• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Apr 2004; 166(4): 1611–1629.
PMCID: PMC1470819

Recombination and migration of Cryphonectria hypovirus 1 as inferred from gene genealogies and the coalescent.

Abstract

Genealogy-based methods were used to estimate migration of the fungal virus Cryphonectria hypovirus 1 between vegetative compatibility types of the host fungus, Cryphonectria parasitica, as a means of estimating horizontal transmission within two host populations. Vegetative incompatibility is a self/non-self recognition system that inhibits virus transmission under laboratory conditions but its effect on transmission in nature has not been clearly demonstrated. Recombination within and among different loci in the virus genome restricted the genealogical analyses to haplotypes with common mutation and recombinational histories. The existence of recombination necessitated that we also use genealogical approaches that can take advantage of both the mutation and recombinational histories of the sample. Virus migration between populations was significantly restricted. In contrast, estimates of migration between vegetative compatibility types were relatively high within populations despite previous evidence that transmission in the laboratory was restricted. The discordance between laboratory estimates and migration estimates from natural populations highlights the challenges in estimating pathogen transmission rates. Genealogical analyses inferred migration patterns throughout the entire coalescent history of one viral region in natural populations and not just recent patterns of migration or laboratory transmission. This application of genealogical analyses provides markedly stronger inferences on overall transmission rates than laboratory estimates do.

Full Text

The Full Text of this article is available as a PDF (381K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Anagnostakis SL. Biological control of chestnut blight. Science. 1982 Jan 29;215(4532):466–471. [PubMed]
  • Anderson RM, May RM. The invasion, persistence and spread of infectious diseases within animal and plant communities. Philos Trans R Soc Lond B Biol Sci. 1986 Dec 15;314(1167):533–570. [PubMed]
  • Bahlo M, Griffiths RC. Inference from gene trees in a subdivided population. Theor Popul Biol. 2000 Mar;57(2):79–95. [PubMed]
  • Beerli P, Felsenstein J. Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics. 1999 Jun;152(2):763–773. [PMC free article] [PubMed]
  • Beerli P, Felsenstein J. Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci U S A. 2001 Apr 10;98(8):4563–4568. [PMC free article] [PubMed]
  • Biella Silvia, Smith Myron L, Aist James R, Cortesi Paolo, Milgroom Michael G. Programmed cell death correlates with virus transmission in a filamentous fungus. Proc Biol Sci. 2002 Nov 7;269(1506):2269–2276. [PMC free article] [PubMed]
  • Bruyere A, Wantroba M, Flasinski S, Dzianott A, Bujarski JJ. Frequent homologous recombination events between molecules of one RNA component in a multipartite RNA virus. J Virol. 2000 May;74(9):4214–4219. [PMC free article] [PubMed]
  • Carbone I, Kohn LM. A microbial population-species interface: nested cladistic and coalescent inference with multilocus data. Mol Ecol. 2001 Apr;10(4):947–964. [PubMed]
  • Carbone I, Kohn LM. Multilocus nested haplotype networks extended with DNA fingerprints show common origin and fine-scale, ongoing genetic divergence in a wild microbial metapopulation. Mol Ecol. 2001 Oct;10(10):2409–2422. [PubMed]
  • Caten CE. Vegetative incompatibility and cytoplasmic infection in fungi. J Gen Microbiol. 1972 Sep;72(2):221–229. [PubMed]
  • Congdon BC, Piatt JF, Martin K, Friesen VL. Mechanisms of population differentiation in marbled murrelets: historical versus contemporary processes. Evolution. 2000 Jun;54(3):974–986. [PubMed]
  • Cortesi P, Milgroom MG. Genetics of vegetative incompatibility in cryphonectria parasitica . Appl Environ Microbiol. 1998 Aug;64(8):2988–2994. [PMC free article] [PubMed]
  • Cortesi P, McCulloch CE, Song H, Lin H, Milgroom MG. Genetic control of horizontal virus transmission in the chestnut blight fungus, Cryphonectria parasitica. Genetics. 2001 Sep;159(1):107–118. [PMC free article] [PubMed]
  • Daly MJ, Rioux JD, Schaffner SF, Hudson TJ, Lander ES. High-resolution haplotype structure in the human genome. Nat Genet. 2001 Oct;29(2):229–232. [PubMed]
  • Fahima T, Kazmierczak P, Hansen DR, Pfeiffer P, Van Alfen NK. Membrane-associated replication of an unencapsidated double-strand RNA of the fungus, Cryphonectria parasitica. Virology. 1993 Jul;195(1):81–89. [PubMed]
  • Fearnhead P, Donnelly P. Estimating recombination rates from population genetic data. Genetics. 2001 Nov;159(3):1299–1318. [PMC free article] [PubMed]
  • Fu YX. New statistical tests of neutrality for DNA samples from a population. Genetics. 1996 May;143(1):557–570. [PMC free article] [PubMed]
  • Liu Y-C, Linder-Basso D, Hillman BI, Kaneko S, Milgroom MG. Evidence for interspecies transmission of viruses in natural populations of filamentous fungi in the genus Cryphonectria. Mol Ecol. 2003 Jun;12(6):1619–1628. [PubMed]
  • Fu YX, Li WH. Statistical tests of neutrality of mutations. Genetics. 1993 Mar;133(3):693–709. [PMC free article] [PubMed]
  • Gabriel Stacey B, Schaffner Stephen F, Nguyen Huy, Moore Jamie M, Roy Jessica, Blumenstiel Brendan, Higgins John, DeFelice Matthew, Lochner Amy, Faggart Maura, et al. The structure of haplotype blocks in the human genome. Science. 2002 Jun 21;296(5576):2225–2229. [PubMed]
  • Milgroom MG, Cortesi P. Analysis of population structure of the chestnut blight fungus based on vegetative incompatibility genotypes. Proc Natl Acad Sci U S A. 1999 Aug 31;96(18):10518–10523. [PMC free article] [PubMed]
  • Griffiths RC, Marjoram P. Ancestral inference from samples of DNA sequences with recombination. J Comput Biol. 1996 Winter;3(4):479–502. [PubMed]
  • Hartl DL, Dempster ER, Brown SW. Adaptive significance of vegetative incompatibility in Neurospora crassa. Genetics. 1975 Nov;81(3):553–569. [PMC free article] [PubMed]
  • Heath Daniel D, Busch Christopher, Kelly Joanne, Atagi Dana Y. Temporal change in genetic structure and effective population size in steelhead trout (Oncorhynchus mykiss). Mol Ecol. 2002 Feb;11(2):197–214. [PubMed]
  • Myers Simon R, Griffiths Robert C. Bounds on the minimum number of recombination events in a sample history. Genetics. 2003 Jan;163(1):375–394. [PMC free article] [PubMed]
  • Hein J. Reconstructing evolution of sequences subject to recombination using parsimony. Math Biosci. 1990 Mar;98(2):185–200. [PubMed]
  • Neuhauser C, Krone SM. The genealogy of samples in models with selection. Genetics. 1997 Feb;145(2):519–534. [PMC free article] [PubMed]
  • Hey J, Wakeley J. A coalescent estimator of the population recombination rate. Genetics. 1997 Mar;145(3):833–846. [PMC free article] [PubMed]
  • Nielsen R, Wakeley J. Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics. 2001 Jun;158(2):885–896. [PMC free article] [PubMed]
  • Nuss DL. Biological control of chestnut blight: an example of virus-mediated attenuation of fungal pathogenesis. Microbiol Rev. 1992 Dec;56(4):561–576. [PMC free article] [PubMed]
  • Hillman BI, Tian Y, Bedker PJ, Brown MP. A North American hypovirulent isolate of the chestnut blight fungus with European isolate-related dsRNA. J Gen Virol. 1992 Mar;73(Pt 3):681–686. [PubMed]
  • Peever TL, Liu YC, Cortesi P, Milgroom MG. Variation in tolerance and virulence in the chestnut blight fungus-hypovirus interaction. Appl Environ Microbiol. 2000 Nov;66(11):4863–4869. [PMC free article] [PubMed]
  • Hudson RR, Slatkin M, Maddison WP. Estimation of levels of gene flow from DNA sequence data. Genetics. 1992 Oct;132(2):583–589. [PMC free article] [PubMed]
  • Jakobsen IB, Wilson SR, Easteal S. The partition matrix: exploring variable phylogenetic signals along nucleotide sequence alignments. Mol Biol Evol. 1997 May;14(5):474–484. [PubMed]
  • Rozas J, Rozas R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics. 1999 Feb;15(2):174–175. [PubMed]
  • Kils-Hütten L, Cheynier R, Wain-Hobson S, Meyerhans A. Phylogenetic reconstruction of intrapatient evolution of human immunodeficiency virus type 1: predominance of drift and purifying selection. J Gen Virol. 2001 Jul;82(Pt 7):1621–1627. [PubMed]
  • Kinnison MT, Bentzen P, Unwin MJ, Quinn TP. Reconstructing recent divergence: evaluating nonequilibrium population structure in New Zealand chinook salmon. Mol Ecol. 2002 Apr;11(4):739–754. [PubMed]
  • Koonin EV, Choi GH, Nuss DL, Shapira R, Carrington JC. Evidence for common ancestry of a chestnut blight hypovirulence-associated double-stranded RNA and a group of positive-strand RNA plant viruses. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10647–10651. [PMC free article] [PubMed]
  • Levin BR. The evolution and maintenance of virulence in microparasites. Emerg Infect Dis. 1996 Apr-Jun;2(2):93–102. [PMC free article] [PubMed]
  • Stumpf Michael P H. Haplotype diversity and the block structure of linkage disequilibrium. Trends Genet. 2002 May;18(5):226–228. [PubMed]
  • Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. [PMC free article] [PubMed]
  • Templeton AR. Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol Ecol. 1998 Apr;7(4):381–397. [PubMed]
  • Vitalis R, Couvet D. Estimation of effective population size and migration rate from one- and two-locus identity measures. Genetics. 2001 Feb;157(2):911–925. [PMC free article] [PubMed]
  • Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. [PMC free article] [PubMed]
  • Wakeley J, Aliacar N. Gene genealogies in a metapopulation. Genetics. 2001 Oct;159(2):893–905. [PMC free article] [PubMed]
  • Watterson GA. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975 Apr;7(2):256–276. [PubMed]
  • Van Alfen NK, Jaynes RA, Anagnostakis SL, Day PR. Chestnut Blight: Biological Control by Transmissible Hypovirulence in Endothia parasitica. Science. 1975 Sep 12;189(4206):890–891. [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...