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Genomic divergence in a ring species complex

Nature volume 511, pages 83–85 (2014)Cite this article

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Abstract

Ring species provide particularly clear demonstrations of how one species can gradually evolve into two, but are rare in nature1,2,3. In the greenish warbler (Phylloscopus trochiloides) species complex, a ring of populations wraps around Tibet. Two reproductively isolated forms co-exist in central Siberia, with a gradient of genetic and phenotypic characteristics through the southern chain of populations connecting them4,5,6. Previous genetic evidence has proven inconclusive, however, regarding whether species divergence took place in the face of continuous gene flow and whether hybridization between the terminal forms of the ring ever occurred7,8,9. Here we use genome-wide analyses to show that, although spatial patterns of genetic variation are currently mostly as expected of a ring species, historical breaks in gene flow have existed at more than one location around the ring, and the two Siberian forms have occasionally interbred. Substantial periods of geographical isolation occurred not only in the north but also in the western Himalayas, where there is now an extensive hybrid zone between genetically divergent forms. Limited asymmetric introgression has occurred directly between the Siberian forms, although it has not caused a blending of those forms, suggesting selection against introgressed genes in the novel genetic background. Levels of reproductive isolation and genetic introgression are consistent with levels of phenotypic divergence around the ring, with phenotypic similarity and extensive interbreeding across the southwestern contact zone and strong phenotypic divergence and nearly complete reproductive isolation across the northern contact zone. These results cast doubt on the hypothesis that the greenish warbler should be viewed as a rare example of speciation by distance6, but demonstrate that the greenish warbler displays a continuum from slightly divergent neighbouring populations to almost fully reproductively isolated species.

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Figure 1: Spatial patterns of genetic differentiation within the greenish warbler ring species.

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Accession codes

Primary accessions

Sequence Read Archive

Data deposits

Raw Illumina sequencing data have been deposited in the Sequence Read Archive (SRA) under accession numbers SRX472921 and SRX473141. The list of contigs and information concerning the physical location of the SNP markers used in this study, using the zebra finch genome assembly as reference, have been deposited in the Dryad repository (http://doi.org/10.5061/dryad.6kn93).

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Acknowledgements

This research was supported by a Marie Curie International Outgoing Fellowship within the 7th European Community Framework Programme (project no. 273773) and an NSERC discovery grant (no. 311931). Original collections were made with a grant from the US NSF. We thank Z. Benowitz-Fredericks, J. Gibson, S. Gross, J. Irwin, G. Kelberg, A. Knorre, K. Marchetti and B. Sheldon for assistance in the field. For additional samples we thank P. Alström, K. Marchetti, U. Olsson, A. Richman and J. Tiainen. We thank J. Irwin and L. Rieseberg for comments and discussion and A. Kuzmin for assistance during library preparation.

Author information

Author notes

  1. irwin@zoology.ubc.ca

Authors and Affiliations

  1. Department of Zoology and Biodiversity Research Centre, University of British Columbia, 6270 University Boulevard, Vancouver, British Columbia V6T 1Z4, Canada,

    Miguel Alcaide & Darren E. Irwin

  2. Department of Evolutionary Ecology, Estación Biológica de Doñana – CSIC, Americo Vespucio s/n, 41092 Sevilla, Spain,

    Miguel Alcaide

  3. Department of Ecology and Evolution, University of Chicago, Chicago, 60637, Illinois, USA

    Elizabeth S. C. Scordato & Trevor D. Price

  4. Department of Ecology and Evolutionary Biology, The University of Colorado, Boulder, Colorado 80309, USA,

    Elizabeth S. C. Scordato

Authors
  1. Miguel Alcaide
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  2. Elizabeth S. C. Scordato
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  3. Trevor D. Price
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  4. Darren E. Irwin
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Contributions

M.A. and D.E.I. conceived the genomic study. M.A. designed the genomic analysis, and collected and analysed the sequence data. D.E.I., E.S.C.S. and T.D.P. conducted fieldwork. D.E.I. conducted the cline analysis in the southwestern contact zone. All authors contributed to the writing of the manuscript and have read and approved the manuscript.

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Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Sampled sites, geographical variation in SNPs and genetic admixtures.

a, Geographical distribution of the sites sampled in this study (see also Extended Data Table 1). Colours correspond to the six subspecies of greenish warblers described in ref. 15 (P.t. trochiloides, yellow; ludlowi, green; obscuratus, orange; nitidus, violet; viridanus, blue; plumbeitarsus, red). Greenish warblers coexisting in central Siberia were classified as viridanus or plumbeitarsus according to their mtDNA, which for males was perfectly concordant with their song4. b, Geographic variation in 2,334 SNP markers across 95 greenish warblers as summarized by PCA. Individual birds are depicted as diamonds and colours represent their geographical origin as shown in a. c, Plot of genetic admixture proportions (Q) according to the five genetic clusters inferred by the software STRUCTURE30. Location names are given in the plot. We also indicate whether a particular individual displays a western (W) or eastern (E) mtDNA haplotype according to ref. 4.

Extended Data Figure 2 Genetic differentiation based on SNP markers increases with corrected geographical distance around the ring.

See ref. 6 for geographical distance; Mantel’s r = 0.71, P < 0.0001. Pair-wise FST values were calculated among those locations where at least 4 individuals were genotyped (N = 8 locations; sites YK, TL, AA, PK, MN, LN, XN and UY, see Extended Data Fig. 1).

Source data

Extended Data Figure 3 Patterns of genetic differentiation among eight sample sites where at least four individuals were genotyped.

The thickness of the lines connecting locations is inversely proportional to the FST values between two given locations. Purple lines connect each population with its closest neighbour around the ring. FST pairwise values ranged from 0.034 to 0.303.

Source data

Extended Data Figure 4 Plots of genetic admixture proportions (Q) according to additional values of K.

Values of Q were inferred by the software STRUCTURE30. Colours are in agreement with those used to label each subspecies at the bottom of this figure.

Extended Data Table 1 Geographic origin of the 135 greenish warblers analysed in the present study
Full size table
Extended Data Table 2 Patterns of genetic diversity for each of the six subspecies of greenish warblers
Full size table
Extended Data Table 3 Number of markers (N) mapping to different avian chromosomes
Full size table

Supplementary information

Supplementary Information File 1

Genotypes of 95 greenish warblers for a selected set of 2,334 SNPs in GenAlex format. Individual IDs are displayed in the first column and SNP marker genotypes are displayed in two columns. Numerical codes and colours represent the four different nucleotide bases (A=101=red; C=102=blue; G=103=yellow; T=104=green). The bottom row indicates the chromosome (using the zebra finch genome assembly28 as reference) where each SNP marker is located. (XLSX 1543 kb)

Supplementary Information File 2

Genotypes of 4,018 polymorphic SNP markers across the greenish warbler range in a set of individuals sampled from Kyrgyzstan (site AA) to Nepal (site LN) that encompasses the entire sampled range of P.t ludlowi. The file is in GenAlex format, as described in SI File 1. (XLSX 1749 kb)

Supplementary Information File 3

Genotypes of greenish warblers for a set of highly differentiated markers (FST >0.85), grouped by chromosome, between viridanus and plumbeitarsus in GenAlex format. P. t. plumbeitarsus individuals with large chunks of DNA introgressing from viridanus are highlighted in yellow. Principal Coordinate Analyses for individual chromosomes are shown in the worksheet labeled as "PCAs". Here, individuals showing mixed ancestry are emphasized with blue squares. The ID of each individual is also given besides each PCA plot. Chromosomes without significant signal of introgression are also included for comparative purposes (e.g. ChrZ, Chr28 and Chr15). The position of each marker, using the zebra finch genome assembly as reference28, is indicated in the worksheet labeled as "Location". (XLSX 948 kb)

Supplementary Information File 4

Summary of the descriptive statistics derived from the Bayesian cluster analysis, as in STRUCTURE30, and generated by the program STRUCTURE Harvester32. (DOCX 164 kb)

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Alcaide, M., Scordato, E., Price, T. et al. Genomic divergence in a ring species complex. Nature 511, 83–85 (2014). https://doi.org/10.1038/nature13285

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