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Inferences about the origin of a field cricket hybrid zone from a mitochondrial DNA phylogeny

Abstract

Two closely related eastern North American field crickets, Gryllus firmus and G. pennsylvanicus, hybridize along a zone that extends from Connecticut and the Hudson River Valley, south along the eastern front of the Appalachian Mountains to at least Virginia. Here we use mitochondrial DNA (mtDNA) sequences to construct a population phylogeny for this pair of hybridizing cricket species. Using a phylogenetic approach, we attempt to discriminate between alternative population histories (secondary contact vs. primary intergradation) leading to formation of the hybrid zone. A strict consensus tree, based on > 1600 bp of the COI-COII region of the mtDNA genome, reveals four exclusive groups, which correspond to regional groupings of conspecific crickets. Surprisingly, the mtDNA sequence data do not reveal any synapomorphies for either G. pennsylvanicus or G. firmus. However, the mtDNA data do reveal a clear north-south split within each of the cricket species, a pattern not seen for morphological or other molecular characters. The biogeographical history of the north-south divergence events remains a puzzle. Observed gene genealogies support a model of secondary contact for the southern part of the hybrid zone. Sequence divergence data argue that lineages currently found in New York and New England were already distinct when this region became habitable following the most recent glaciation.

References

  • Avise, J C, Neigel, J E, and Arnold, J. 1984. Demographic influences on mitochondrial DNA lineage survivorship in animal populations. J Mol Evol, 20, 99–105.

    CAS  Article  Google Scholar 

  • Barton, N H, and Hewitt, G M. 1985. Analysis of hybrid zones. Ann Rev Ecol Syst, 16, 113–148.

    Article  Google Scholar 

  • Brower, A V Z. 1994. Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc Natl Acad Sci USA, 91, 6491–6495.

    CAS  Article  Google Scholar 

  • Brower, A V Z. 1996. Parallel race formation and the evolution of mimicry in Heliconius butterflies: a phylogenetic hypothesis from mitochondrial DNA sequences. Evolution, 5, 195–221.

    Article  Google Scholar 

  • Brown, J M, Pellmyr, O, Thompson, J N, and Harrison, R O. 1994. Phylogeny of Greya (Lepidoptera: Prodoxidae), based on nucleotide sequence variation in mitochondrial cytochrome oxidase I and II: congruence with morphological data. Mol Biol Evol, 11, 128–141.

    CAS  Google Scholar 

  • Clary, D O, and Wolstenhome, D R. 1985. The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol, 22, 252–272.

    CAS  Article  Google Scholar 

  • Cooper, S J B, and Hewitt, G M. 1993. Nuclear DNA sequence divergence between parapatric subspecies of the grasshopper Chorthippus parallelus. Insect Mol Biol, 2, 185–194.

    CAS  Article  Google Scholar 

  • Cooper, S J B, Ibrahim, K M, and Hewitt, G M. 1995. Postglacial expansion and genome subdivision in the European grasshopper Chorthippus parallelus. Mol Ecol, 4, 49–60.

    CAS  Article  Google Scholar 

  • Crandall, K A, and Templeton, A R. 1993. Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics, 134, 959–969.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Davis, M B. 1976. Pleistocene biogeography of temperate deciduous forests. Geosci and Man, 13, 13–26.

    Google Scholar 

  • Dyke, A S, and Prest, V K. 1987. Late Wisconsinan and Holocene history of the Laurentide ice sheet. Geogr Phys Quaternaire, 41, 237–264.

    Article  Google Scholar 

  • Endler, J A. 1977. Geographic Variation, Speciation, and Clines. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Harrison, R G. 1983. Barriers to gene exchange between closely related species. I. Laboratory hybridization studies. Evolution, 37, 245–251.

    Article  Google Scholar 

  • Harrison, R G. 1986. Pattern and process in a narrow hybrid zone. Heredity, 56, 337–349.

    Article  Google Scholar 

  • Harrison, R G. 1990. Hybrid zones: windows on evolutionary process. In Futuyma, D. and Antonovics, J. (eds) Oxford Surveys in Evolutionary Biology, 7, 69–128. Oxford University Press, Oxford.

    Google Scholar 

  • Harrison, R G, and Arnold, J. 1982. A narrow hybrid zone between closely related cricket species. Evolution, 36, 535–552.

    Article  Google Scholar 

  • Harrison, R G, and Rand, D M. 1989. Mosaic hybrid zones and the nature of species boundaries. In: Otte, D. and Endler, J. A. (eds) Speciation and Its Consequences, pp. 111–133. Sinauer, Sunderland, MA.

    Google Scholar 

  • Harrison, R G, and Bogdanowicz, S M. 1995. Mitochondrial phylogeny of North American field crickets: perspectives on the evolution of life cycles, songs and habitat associations. J Evol Biol, 8, 209–232.

    CAS  Article  Google Scholar 

  • Harrison, R G, and Bogdanowicz, S M. 1997. Patterns of variation and linkage disequilibrium in a field cricket hybrid zone. Evolution, 51, 493–505.

    CAS  Article  Google Scholar 

  • Harrison, R G, Rand, D M, and Wheeler, W C. 1987. Mitochondrial DNA variation in field crickets across a narrow hybrid zone. Mol Biol Evol, 4, 144–158.

    CAS  Google Scholar 

  • Higuchi, R, and Ochman, H. 1989. Production of single-stranded DNA templates by exonuclease digestion following the polymerase chain reaction Nucl Acids Res, 17, 5865.

    CAS  Article  Google Scholar 

  • Liu, H, and Beckenbach, A T. 1992. Evolution of the mitochondrial cytochrome oxidase II gene among 10 orders of insects. Mol Phytogen Evol, 1, 41–52.

    CAS  Article  Google Scholar 

  • Maddison, W P, and Maddison, D R. 1992. MACCLADE 3.0. Analysis of Phylogeny and Character Evolution. Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Maxwell, J A, and Davis, M B. 1972. Pollen evidence of Pleistocene and Holocene vegetation on the Allegheny Plateau, Maryland. Quarternary Res, 2, 506–530.

    Article  Google Scholar 

  • Mayr, E. 1942. Systematics and the Origin of Species Columbia University Press, New York.

    Google Scholar 

  • Nachman, M W, Boyer, S N, Searle, J B, and Aquadro, C F. 1994. Mitochondrial DNA variation and the evolution of Robertsonian chromosomal races of house mice, Mus domesticus. Genetics, 136, 1105–1120.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Neigel, J E, and Avise, J C. 1986. Phylogenetic relationships of mitochondrial DNA under various demographic models of speciation. In: Karlin, S. and Nevo, E. (eds) Evolutionary Processes and Theory, pp. 515–534. Academic Press, New York.

    Chapter  Google Scholar 

  • Patton, J L, and Smith, M F. 1992. MtDNA phylogeny of Andean mice: a test of diversification across ecological gradients. Evolution, 46, 174–183.

    CAS  PubMed  Google Scholar 

  • Patton, J L, Da Silva, M N F, and Malcolm, J R. 1994. Gene genealogy and differentiation among arboreal spiny rats (Rodentia: Echimyidae) of the Amazon Basin: a test of the riverine barrier hypothesis. Evolution, 48, 1314–1323.

    Article  Google Scholar 

  • Rand, D M, and Harrison, R O. 1989. Ecological genetics of a mosaic hybrid zone: mitochondrial, nuclear and reproductive differentiation of crickets by soil type. Evolution, 43, 432–449.

    Article  Google Scholar 

  • Simon, C, Frati, F, Beckenbach, A, Liu, H, and Floor, P. 1994. Evolution, weighting and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am, 87, 651–701.

    CAS  Article  Google Scholar 

  • Swofford, D L. 1993. PAUP 3.1.1. Illnois Natural History Survey, Champaign, IL.

  • Watts, W A. 1979. Late Quaternary vegetation of central Appalachia and the New Jersey coastal plain. Ecol Monogr, 49, 427–469.

    Article  Google Scholar 

  • Watts, W A. 1983. Vegetational history of the eastern United States 25,000 to 10,000 years ago. In: Porter, S. C. (ed.) Late-Quarternary Environments of the United States, Vol. 1, The Late Pleistocene, pp. 294–310. University of Minnesota Press, Minneapolis, MN.

    Google Scholar 

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Correspondence to Richard G Harrison.

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Willett, C., Ford, M. & Harrison, R. Inferences about the origin of a field cricket hybrid zone from a mitochondrial DNA phylogeny. Heredity 79, 484–494 (1997). https://doi.org/10.1038/hdy.1997.188

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  • DOI: https://doi.org/10.1038/hdy.1997.188

Keywords

  • crickets
  • gene genealogy
  • Gryllus
  • hybrid zone
  • mitochondrial DNA
  • secondary contact

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