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Population structure of two beetle-associated yeasts: comparison of a New World asexual and an endemic Nearctic sexual species in the Metschnikowia clade

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Abstract

The genetic structure of two related yeast species, one sexual and one asexual, was compared using polymorphic DNA markers. Although both yeasts propagate by asexual budding of haploid cells, Metschnikowia borealis reproduces sexually when compatible strains come in contact. To what extent this has occurred in nature was not known. As Candida ipomoeae is a closely related, asexual species, the two yeasts provide an excellent model system to assess the role of sexual reproduction in a biogeographic context. Natural isolates of the two species were characterized using several polymorphic DNA markers. As predicted for an organism whose reproduction is strictly clonal, C. ipomoeae exhibited low haplotype diversity, high linkage disequilibrium, and high population differentiation. In contrast, M. borealis had unique haplotypes in most isolates, lower population differentiation, and little linkage disequilibrium, demonstrating that sexual recombination is prevalent. Geographic gradients were identified in both species, indicating that historical and climatic factors both play a role in shaping the populations. The spatial structure is also thought to be influenced by the ecology of the small floricolous beetles (family Nitidulidae) that vector the yeasts. For example, Hawaiian strains of C. ipomoeae show evidence of having undergone a genetic bottleneck, most likely when the vector was introduced to the islands. The two haplotypes found in Hawaii were nearly identical and were also found in North and Central America. M. borealis had a more continuous distribution where the genetic markers follow latitudinal and longitudinal gradients.

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References

  • Aa E, Townsend JP, Adams RI, Nielsen KM, Taylor JW (2006) Population structure and gene evolution in Saccharomyces cerevisiae. FEMS Yeast Res 6:702–715. doi:10.1111/j.1567-1364.2006.00059.x

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Bell G (1988) Uniformity and diversity in the evolution of sex. In: Michod RE, Leven BR (eds) The evolution of sex. Sinauer, Sunderland, Massachusetts, pp 126–138

    Google Scholar 

  • Burt A, Carter DA, White TJ, Taylor JW (1994) DNA sequencing with arbitrary primer pairs. Mol Ecol 3:523–524. doi:10.1111/j.1365-294X.1994.tb00131.x

    Article  PubMed  CAS  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660. doi:10.1046/j.1365-294x.2000.01020.x

    Article  PubMed  CAS  Google Scholar 

  • Fidalgo Jiménez A, Daniel HM, Evrard P, Decock C, Lachance MA (2008) Metschnikowia cubensis sp. nov., a novel yeast species isolated from flowers in Cuba. Int J Syst Evol Microbiol 58:2955–2961. doi:10.1099/ijs.0.2008/001198-0

    Article  PubMed  Google Scholar 

  • Gräser Y, Volovsek M, Arrington J, Schönian G, Presber W, Mitchell TG, Vilgalys R (1996) Molecular markers reveal that population structure of the human pathogen Candida albicans exhibits both clonality and recombination. Proc Natl Acad Sci USA 93:12473–12477. doi:10.1073/pnas.93.22.12473

    Article  PubMed  Google Scholar 

  • Hillis DM (2007) Asexual evolution: can species exist without sex? Curr Biol 17:R543–R544. doi:10.1016/j.cub.2007.05.015

    Article  PubMed  CAS  Google Scholar 

  • Hudson RR, Kreitman M, Aguadé M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159

    PubMed  CAS  Google Scholar 

  • Johnson LJ, Koufopanou V, Goddard MR, Hetherington R, Schäfer SM, Burt A (2004) Population genetics of the wild yeast Saccharomyces paradoxus. Genetics 166:43–52. doi:10.1534/genetics.166.1.43

    Article  PubMed  CAS  Google Scholar 

  • Koufopanou V, Hughes J, Bell G, Burt A (2006) The spatial scale of genetic differentiation in a model organism: the wild yeast Saccharomyces paradoxus. Phil Trans Royal Soc Lond. Ser B Biol Sci 361:1941–1946

    Article  Google Scholar 

  • Kuehne HA, Murphy HA, Francis CA, Sniegowski PD (2007) Allopatric divergence, secondary contact, and genetic isolation in wild yeast populations. Curr Biol 17:407–411. doi:10.1016/j.cub.2006.12.047

    Article  PubMed  CAS  Google Scholar 

  • Kurtzman CP, Robnett CJ (1998) Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie Van Leeuwenhoek 73:331–371. doi:10.1023/A:1001761008817

    Article  PubMed  CAS  Google Scholar 

  • Lachance MA, Rosa CA, Starmer WT, Schlag-Edler B, Barker JSF, Bowles JM (1998a) Metschnikowia continentalis var. continentalis, Metschnikowia continentalis var. borealis, and Metschnikowia hibisci, new heterothallic haploid yeasts from ephemeral flowers and associated insects. Can J Microbiol 44:279–288. doi:10.1139/cjm-44-3-279

    Article  CAS  Google Scholar 

  • Lachance MA, Rosa CA, Starmer WT, Bowles JM (1998b) Candida ipomoeae, a new yeast species related to large-spored Metschnikowia species. Can J Microbiol 44:718–722. doi:10.1139/cjm-44-8-718

    Article  PubMed  CAS  Google Scholar 

  • Lachance MA, Starmer WT, Bowles JM, Phaff HJ, Rosa CA (2000) Ribosomal DNA, species structure, and biogeography of the cactophilic yeast Clavispora opuntiae. Can J Microbiol 46:195–210. doi:10.1139/cjm-46-3-195

    Article  PubMed  CAS  Google Scholar 

  • Lachance MA, Bowles JM, Kwon S, Marinoni G, Starmer WT, Janzen DH (2001a) Metschnikowia lochheadii and Metschnikowia drosophilae, two new yeast species isolated from insects associated with flowers. Can J Microbiol 47:103–109. doi:10.1139/cjm-47-2-103

    Article  PubMed  CAS  Google Scholar 

  • Lachance MA, Starmer WT, Rosa CA, Bowles JM, Barker JSF, Janzen DH (2001b) Biogeography of the yeasts of ephemeral flowers and their insects. FEMS Yeast Res 1:1–8

    PubMed  CAS  Google Scholar 

  • Lachance MA, Bowles JM, Starmer WT (2003) Metschnikowia santaceciliae, Candida hawaiiana, and Candida kipukae, three new yeast species associated with insects of tropical morning glory. FEMS Yeast Res 3:97–103

    PubMed  CAS  Google Scholar 

  • Lachance MA, Ewing CP, Bowles JM, Starmer WT (2005) Metschnikowia hamakuensis sp. nov., Metschnikowia kamakouana sp. nov., and Metschnikowia mauinuiana sp. nov., three endemic yeasts from Hawaiian nitidulid beetles. Int J Syst Evol Microbiol 55:1369–1377. doi:10.1099/ijs.0.63615-0

    Article  PubMed  CAS  Google Scholar 

  • Lachance MA, Lawrie D, Dobson J, Piggott J (2008) Biogeography and population structure of the Neotropical endemic yeast species Metschnikowia lochheadii. Antonie Van Leeuwenhoek 94:403–414. doi:10.1007/s10482-008-9258-7

    Article  PubMed  Google Scholar 

  • Lomolino MV, Riddle BR, Brown JH (2006) Biogeography, 3rd edn. Sinauer Associates, Sunderland, Massachuetts, 752 pp

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    PubMed  CAS  Google Scholar 

  • Marinoni G, Lachance MA (2004) Speciation in the large-spored Metschnikowia clade and establishment of a new species, Metschnikowia borealis comb. nov. FEMS Yeast Res 4:587–596. doi:10.1016/j.femsyr.2003.12.005

    Article  CAS  Google Scholar 

  • Marinoni G, Piskur J, Lachance MA (2003) Ascospores of large-spored Metschnikowia species are genuine meiotic products of these yeasts. FEMS Yeast Res 3:85–90

    PubMed  CAS  Google Scholar 

  • Maynard Smith J, Smith NH, O’Rourke M, Spratt B (1993) How clonal are bacteria? Proc Natl Acad Sci USA 90:4384–4388. doi:10.1073/pnas.90.10.4384

    Article  Google Scholar 

  • McNeill J et al (2006) International Code of Botanical Nomenclature (Vienna Code). Fantner Verlag, Ruggell, p 568

    Google Scholar 

  • Nasir H, Noda H (2003) Yeast-like symbiotes as a sterol source in anobiid beetles (Coleoptera, Anobiidae): possible metabolic pathways from fungal sterols to 7-dehydrocholesterol. Arch Insect Biochem Physiol 52:175–182. doi:10.1002/arch.10079

    Article  PubMed  CAS  Google Scholar 

  • Nishida T (1957) Food plants, distribution, and variation in abundance of Conotelus mexicanus Murray, a recently discovered immigrant insect in Hawaii (Coleoptera: Nitidulidae). Proc Hawaii Entomol Soc 16:307–312

    Google Scholar 

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

    Google Scholar 

  • Replansky T, Koufopanou V, Greig D, Bell G (2008) Saccharomyces sensu stricto as a model system for evolution and ecology. Trends Ecol Evol 23:494–501. doi:10.1016/j.tree.2008.05.005

    Article  PubMed  Google Scholar 

  • Rosa CA, Lachance MA, Teixeira LCRS, Pimenta RS, Morais PB (2007) Metschnikowia cerradonensis sp. nov., a yeast species isolated from ephemeral flowers and their nitidulid beetles in Brazil. Int J Syst Evol Microbiol 57:161–165. doi:10.1099/ijs.0.64624-0

    Article  PubMed  CAS  Google Scholar 

  • Rozas J, Sanchez-Delbarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497. doi:10.1093/bioinformatics/btg359

    Article  PubMed  CAS  Google Scholar 

  • Sampaio JP, Gonçalves P (2008) Natural populations of Saccharomyces kudriavzevii in Portugal are associated with oak bark and are sympatric with S. cerevisiae and S. paradoxus. Appl Environ Microbiol 74:2144–2152. doi:10.1128/AEM.02396-07

    Article  PubMed  CAS  Google Scholar 

  • Sniegowski PD, Dombrowski PG, Fingerman E (2002) Saccharomyces cerevisiae and Saccharomyces paradoxus coexist in a natural woodland site in North America and display different levels of reproductive isolation from European conspecifics. FEMS Yeast Res 1:299–306

    PubMed  CAS  Google Scholar 

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633

    PubMed  CAS  Google Scholar 

  • Tsai IJ, Bensasson D, Burt A, Koufopanou V (2008) Population genomics of the wild yeast Saccharomyces paradoxus: quantifying the life cycle. Proc Natl Acad Sci USA 105:4957–4962. doi:10.1073/pnas.0707314105

    Article  PubMed  CAS  Google Scholar 

  • Weaver SE, Riley WR (1982) The biology of Canadian weeds. 53. Convoluvulus arvensis. Can J Plant Sci 62:461–472

    Article  Google Scholar 

  • Williams RN, Jelínek J, Habeck DH (1988) Annotated bibliography of the genus Conotelus Erichson (Coleoptera: Nitidulidae). Miscell Publ Entomol Soc Am 69:1–14

    Google Scholar 

  • Xu J (2004) The prevalence and evolution of sex in microorganisms. Genome 47:775–780. doi:10.1139/g04-037

    Article  PubMed  Google Scholar 

  • Yarrow D (1998) Methods for the isolation and identification of yeasts. In: Kurtzman CP, Fell JW (eds) The yeasts, a taxonomic study, vol 4. Elsevier, Amsterdam, pp 77–100

    Chapter  Google Scholar 

  • Zeyl C (2007) Ploidy and the sexual yeast genome in theory, nature, and experiment. In: Hietman J, Kronstad JW, Taylor JW, Casselton LA (eds) Sex in Fungi. Molecular determination, evolutionary implications. ASM Press, Washington, pp 507–525

    Google Scholar 

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Acknowledgments

We acknowledge funding from the Natural Science and Engineering Research Council (Discovery Grant to MAL, USRA Scholarships to AMW and KCM). We also acknowledge the Costa Rican Ministry of the Environment and the US National Park Service for the issuance of collection or research permits. Assistance with field collections by Jane Bowles, Felipe Chavaria, Dan Janzen, Louise Lachance, Marcel Legault, Michal Polak, Carlos Rosa, and Tom Starmer is greatly appreciated. We thank Julie Collens and an anonymous reviewer for very helpful suggestions.

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Correspondence to Marc-André Lachance.

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Wardlaw, A.M., Berkers, T.E., Man, K.C. et al. Population structure of two beetle-associated yeasts: comparison of a New World asexual and an endemic Nearctic sexual species in the Metschnikowia clade. Antonie van Leeuwenhoek 96, 1–15 (2009). https://doi.org/10.1007/s10482-009-9330-y

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