Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis

  1. Jeffrey L. Feder,,
  2. Xianfa Xie,
  3. Juan Rull§,
  4. Sebastian Velez,
  5. Andrew Forbes,
  6. Brian Leung,,
  7. Hattie Dambroski,,
  8. Kenneth E. Filchak, and
  9. Martin Aluja§
  1. Department of Biological Sciences, University of Notre Dame, Galvin Life Science Center, P.O. Box 369, Notre Dame, IN 46556-0369; §Instituto de Ecología, Asociación Civil, Kilometro 2.5 Antigua Carretera a Coatepec 351, 91070 Xalapa, Veracruz, Mexico; Department of Biology, McGill School of Environment, McGill University, Montreal, QB, Canada H3A 1B1; and Cereal Disease Laboratory, United States Department of Agriculture, Agricultural Research Service, Midwest Area Office, University of Minnesota, 1551 Lindig Avenue, St. Paul, MN 55104

Abstract

The Rhagoletis pomonella sibling species complex is a model for sympatric speciation by means of host plant shifting. However, genetic variation aiding the sympatric radiation of the group in the United States may have geographic roots. Inversions on chromosomes 1-3 affecting diapause traits adapting flies to differences in host fruiting phenology appear to exist in the United States because of a series of secondary introgression events from Mexico. Here, we investigate whether these inverted regions of the genome may have subsequently evolved to become more recalcitrant to introgression relative to collinear regions, consistent with new models for chromosomal speciation. As predicted by the models, gene trees for six nuclear loci mapping to chromosomes other than 1-3 tended to have shallower node depths separating Mexican and U.S. haplotypes relative to an outgroup sequence than nine genes residing on chromosomes 1-3. We discuss the implications of secondary contact and differential introgression with respect to sympatric host race formation and speciation in Rhagoletis, reconciling some of the seemingly dichotomous views of Mayr, Dobzhansky, and Bush concerning modes of divergence.

Footnotes

  • To whom correspondence should be addressed. E-mail: feder.2{at}nd.edu.

  • This paper results from the Arthur M. Sackler Colloquium of the National Academy of Sciences, “Systematics and the Origin of Species: On Ernst Mayr's 100th Anniversary,” held December 16-18, 2004, at the Arnold and Mabel Beckman Center of the National Academies of Science and Engineering in Irvine, CA.

  • Abbreviations: Mya, million years ago; ML, maximum likelihood; MP, maximum parsimony; RND, relative node depth.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. AY152477-AY152526 and AY930466-AY931013).

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