Distinguishing migration from isolation using genes with intragenic recombination: detecting introgression in the Drosophila simulans species complex

BMC Evolutionary Biology

Frantz Depaulis²  Marie-Louise Cariou³  Cécile Campagne³  Delphine Legrand³  Miguel Navascués¹ 

[1] INRA, UMR1062 CBGP, F-34988 Montferrier-sur-Lez, France;Laboratoire d’Écologie, École Normale Supérieure, 46 rue d’Ulm, 75230 Paris cedex 05, France;UPR 9034 Évolution, Génomes et Spéciation, CNRS, avenue de la Terrasse, 91198 Gif sur Yvette, France

关键词: Drosophila simulans complex;    Incomplete lineage sorting;    Gene flow;    Hybridization;    Recombination;    Shared polymorphism;   

Others  :  856642
DOI  :  10.1186/1471-2148-14-89

 received in 2013-11-14, accepted in 2014-04-03,  发布年份 2014

【 摘 要 】

Background

Determining the presence or absence of gene flow between populations is the target of some statistical methods in population genetics. Until recently, these methods either avoided the use of recombining genes, or treated recombination as a nuisance parameter. However, genes with recombination contribute additional information for the detection of gene flow (i.e. through linkage disequilibrium).

Methods

We present three summary statistics based on the spatial arrangement of fixed differences, and shared and exclusive polymorphisms that are sensitive to the presence and direction of gene flow. Power and false positive rate for tests based on these statistics are studied by simulation.

Results

The application of these tests to populations from the Drosophila simulans species complex yielded results consistent with migration between D. simulans and its two endemic sister species D. mauritiana and D. sechellia, and between populations D. mauritiana on the islands of the Mauritius and Rodrigues.

Conclusions

We demonstrate the sensitivity of the developed statistics to the presence and direction of gene flow, and characterize their power as a function of differentiation level and recombination rate. The properties of these statistics make them especially suitable for analyzing high-throughput sequencing data or for their integration within the approximate Bayesian computation framework.

【 授权许可】

   
2014 Navascués et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Dobzhansky T, Wright S: Genetics of natural populations. v. relations between mutation rate and accumulation of lethals in populations of drosophila pseudoobscura. Genetics 1941, 26:23-51.
• [2]Cavalli-Sforza LL: Human Diversity. In Proceedings of the 12th International Congress on Genetics. Volume 3. Tokyo; 1969:405-416.
• [3]Wakeley J: Distinguishing migration from isolation using the variance of pairwise differences. Theor Popul Biol 1996, 49:369-386.
• [4]Nielsen R, Wakeley J: Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 2001, 158:885-896.
• [5]Pinho C, Hey J: Divergence with gene flow: models and data. Annu Rev Ecol Evol Syst 2010, 41:215-230.
• [6]Hey J, Nielsen R: Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc Natl Acad Sci U S A 2007, 104:2785-2790.
• [7]Strasburg JL, Rieseberg LH: How robust are “Isolation with Migration” analyses to violations of the IM model? A simulation study. Mol Biol Evol 2010, 27:297-310.
• [8]Becquet C, Przeworski M: A new approach to estimate parameters of speciation models with application to apes. Genome Res 2007, 17:1505-1519.
• [9]Gutenkunst RN, Hernandez RD, Williamson SH, Bustamante CD: Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet 2009, 5:e1000695.
• [10]Tellier A, Pfaffelhuber P, Haubold B, Naduvilezhath L, Rose LE, Städler T, Stephan W, Metzler D: Estimating parameters of speciation models based on refined summaries of the joint site-frequency spectrum. PLoS One 2011, 6:e18155.
• [11]Machado CA, Kliman RM, Markert JA, Hey J: Inferring the history of speciation from multilocus DNA sequence data: the case of Drosophila pseudoobscura and close relatives. Mol Biol Evol 2002, 19:472-488.
• [12]Davison D, Pritchard JK, Coop G: An approximate likelihood for genetic data under a model with recombination and population splitting. Theor Popul Biol 2009, 75:331-345.
• [13]Harris K, Nielsen R: Inferring Demographic History from a Spectrum of Shared Haplotype Lengths. PLoS Genet 2013, 9:e1003521.
• [14]Lachaise D, Capy P, Cariou M-L, Joly D, Lemeunier F, David JR: Nine relatives from one African ancestor: population biology and evolution of the Drosophila melanogaster subgroup species. In The Evolution of Population Biology. Edited by Singh RS, Uyenoyama MK. Cambridge: Cambridge University Press; 2004:315-343.
• [15]Mallet J: What does Drosophila genetics tell us about speciation? Trends Ecol Evol 2006, 21:386-393.
• [16]Garrigan D, Kingan SB, Geneva AJ, Andolfatto P, Clark AG, Thornton KR, Presgraves DC: Genome sequencing reveals complex speciation in the Drosophila simulans clade. Genome Res 2012, 22:1499-1511.
• [17]Dean MD, Ballard JWO: Linking phylogenetics with population genetics to reconstruct the geographic origin of a species. Mol Phylogenet Evol 2004, 32:998-1009.
• [18]Irvin SD, Wetterstrand KA, Hutter CM, Aquadro CF: Genetic Variation and Differentiation at Microsatellite Loci in Drosophila simulans: Evidence for Founder Effects in New World Populations. Genetics 1998, 150:777-790.
• [19]Veuille M, Baudry E, Cobb M, Derome N, Gravot E: Historicity and the population genetics of Drosophila melanogaster and D. simulans. Genetica 2004, 120:61-70.
• [20]Schöfl G, Schlötterer C: Microsatellite variation and differentiation in African and non-African populations of Drosophila simulans. Mol Ecol 2006, 15:3895-3905.
• [21]R’Kha S, Capy P, David JR: Host-plant specialization in the Drosophila melanogaster species complex: a physiological, behavioral, and genetical analysis. Proc Natl Acad Sci U S A 1991, 88:1835-1839.
• [22]R’Kha S, Moreteau B, Coyne JA, David JR: Evolution of a lesser fitness trait: egg production in the specialist Drosophila sechellia. Genet Res 1997, 69:17-23.
• [23]Cariou M-L, Solignac M, Monnerot M, David JR: Low allozyme and mtDNA variability in the island endemic species Drosophila sechelia (D. melanogaster complex). Experientia 1990, 46:101-104.
• [24]Kliman RM, Andolfatto P, Coyne JA, Depaulis F, Kreitman M, Berry AJ, McCarter J, Wakeley J, Hey J: The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics 2000, 156:1913-1931.
• [25]Legrand D, Tenaillon MI, Matyot P, Gerlach J, Lachaise D, Cariou M-L: Species-wide genetic variation and demographic history of Drosophila sechellia, a species lacking population structure. Genetics 2009, 182:1197-1206.
• [26]Legrand D, Vautrin D, Lachaise D, Cariou M-L: Microsatellite variation suggests a recent fine-scale population structure of the island endemic species Drosophila sechellia. Genetica 2011, 139:909-919.
• [27]Legrand D, Chenel T, Campagne C, Lachaise D, Cariou M-L: Inter-island divergence within Drosophila mauritiana, a species of the D. simulans complex: Past history and/or speciation in progress? Mol Ecol 2011, 20:2787-2804.
• [28]Lachaise D, Cariou M-L, David JR, Lemeunier F, Tsacas L, Ashburner M: Historical biogeography of the Drosophila melanogaster species subgroup. Evol Biol 1988, 22:159-225.
• [29]Cariou M-L, Silvain J-F, Daubin V, Da Lage J-L, Lachaise D: Divergence between Drosophila santomea and allopatric or sympatric populations of D. yakuba using paralogous amylase genes and migration scenarios along the Cameroon volcanic line. Mol Ecol 2008, 10:649-660.
• [30]Wakeley J, Hey J: Estimating ancestral population parameters. Genetics 1997, 145:847-855.
• [31]DeMarais BD, Dowling TE, Douglas ME, Minckley WL, Marsh PC: Origin of Gila seminuda (Teleostei: Cyprinidae) through introgressive hybridization: implications for evolution and conservation. Proc Natl Acad Sci U S A 1992, 89:2747-2751.
• [32]Plagnol V, Wall JD: Possible ancestral structure in human populations. PLoS Genet 2006, 2:e105.
• [33]Pool JE, Nielsen R: Inference of historical changes in migration rate from the lengths of migrant tracts. Genetics 2009, 181:711-719.
• [34]Wald A, Wolfowitz J: On a test whether two samples are from the same population. Ann Math Stat 1940, 11:147-162.
• [35]Nei M, Li W-H: Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci U S A 1979, 76:5269-5273.
• [36]Ramos-Onsins SE, Stranger BE, Mitchell-Olds T, Aguadé M: Multilocus analysis of variation and speciation in the closely related species Arabidopsis halleri and A. lyrata. Genetics 2004, 166:373-388.
• [37]Sherman B: A random variable related to the spacing of sample values. Ann Math Stat 1950, 21:339-361.
• [38]Sneath PHA: The distribution of the random division of a molecular sequence. Binary Comput Microb 1995, 7:148-152.
• [39]Nunes MDS, Orozco-Ter Wengel P, Kreissl M, Schlötterer C: Multiple hybridization events between Drosophila simulans and Drosophila mauritiana are supported by mtDNA introgression. Mol Ecol 2010, 19:4695-4707.
• [40]David JR, McEvey SF, Solignac M, Tsacas L: Drosophila communities on Mauritius and the ecological niche of D. mauritiana (Diptera, Drosophilidae). J Afr Zool 1989, 103:107-116.
• [41]Hey J, Nielsen R: Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 2004, 167:747-760.
• [42]Huang W, Takebayashi N, Qi Y, Hickerson M: MTML-msBayes: approximate Bayesian comparative phylogeographic inference from multiple taxa and multiple loci with rate heterogeneity. BMC Bioinforma 2011, 12:1.
• [43]Futschik A, Schlotterer C: The next generation of molecular markers from massively parallel sequencing of pooled DNA samples. Genetics 2010, 186:207-218.
• [44]Hudson RR: Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 2002, 18:337-338.
• [45]McVean G, Awadalla P, Fearnhead P: A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 2002, 160:1231-1241.
• [46]R Development Core Team: R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2009.
• [47]Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.