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Microsatellite variation suggests a recent fine-scale population structure of Drosophila sechellia, a species endemic of the Seychelles archipelago

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Abstract

Drosophila sechellia is closely related to the cosmopolitan and widespread model species, D. simulans. This species, endemic to the Seychelles archipelago, is specialized on the fruits of Morinda citrifolia, and harbours the lowest overall genetic diversity compared to other species of Drosophila. This low diversity is associated with a small population size. In addition, no obvious population structure has been evidenced so far across islands of the Seychelles archipelago. Here, a microsatellite panel of 17 loci in ten populations from nine islands of the Seychelles was used to assess the effect of the D. sechellia’s fragmented distribution on the fine-scale population genetic structure, the migration pattern, as well as on the demography of the species. Contrary to previous results, also based on microsatellites, no evidence for population contraction in D. sechellia was found. The results confirm previous studies based on gene sequence polymorphism that showed a long-term stable population size for this species. Interestingly, a pattern of Isolation By Distance which had not been described yet in D. sechellia was found, with evidence of first-generation migrants between some neighbouring islands. Bayesian structuring algorithm results were consistent with a split of D. sechellia into two main groups of populations: Silhouette/Mahé versus all the other islands. Thus, microsatellites suggest that variability in D. sechellia is most likely explained by local genetic exchanges between neighbouring islands that have recently resulted in slight differentiation of the two largest island populations from all the others.

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References

  • Amlou M, Moreteau B, David JR (1998) Larval tolerance in the Drosophila melanogaster species complex toward the two toxic acids of the D. sechellia host plant. Hereditas 129:7–14

    Article  PubMed  CAS  Google Scholar 

  • Andolfatto P (2001) Contrasting patterns of nucleotide variation at X-linked and autosomal loci in Drosophila melanogaster and D. simulans. Mol Biol Evol 18:275–290

    Google Scholar 

  • Begun DJ, Whitley P (2000) Reduced X-linked nucleotide polymorphism in Drosophila simulans. Proc Natl Acad Sci USA 97:5960–5965

    Article  PubMed  CAS  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of false discovery rate under dependency. Ann Stat 29:1165–1188

    Article  Google Scholar 

  • Bilgin R (2007) Kgtests: a simple excel macro program to detect signatures of population expansion using microsatellites. Mol Ecol Notes 7:416–417

    Article  CAS  Google Scholar 

  • Cariou M-L, Solignac M, Monnerot M, David JR (1990) Low allozyme and mtDNA variability in the island endemic species Drosophila sechellia (D. melanogaster complex). Experientia 46:101–104

    Article  PubMed  CAS  Google Scholar 

  • Cobb M, Huet M, Lachaise D, Veuille M (2001) Fragmented forests, evolving flies: molecular variation in African populations of Drosophila teissieri. Mol Ecol 9:1591–1597

    Article  Google Scholar 

  • Colson I, Goldstein DB (1999) Evidence for complex mutations at microsatellite loci in Drosophila. Genetics 152:617–627

    PubMed  CAS  Google Scholar 

  • Colson I, MacDonald SJ, Goldstein DB (1999) Microsatellite markers for interspecific mapping of Drosophila simulans and D. sechellia. Mol Ecol 8:1951–1955

    Article  PubMed  CAS  Google Scholar 

  • Cornuet J-M, Luikart G (1996) Description and power analysis of two tests for detecting recent bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • Dekker T, Ibba I, Siju KP, Stensmyr MC, Hansson BS (2006) Olfactory shifts parallel superspecialism for toxic fruit in Drosophila melanogaster sibling, D. sechellia. Curr Biol 16:101–109

    Article  PubMed  CAS  Google Scholar 

  • Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169

    Article  CAS  Google Scholar 

  • Dobzhansky T, Powell JR (1974) Rates of dispersal of Drosophila pseudoobscura and its relatives. Proc R Soc Lond B Biol Sci 187:281–298

    Article  PubMed  CAS  Google Scholar 

  • Dworkin I, Jones CD (2009) Genetic changes accompagnying the evolution of host specialization in Drosophila sechellia. Genetics 181:721–736

    Article  PubMed  CAS  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) ARLEQUIN (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinf Online 1:47–50

    CAS  Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  PubMed  CAS  Google Scholar 

  • Glaubitz JC (2004) CONVERT: a user friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Mol Ecol Notes 4:309–310

    Article  CAS  Google Scholar 

  • Goldstein DB, Clark AG (1995) Microsatellite variation in North American populations of Drosophila melanogaster. Nucleic Acids Res 23:3882–3886

    Article  PubMed  CAS  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil2.ch/genpop/softwares/fstat.html

  • Harr B, Schlötterer C (2004) Patterns of microsatellite variability in the Drosophila melanogaster complex. Genetica 120:71–77

    Article  PubMed  CAS  Google Scholar 

  • Hutter CM, Schug MD, Aquadro CF (1998) Molecular variation in Drosophila melanogaster and Drosophila simulans: a reciprocal test of the ascertainment bias hypothesis. Mol Biol Evol 15:1620–1636

    PubMed  CAS  Google Scholar 

  • Jones CD (2005) The genetics of adaptation in Drosophila sechellia. Genetica 123:137–145

    Article  PubMed  Google Scholar 

  • Kliman RM, Andolfatto P, Coyne JA, Depaulis F, Kreitman M, Berry AJ, McCarter J, Wakeley J, Hey J (2000) The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics 156:1913–1931

    PubMed  CAS  Google Scholar 

  • Kopp A, Barmina O, Hamilton AM, Higgins L, McIntyre LM, Jones CD (2008) Evolution of gene expression in the Drosophila olfactory system. Mol Biol Evol 25:1081–1092

    Article  PubMed  CAS  Google Scholar 

  • Lachaise D, Silvain J-F (2004) How two Afrotropical endemics made two cosmopolitan human commensals: the Drosophila melanogaster-D. simulans paleogeographic riddle. Genetica 120:17–39

    Article  PubMed  Google Scholar 

  • Lachaise D, Cariou ML, David JR, Lemeunier F, Tsacas L, Ashburner M (1988) Historical biogeography of the Drosophila melanogaster species subgroup. Evol Biol 22:159–225

    Google Scholar 

  • Lachaise D, Capy P, Cariou ML, Joly D, Lemeunier F, David JR (2004) Nine relatives from one African ancestor: population biology and evolution of the Drosophila melanogaster subgroup species. In: Singh RS, Uyenoyama MK (eds) The evolution of population biology. Cambridge University Press, Cambridge, pp 315–343

    Chapter  Google Scholar 

  • Legrand D, Tenaillon MI, Matyot P, Gerlach J, Lachaise D, Cariou M-L (2009) Species-wide genetic variation and demographic history of Drosophila sechellia, a species lacking population structure. Genetics 182:1197–1206

    Article  PubMed  CAS  Google Scholar 

  • Legrand D, Chenel T, Campagne C, Lachaise D, Cariou M-L (2011) Inter-island divergence within Drosophila mauritiana, a species of the D. simulans complex: past history and/or speciation in progress? Mol Ecol 20:2787–2804

  • Louis J, David JR (1986) Ecological specialization in the Drosophila melanogaster species subgroup: a case study of D. sechellia. Acta Oecol 7:215–229

    Google Scholar 

  • Luikart G, Cornuet J-M, Allendorf FW, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247

    Article  PubMed  CAS  Google Scholar 

  • Mallet J (2006) What does Drosophila genetics tell us about speciation? Trends Ecol Evol 21:386–393

    Article  PubMed  Google Scholar 

  • Matsuo T, Sugaya S, Yasukawa J, Aigaki T, Fuyama Y (2007) Odorant-binding proteins OBP57d and OBP57e affect taste perception and host-plant preference in Drosophila sechellia. PLoS Biol 5:e118

    Article  PubMed  Google Scholar 

  • McBride CS (2007) Rapid evolution of smell and taste receptor genes during host specialization in Drosophila sechellia. Proc Natl Acad Sci USA 104:4996–5001

    Article  PubMed  CAS  Google Scholar 

  • Nielsen R, Beaumont MA (2009) Statistical inferences in phylogeography. Mol Ecol 18:1034–1047

    Article  PubMed  CAS  Google Scholar 

  • Nunes MDS, Neumeier H, Schlötterer C (2008) Contrasting patterns of natural variation in global Drosophila melanogaster populations. Mol Ecol 17:4470–4479

    Article  PubMed  CAS  Google Scholar 

  • Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354

    Article  PubMed  CAS  Google Scholar 

  • Paetkau D, Slade R, Burden M, Estoup A (2004) Direct, real-time estimation of migration rate using assignment methods: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65

    Article  PubMed  CAS  Google Scholar 

  • Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GENEClASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    Article  PubMed  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201

    Article  PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249

    Google Scholar 

  • Reich DE, Goldstein DB (1998) Genetic evidence for a Paleolithic human population expansion in Africa. Proc Natl Acad Sci USA 95:8119–8123

    Article  PubMed  CAS  Google Scholar 

  • Reich DE, Feldman MW, Goldstein DB (1999) Statistical properties of two tests that use multilocus data sets to detect population expansion. Mol Biol Evol 16:453–466

    CAS  Google Scholar 

  • R’kha S, Capy P, David JR (1991) Host-plant specialization in the Drosophila melanogaster species complex: a physiological, behavioral, and genetical analysis. Proc Natl Acad Sci USA 88:1835–1839

    Article  PubMed  Google Scholar 

  • Rogers A, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    PubMed  CAS  Google Scholar 

  • Roose-Amsaleg C, Cariou-Pham E, Vautrin D, Tavernier R, Solignac M (2006) Polymorphic microsatellite loci in Linum usitatissimum. Mol Ecol Notes 6:796–799

    Article  CAS  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    PubMed  CAS  Google Scholar 

  • Schöfl G, Schlötterer C (2006) Microsatellite variation and differentiation in African and non-African populations of Drosophila simulans. Mol Ecol 15:3895–3905

    Article  PubMed  Google Scholar 

  • Schug MD, Mackay TF, Aquadro CF (1997) Low mutation rates of microsatellite loci in Drosophila melanogaster. Nature Rev Genet 15:99–102

    Article  CAS  Google Scholar 

  • Solignac M (2004) Mitochondrial DNA in the Drosophila melanogaster complex. Genetica 120:41–50

    Article  PubMed  CAS  Google Scholar 

  • Tsacas L, Bächli G (1981) Drosophila sechellia, n.sp., huitième espèce du sous-groupe melanogaster des Iles Séchelles [Diptera, Drosophilidae]. Revue Fr Ent NS 3:146–150

    Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-Statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Zhang DX, Hewitt GM (2003) Nuclear DNA analyses in genetic studies of populations: practice, problems and prospects. Mol Ecol 12:563–584

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the two reviewers for helpful comments and valuable suggestions. We thank Jean-Luc Da Lage for analyzing the data with M_P_VAL.EXE software and Emilie Robillard for formatting the data. This work was funded by the French Ministry of Environment and Sustainable Development through the programme “Invasions Biologiques” (CV 02000216), by the Centre National de la Recherche Scientifique and by the ANR Biodiversity program (ANR-06-BDIV-002-05).

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Correspondence to Marie-Louise Cariou.

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Daniel Lachaise deceased in 2006.

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10709_2011_9595_MOESM1_ESM.docx

Figure S1: Determination of the number of clusters best fitting allele frequencies at 17 microsatellites in D. sechellia. (above): Mean log-likelihood over five runs for K comprised between 1 and 10, (below): ΔK as a function of K following Evanno et al. (2005)

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Legrand, D., Vautrin, D., Lachaise, D. et al. Microsatellite variation suggests a recent fine-scale population structure of Drosophila sechellia, a species endemic of the Seychelles archipelago. Genetica 139, 909–919 (2011). https://doi.org/10.1007/s10709-011-9595-8

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