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United States Department of Agriculture

Agricultural Research Service

Research Project: Sustainable Vineyard Production Systems Title: Evolutionary consequences of putative intra- and interspecific hybridization in agaric fungi

Authors
item Hughes, Karen -
item Peterson, Ronald -
item Lodge, D Jean -
item Bergemann, Sarah -
item Baumgartner, Kendra
item Tulloss, Rodham -
item Lickey, E -
item Cifuentes, Joaquin -

Submitted to: Mycologia
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: March 15, 2013
Publication Date: August 8, 2013
Repository URL: http://www.mycologia.org/content/105/6/1577.abstract
Citation: Hughes, K.W., Peterson, R.H., Lodge, D., Bergemann, S.E., Baumgartner, K., Tulloss, R.E., Lickey, E., Cifuentes, J. 2013. Evolutionary consequences of putative intra- and interspecific hybridization in agaric fungi. Mycologia. 105:1577-1594.

Interpretive Summary: Mushrooms of the Great Smoky Mountains National Park of the southern Appalachians are often heterozygous for the rDNA internal transcribed spacer region (ITS) with >42% of collections showing some level of heterozygosity for indels and/or base-pair substitutions. For such species, intra-individual haplotype divergence is typically less than 2%, but for 3% of these collections, intra-individual haplotype divergence exceeds that figure. We hypothesize that high intra-individual haplotype divergence is due to hybridization between parental populations with divergent haplotypes, perhaps migrants from geographically-isolated glacial refugia. Four species with relatively high haplotype divergence were examined: Armillaria mellea, Amanita citrina f. lavendula, Gymnopus dichrous, and the Hygrocybe flavescens/ chlorophana complex. The ITS region was sequenced, haplotypes of heterozygotes were resolved through cloning, and phylogenetic analyses were used to determine the outcome of hybridization events. Within A. mellea and A. citrina f. lavendula, we found evidence of interbreeding and recombination. In G. dichrous and H. flavescens/ chlorophana, hybrids were identified, but there is no evidence for F2 or higher progeny in natural populations suggesting that the hybrid fruitbodies may be an evolutionary dead end and that the genetically divergent Mendelian populations from which they were derived are in fact separate species. The association between levels of ITS haplotype divergence of less than 5% (A. mellea = 2.59% excluding gaps; A. citrina f. lavendula = 3.27%) with the presence of putative recombinants, and greater than 5% (G. dichrous=5.68%; H. flavescens/ chlorophana=14.07%) with apparent failure of F1 hybrids to produce F2 or higher progeny in nature may suggest a generalized correlation between genetic distance and reproductive isolation.

Technical Abstract: Agaric fungi of the southern Appalachians including the Great Smoky Mountains National Park are often heterozygous for the rDNA internal transcribed spacer region (ITS) with >42% of collections showing some level of heterozygosity for indels and/or base-pair substitutions. For these collections, intra-individual haplotype divergence is typically less than 2%, but for 3% of these collections, intra-individual haplotype divergence exceeds that figure. We hypothesize that high intra-individual haplotype divergence is due to hybridization between agaric fungi with divergent haplotypes, perhaps migrants from geographically isolated glacial refugia. Four species with relatively high haplotype divergence were examined: Armillaria mellea, Amanita citrina f. lavendula, Gymnopus dichrous, and the Hygrocybe flavescens/ chlorophana complex. The ITS region was sequenced, haplotypes of heterozygotes were resolved through cloning, and phylogenetic analyses were used to determine the outcome of hybridization events. Within A. mellea and A. citrina f. lavendula, we found evidence of interbreeding and recombination. In G. dichrous and H. flavescens/ chlorophana, hybrids were identified, but there is no evidence for F2 or higher progeny in natural populations suggesting that the hybrid fruitbodies may be an evolutionary dead end and that the genetically divergent Mendelian populations from which they were derived are in fact separate species. The association between levels of ITS haplotype divergence of less than 5% (A. mellea = 2.59% excluding gaps; A. citrina f. lavendula = 3.27%) with the presence of putative recombinants, and greater than 5% (G. dichrous=5.68%; H. flavescens/ chlorophana=14.07%) with apparent failure of F1 hybrids to produce F2 or higher progeny in nature may suggest a generalized correlation between genetic distance and reproductive isolation.

Last Modified: 10/24/2014
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