Host shift to an invasive plant triggers rapid animal hybrid speciation

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Abstract

Speciation in animals is almost always envisioned as the split of an existing lineage into an ancestral and a derived species. An alternative speciation route is homoploid hybrid speciation1 in which two ancestral taxa give rise to a third, derived, species by hybridization without a change in chromosome number. Although theoretically possible it has been regarded as rare1 and hence of little importance in animals. On the basis of molecular and chromosomal evidence, hybridization is the best explanation for the origin of a handful of extant diploid bisexual animal taxa2,3,4,5,6. Here we report the first case in which hybridization between two host-specific animals (tephritid fruitflies) is clearly associated with the shift to a new resource. Such a hybrid host shift presents an ecologically robust scenario for animal hybrid speciation because it offers a potential mechanism for reproductive isolation through differential adaptation to a new ecological niche7. The necessary conditions for this mechanism of speciation7 are common in parasitic animals, which represent much of animal diversity8. The frequency of homoploid hybrid speciation in animals may therefore be higher than previously assumed.

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Figure 1: Allele frequencies at hybrid diagnostic nuclear and mitochondrial loci in Lonicera fly and parental populations from central Pennsylvania.
Figure 2: Assignment of ancestry from two parental populations to individuals of the Lonicera fly and its parents.
Figure 3: Posterior probability for the assignment of observed Lonicera fly individuals as F1 hybrids between R. mendax and R. zephyria.

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Acknowledgements

We thank K. Shoemaker and A. Forbes for technical assistance, G. Yatskievich for plant identifications, O. Bjørnstad for comments on the manuscript and help with probability models, and J. Smith, S. Berlocher and L. Rieseberg for comments on the manuscript. Partial funding for this study came from the Pennsylvania Agricultural Experiment Station, the Herbert E. Longenecker Student Research Endowment and the National Science Foundation.

Author information

Correspondence to Dietmar Schwarz.

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Competing interests

The mtDNA COII sequences from the populations of R. mendax, R. zephyria and the Lonicera fly were submitted to GenBank with accession numbers AY846885–AY847000 and AY847015–AY847031. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

Additional background information on the Rhagoletis pomonella species group; preliminary information on the geographic distribution of the Lonicera fly; and methodology and results of additional data analyses. (DOC 89 kb)

Supplementary Table S1

Literature sources for allozyme data in Table 1 (main text). (DOC 44 kb)

Supplementary Table S2

Allele frequencies at nuclear loci for the Lonicera fly and its parent taxa. (DOC 142 kb)

Supplementary Table S3

Permutation test for deviations from Hardy-Weinberg equilibrium in Lonicera fly populations. (DOC 41 kb)

Supplementary Table S4

Permutation test for deviations from pairwise linkage equilibrium between allozymes in Lonicera Fly State College. (DOC 28 kb)

Supplementary Figure S1

Posterior probability for the assignment of observed Lonicera fly individuals to different hybrid classes that result from two generations of hybridization between R. mendax and R. zephyria. (PDF 135 kb)

Supplementary Figure S2

Comparison of allele frequencies for the most common allele in the Lonicera fly between R. mendax, the Lonicera fly and R. zephyria at seven nuclear loci. (PDF 110 kb)

Supplementary Figure S3

Decay of expected admixture linkage disequilibrium between Aat-2 and Idh in the Lonicera fly under the hybrid-isolation model. (PDF 81 kb)

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Schwarz, D., Matta, B., Shakir-Botteri, N. et al. Host shift to an invasive plant triggers rapid animal hybrid speciation. Nature 436, 546–549 (2005) doi:10.1038/nature03800

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