Shi YF, Cui ZJ, Su Z, (2006) The Quaternary Glaciations and Environmental Variations in China. Hebei Science and Technology Press, Shijiazhuang
95. Shimodaira H, Hasegawa M, (2001) CONSEL: For assessing the confidence of phylogenetic tree selection. Bioinformatics, 17, 1246-1247.
96. Slatkin M, Hudson RR, (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics, 129, 555-562.
97. Stephens M, Smith N, Donnelly P, (2001) A new statistical method for haplotype reconstruction from population data. AmericanJournal of Human Genetics, 68, 978-989.
98. Strasburg JL, Rieseberg LH, (2010) How robust are "Isolation with Migration" analyses to violations of the IM model? A simulation study Molecular Biology and Evolution, 27, 297-310.
99. Strasburg J, Rieseberg LH, (2011) Interpreting the estimated timing of migration events between hybridization species. Molecular Ecology, 20, 2353-2366.
100. Swofford DL, (2002) PAUP* Ver 4.0.B10. Phylogenetic Analysis Using Parsimony and Other Methods. Sinauer & Associates, Sunderland, Massachusetts.
101. Tajima F, (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585-595.
102. Thabah A, Rossiter SJ, Kingston T, et al,. (2006) Genetic divergence and echolocation call frequency in cryptic species of Hipposideros larvatus s.l (Chiroptera: Hipposideridae) from the Indo-Malayan region. Biological Journal of the Linnean Society, 88, 119-130.
103. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG, (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876-4882.
104. Turmelle AS, Kunz TH, Sorenson MD, (2010) A tale of two genomes: contrasting patterns of phylogeographic structure in a widely distributed bat. Molecular Ecology, 20, 357-375.
105. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P, (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535-538.
106. You Y, Sun K, Xu L, et al,. (2010) Pleistocene glacial cycle effects on the phylogeography of the Chinese endemic bat species, Myotis advidii. BMC Evolutionary Biology, 10, 208.
107. Zhan XJ, Zheng YF, Wei FW, Bruford MW, Jia C, (2011) Molecular evidence for Pleistocene refugia at the eastern edge of the Tibetan Plateau. Molecular Ecology, 20, 3014-3026.
108. Zhang H, Yan J, Zhang G, Zhou K, (2008) Phylogeography and demographic history of Chinese black-spotted frog populations (Pelophylax nigromaculata): evidence for independent refugia expansion and secondary contact. BMC Evolutionary Biology, 8, 21.
109. Zhang L, Jones G, Zhang J, et al,. (2009) Recent surveys of bats (Mammalia: Chiroptera) from China. I. Rhinolophidae and Hipposideridae. Acta Chiropterologica, 11, 71-88.
110. Zhao HB, Rossiter SJ, Teeling EC, Li CJ, Cotton JA, Zhang SY, (2009) The evolution of color vision in nocturnal mammals. Proceedings of the National Academy of Sciences of the United States of America, 106, 8980-8985.
111. Zhou ZM, Xu WX, Wu Y, Li YC, Hu JC, (2005) Morphometric characteristics of three subspecies of Rhinolophus affinis in China. Zoological Research, 26, 645-651.