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Evolutionary genetics of Carpodacus mexicanus, a recently colonized host of a bacterial pathogen, Mycoplasma gallisepticum

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Abstract

We present molecular data documenting how introduction to the eastern United States and an epizootic involving a bacterial pathogen has affected the genetic diversity of house finches, a cardueline songbird. Population bottlenecks during introduction can cause loss of genetic variation and may negatively affect a population’s ability to adapt to novel stressors such as disease. Although a genome-wide survey using Amplified Fragment Length Polymorphism (AFLP) markers suggests little loss of genetic diversity in introduced populations, an epizootic of bacterial Mycoplasma has nonetheless caused dramatic declines in the eastern US population. Sequence analysis of a candidate gene for pathogen resistance in the Major Histocompatibity Complex (MHC) in pre- and post-epizootic population samples reveals allele frequency shifts since introduction of the pathogen, but similar shifts are also observed in control populations not exposed to the bacteria, and in a neutral non-coding locus. Expression studies using a novel subtractive hybridization approach indicate decreased expression of the class II MHC locus upon exposure to Mycoplasma, a pattern also seen in MHC class I loci in mice infected with cytomegalovirus and consistent with manipulation of the finch immune system by Mycoplasma. These results will be further expanded using experimental studies as well as examination of evolution of the pathogen genome itself.

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References

  • Abendroth A, Arvin A (1999) Varicella-zoster virus immune evasion. Immunol Rev 168:143–156

    Article  PubMed  CAS  Google Scholar 

  • Barton NH, Charlesworth B (1987) Genetic revolutions, founder effects and speciation. Annu Rev Ecol Syst 15:133–164

    Article  Google Scholar 

  • Benner WL (1991) Mitochondrial DNA variation in the house finch, Carpodacus mexicanus. Masters Thesis, University of Toronto

  • Case TJ, Bulger DT (1991) The role of interspecific competition in the biogeography of island lizards. Trends Ecol Evol 6:135–139

    Article  Google Scholar 

  • Clark A (1990) Inference of haplotypes from PCR-amplified samples of diploid populations. Mol Biol Evol 7(2):111–122

    PubMed  CAS  Google Scholar 

  • Clegg SM, Degnan SM, Kikkawa J, Moritz C, Estoup A, Owens IP (2002) Genetic consequences of sequential founder events by an island-colonizing bird. Proc Natl Acad Sci USA 99:8127–8132

    Article  PubMed  CAS  Google Scholar 

  • Dhondt AA, Tessaglia DL, Slothower RL (1998) Epidemic mycoplasmal conjunctivitis in house finches from Eastern North America. J Wildl Dis 34(2):265–280

    PubMed  CAS  Google Scholar 

  • Diatchenko L, Lau Y-FC, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD (1996) Suppression subtractive hybridization: A method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93(12):6025–6030

    Article  PubMed  CAS  Google Scholar 

  • Edwards SV, Dillon M (2004) Hitchhiking and recombination in birds: evidence from Mhc-linked and unlinked loci in Red-winged Blackbirds (Agelaius phoeniceus). Genet Res 84(3):175–192

    Article  PubMed  CAS  Google Scholar 

  • Edwards SV, Grahn M, Potts WK (1995) Dynamics of Mhc evolution in birds and crocodilians: amplification of class II genes with degenerate primers. Mol Ecol 4:719–729

    PubMed  CAS  Google Scholar 

  • Edwards SV, Hedrick PW (1998) Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 13:305–311

    Article  Google Scholar 

  • Edwards SV, Hess CM, Gasper J, Garrigan D (1999) Toward an evolutionary genomics of the avian Mhc. Immunol Rev 167:119–132

    Article  PubMed  CAS  Google Scholar 

  • Edwards SV, Nusser J, Gasper J (2000) Characterization and evolution of Mhc genes from non-model organisms, with examples from birds. In: Baker AJ (ed) Molecular methods in ecology. Cambridge, Blackwell Scientific, pp. 168–207

    Google Scholar 

  • Elliot JJ, Arbib RS (1953) Origin and status of the house finch in the eastern United States. Auk 70:31–37

    Google Scholar 

  • Farmer K, Hill G, Roberts SR (2002) Susceptibility of a naïve population of house finches to Mycoplasma gallisepticum. J Wildl Dis 38:282–286

    PubMed  Google Scholar 

  • Gilligan DM, Briscoe DA, Frankham R (2005) Comparative losses of quantitative and molecular geneticvariation in finite populations of Drosophila. Genet Res 85:47–55

    Article  PubMed  CAS  Google Scholar 

  • Grinnell J (1911) The linnet of the Hawaiian Islands: a problem in speciation. Univ Calif Publ Zool 7:179–195

    Google Scholar 

  • Hawley DM, Hanley D, Dhondt AA, Lovette IJ (2006) Molecular evidence for a founder effect in invasive house finch (Carpodacus mexicanus) populations experiencing an emergent disease epidemic. Mol Ecol 15:263–275

    Article  PubMed  CAS  Google Scholar 

  • Hedrick PW, Whittam TS, Parham P (1991) Heterozygosity at individual amino-acid sites––extremely high levels for HLA-A and HLA-B genes. Proc Natl Acad Sci USA 88:5897–5901

    Article  PubMed  CAS  Google Scholar 

  • Hengel H, Reusch U, Gutermann A, Ziegler H, Jonjic S, Lucin P, Koszinowski UH (1999) Cytomegaloviral control of MHC class I function in the mouse. Immunol Rev 168:167–176

    Article  PubMed  CAS  Google Scholar 

  • Hess CM, Edwards SV (2002) The evolution of the major histocompatibility complex in birds. BioScience 52(5):423–431

    Article  Google Scholar 

  • Hess CM, Gasper J, Hoekstra HE, Hill CE, Edwards SV (2000) MHC class II pseudogene and genomic signature of a 32-kb cosmid in the house finch (Carpodacus mexicanus). Genome Res 10(5):613–623

    Article  PubMed  CAS  Google Scholar 

  • Hill AVS (1991) HLA associations with malaria in Africa: some implications for MHC evolution. In: Klein J, Klein D (eds) Molecular evolution of the major histocompatibility complex. Springer-Verlag, Berlin, pp 403–420

    Google Scholar 

  • Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350(6316):337–339

    Article  Google Scholar 

  • Hill GE (1992) Proximate basis of variation in carotenoid pigmentation in male house finches. Auk 109(1):U1–12

    Google Scholar 

  • Hill GE (1993) House Finch (Carpodacus mexicanus). In: Poole A, Gill F (eds) The birds of North America. No. 46, Philadelphia: The Academy of Natural Sciences. The American Ornithologists’ Union, Washington, DC

  • Hill GE (1994) Geographic-variation in male ornamentation and female mate preference in the house finch––a comparative test of models of sexual selection. Behav Ecol 5(1):64–73

    Article  Google Scholar 

  • Hill GE (2000) Energetic constraints on expression of carotenoid-based plumage coloration. J of Avian Biol 31(4):559–566

    Article  Google Scholar 

  • Hill GE, Farmer KL, Beck ML (2004) The effect of mycoplasmosis on carotenoid plumage coloration in male house finches. J Exp Biol 207(12):2095–2099

    Article  PubMed  CAS  Google Scholar 

  • Hill GE, Montgomerie R (1994) Plumage color signals nutritional condition in the House Finch. Proc Royal Soc London Series B-Biol Sci 258(1351):47–52

    Article  Google Scholar 

  • Hill GE, Montgomerie R, Inouye CY, Dale J (1994) Influence of dietary carotenoids on plasma and plumage color in the House Finch––intrasexual and intersexual variation. Funct Ecology 8(3):343–350

    Article  Google Scholar 

  • Hill GE, Nolan PM, Stoehr AM (1999) Pairing success relative to male plumage redness and pigment symmetry in the house finch: temporal and geographic constancy. Behav Ecol 10(1):48–53

    Article  Google Scholar 

  • Hoelzel AR, Fleischer RC, Campagna C, LeBoeuf BJ, Alvord G (2002) Impact of a population bottleneck on symmetry and genetic diversity in the northern elephant seal. J Evol Biol 15:567–575

    Article  Google Scholar 

  • Hosseini PR, Dhondt AA, Dobson A (2004) Seasonality and wildlife disease: how seasonal birth, aggregation and variation in immunity affect the dynamics of Mycoplasma gallisepticum in house finches. Proc Royal Soc London Series B-Biol Sci 271(1557):2569–2577

    Article  Google Scholar 

  • Kaufman J, Göbel Milne S, Walker BA, Jacob JP, Auffrey C, Zoorob R, Beck S (1999) The chicken B locus is a minimal-essential major histocompatibility complex. Nature 401:923–925

    Article  CAS  Google Scholar 

  • Klein J (1986) Natural history of the major histocompatibility complex. Wiley, New York

    Google Scholar 

  • Leberg P (2002) Estimating allelic richness: Effects of sample size and bottlenecks. Mol Ecol 11:2445–2449

    Article  PubMed  CAS  Google Scholar 

  • Luttrell MP, Stallknecht DE, Fischer JR, Sewell CT, Kleven SH (1998) Natural Mycoplasma gallisepticum infection in a captive flock of house finches. J Wildl Dis 34:289–286

    PubMed  CAS  Google Scholar 

  • Luttrell MP, Fischer JR, Stallknecht DE, Kleven SH (1996) Field investigation of Mycoplasma gallisepticum infections in house finches (Carpodacus mexicanus) from Maryland and Georgia. Avian Dis 40:335–341

    Article  PubMed  CAS  Google Scholar 

  • National Audubon Society (2002) The Christmas bird count historical results (online). Available at: http://www.audubon.org/bird/cbc. Accessed January 2004

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) Bottleneck effect and genetic-variability in populations. Evolution 29(1):1–10

    Article  Google Scholar 

  • Pimental D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. BioScience 50(1):53–65

    Article  Google Scholar 

  • Reche PA, Reinherz EL (2003). Sequence variability analysis of human class I and class II MHC molecules: functional and structural correlates of amino acid polymorphisms. J Mol Biol 331:623–641

    Article  PubMed  CAS  Google Scholar 

  • Richman AD, Herrera LG, Nash D, Schierup MH (2003) Relative roles of mutation and recombination in generating allelic polymorphism at an MHC class II locus in Peromyscus maniculatus. Genet Res 82(2):89–99

    Article  PubMed  CAS  Google Scholar 

  • Roberts SR, Nolan PM, Lauerman LH, Li LQ, Hill GE (2001) Characterization of the mycoplasmal conjunctivitis epizootic in a house finch population in the southeastern USA. J Wildl Dis 37(1):82–88

    PubMed  CAS  Google Scholar 

  • Rozas J, Rozas R (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15(2):174–175

    Article  PubMed  CAS  Google Scholar 

  • Slatkin M (2004) A population-genetic test of founder effects and implications for Ashkenazi Jewish diseases. Am J Hum Genet 75(2):282–293

    Article  PubMed  CAS  Google Scholar 

  • Tajima F (1989) The effect of change in population-size on DNA polymorphism. Genetics 123(3):597–601

    PubMed  CAS  Google Scholar 

  • Vasquez-Phillips, MA (1992) Population differentiation of the house finch (Carpodacus mexcicanus) in North America and the Hawaiian Islands. Masters Thesis, University of Toronto

  • Wakenell PS, Miller MM, Goto RM, Gauderman WJ, Briles WE (1996) Association between the Rfp-Y haplotype and the incidence of Marek’s disease in chickens. Immunogenetics 44(4):242–5

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Baker AJ, Hill GE, Edwards SV (2003) Reconciling actual and infected population histories in the house finch (Carpodacus mexicanus) by AFLP analysis. Evolution 37(12):2852–2864

    Google Scholar 

  • Wang Z, Farmer K, Hill GE, Edwards SV (2006) A cDNA macroarray approach to parasite-induced gene expression changes in a songbird host: genetic response of house finches to experimental infection by Mycoplasma gallisepticum. Mol Ecol 15(5):1263–1273

    Article  PubMed  CAS  Google Scholar 

  • Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 11:141–160

    Article  Google Scholar 

  • Wenink PW, Groen AF, Roelke-Parker ME, Prins HHT (1998) African buffalo maintain high genetic diversity in the major histocompatibility complex in spite of historically known population bottlenecks. Mol Ecol 7(10):1315–1322

    Article  PubMed  CAS  Google Scholar 

  • Westerdahl H, Hansson B, Bensch S, Hasselquist D (2004) Between-year variation of MHC allele frequencies in great reed warblers: Selection or drift? J Evol Biol 17:485–492

    Article  PubMed  CAS  Google Scholar 

  • Zahavi, A (1997) The handicap principle: a missing piece of Darwin’s puzzle. Oxford University Press, New York

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Acknowledgements

We are thankful for early discussions on the ideas in this manuscript with Geoff Hill, Sharon Roberts, Kristy Farmer, Hollie Walsh, Monica Silva, Bethanne Zelano and Robb Brumfield. Paul Nolan helped greatly by filling out some of the sampling for post-exposure birds. Hollie Walsh made many helpful suggestions to improve the manuscript. This work was supported by NSF grant DEB (IRCEB) 0077804 to Geoff Hill, Sharon Roberts and SVE.

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Authors and Affiliations

  1. Department of Biology, University of Washington, Seattle, USA

    Christopher M. Hess

  2. Department of Biology, University of Portland, 5000 N. Williamette Blvd, Portland, OR, 97803-5798, USA

    Christopher M. Hess

  3. Department of Pharmacology, University of Washington, Seattle, USA

    Zhenshan Wang

  4. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, USA

    Scott V. Edwards

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  1. Christopher M. Hess
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  2. Zhenshan Wang
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Correspondence to Christopher M. Hess.

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Hess, C.M., Wang, Z. & Edwards, S.V. Evolutionary genetics of Carpodacus mexicanus, a recently colonized host of a bacterial pathogen, Mycoplasma gallisepticum . Genetica 129, 217–225 (2007). https://doi.org/10.1007/s10709-006-9016-6

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  • DOI: https://doi.org/10.1007/s10709-006-9016-6

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