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Reinforcement drives rapid allopatric speciation

Abstract

Allopatric speciation results from geographic isolation between populations. In the absence of gene flow, reproductive isolation arises gradually and incidentally as a result of mutation, genetic drift and the indirect effects of natural selection driving local adaptation1,2,3. In contrast, speciation by reinforcement is driven directly by natural selection against maladaptive hybridization1,4. This gives individuals that choose the traits of their own lineage greater fitness, potentially leading to rapid speciation between the lineages1,4. Reinforcing natural selection on a population of one of the lineages in a mosaic contact zone could also result in divergence of the population from the allopatric range of its own lineage outside the zone4,5,6. Here we test this with molecular data, experimental crosses, field measurements and mate choice experiments in a mosaic contact zone between two lineages of a rainforest frog. We show that reinforcing natural selection has resulted in significant premating isolation of a population in the contact zone not only from the other lineage but also, incidentally, from the closely related main range of its own lineage. Thus we show the potential for reinforcement to drive rapid allopatric speciation.

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Figure 1: Distribution of the N (pale shading) and S (dark shading) lineages of L. genimaculata.
Figure 2: Divergence in male body size across the mosaic contact zone.
Figure 3: Divergence in call across the mosaic contact zone.
Figure 4: Female choice of male calls at contacts A and B.

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Acknowledgements

We thank B. Phillips, J. MacKenzie, M. Tonione, J. Gardiner, M. Blows, J. Austin, M. Cunningham, H. McCallum, G. Dolman, S. Williams, H. Rundle, S. Chenoweth, A. Freeman, F. J. Rohlf and D. Wake. We are also grateful to B. Phillips and M. Cunningham for locating the contact zone. Supported by the National Science Foundation (C.M.), an Australian Postgraduate Award (C.J.H.), a University of Queensland Graduate School Research Travel Award (C.J.H.), the Cooperative Research Centre for Tropical Rainforest Ecology and Management (C.J.H.) and Queensland Parks and Wildlife Service.

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Correspondence to Conrad J. Hoskin.

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Competing interests

Sequences are deposited in the EMBL database under the following accession numbers: AF304205–AF304229 (ref. 11) and AJ872186–AJ872201. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Methods and Results

Details of the methods and analyses, and additional analyses and results not presented in the paper. The file is broken into sub-headings matching those in the ‘Methods’ section of the main paper. Included are 9 Supplementary Tables that present the results of ANCOVAs and contrasts referred to in the Supplementary Information. (DOC 109 kb)

Supplementary Figure 1

Map showing the sampling sites outside the contact region, and the lineage (N or S) of individuals at each site. (PDF 662 kb)

Supplementary Figure 2

Map showing the sampling sites across the mosaic contact zone, and the lineage (N, S/iS or mixed) of individuals at each site. (PDF 610 kb)

Supplementary Figure 3

Graph showing variation in male size in the southern lineage. The graph compares southern lineage males at Contact B (iS), at Contact A, and outside the contact region. (DOC 24 kb)

Supplementary Figure 4

Graph showing call variation in the southern lineage. The graph compares southern lineage males at Contact B (iS), at Contact A, and outside the contact region. (DOC 24 kb)

Supplementary Figure 5

Graph showing the relationship between call divergence and body size for N, S and iS. (DOC 25 kb)

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Hoskin, C., Higgie, M., McDonald, K. et al. Reinforcement drives rapid allopatric speciation. Nature 437, 1353–1356 (2005). https://doi.org/10.1038/nature04004

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