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Female-biased gene flow between two species of Darwin’s finches

Nature Ecology & Evolution volume 4, pages 979–986 (2020)Cite this article

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Abstract

The mosaic nature of hybrid genomes is well recognized, but little is known of how they are shaped initially by patterns of breeding, selection, recombination and differential incompatibilities. On the small Galápagos island of Daphne Major, two species of Darwin’s finches, Geospiza fortis and G. scandens, hybridize rarely and back-cross bidirectionally with little or no loss of fitness under conditions of plentiful food. We used whole-genome sequences to compare genomes from periods before and after successful interbreeding followed by back-crossing. We inferred extensive introgression from G. fortis to G. scandens on autosomes and mitochondria but not on the Z chromosome. The unique combination of long-term field observations and genomic data shows that the reduction of gene flow for Z-linked loci primarily reflects female-biased gene flow, arising from a hybrid-male disadvantage in competition for high-quality territories and mates, rather than from genetic incompatibilities at Z-linked loci.

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Fig. 1: Changes in morphology and introgression.
Fig. 2: Introgression between G. fortis and G. scandens.
Fig. 3: Differentiation across the genome and at ALX1.
Fig. 4: Genomic regions resistant to gene flow.

Data availability

The Illumina reads have been submitted to the short reads archive (http://www.ncbi.nlm.nih.gov/sra) under accession number PRJNA530015. The following figures have associated raw data: Fig. 1a,b and Extended Data Fig. 1. The raw data are available in Supplementary Table 1.

Code availability

The analyses of the data were carried out with publicly available software, and all are cited in the Methods. The custom scripts used are available at https://github.com/sangeet2019/Darwins-Finches.

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Acknowledgements

We thank U. Gustafson for expert wet laboratory assistance and E. Enbody for helpful discussion on the manuscript. The collection of the material, funded by the National Science Foundation (NSF), was conducted with annual permits from the Galápagos National Parks Directorate, with the approval of Princeton University’s Animal Care Committee and in accordance with its protocols, and supported logistically by the Charles Darwin Research Station in Galápagos. The project was supported by Vetenskapsrådet and Knut and Alice Wallenberg Foundation. The genome sequencing was performed by the SNP&SEQ Technology Platform, supported by Uppsala University and SciLifeLab. Computer resources for the bioinformatics analysis were supplied by the Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX).

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Author notes

  1. Sangeet Lamichhaney

    Present address: Department of Biological Sciences, Kent State University, Kent, OH, USA

  2. These authors contributed equally: Sangeet Lamichhaney, Fan Han.

Authors and Affiliations

  1. Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden

    Sangeet Lamichhaney, Fan Han, Matthew T. Webster & Leif Andersson

  2. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA

    B. Rosemary Grant & Peter R. Grant

  3. Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, Uppsala, Sweden

    Leif Andersson

  4. Department of Veterinary Integrative Biosciences, Texas A&M University, College Station, TX, USA

    Leif Andersson

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Contributions

P.R.G. and B.R.G. collected the material. L.A., P.R.G. and B.R.G. conceived the study. L.A. and M.T.W. led the bioinformatic analysis of the data. S.L. and F.H. performed the bioinformatic analysis and experimental work. L.A., S.L., F.H., B.R.G. and P.R.G. wrote the paper with input from the other authors. All authors approved the manuscript before submission.

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Correspondence to Leif Andersson.

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Extended data

Extended Data Fig. 1

Beak length and beak depth in six groups of G. scandens and G. fortis population, based on data presented in Supplementary Table 1.

Extended Data Fig. 2 Beak size (PC1) and beak shape (PC2) of the six groups of finches.

In a Principal Components analysis of beak length, depth and width of all individuals, 30 per group (29 only for early G. fortis), PC1 explained 64.5% of the variation and PC2 explained an additional 31.4%. The combined groups were heterogeneous in PC1 (F5,173 = 27.6, P < 0.0001) and PC2 scores (F5,173 = 497.3, P < 0.0001), more strongly in PC2 (adj R2 = 0.93) than in PC1 (adj R2 = 0.43). All pairwise differences in PC2 scores between groups of the same species are statistically significant at P < 0.0001, except for G. scandens early and late pointed groups at P = 0.02. The two groups that contain putatively introgressed individuals, G. fortis late pointed and G. scandens late blunt, do not differ in beak shape (P = 0.72).

Extended Data Fig. 3

Allele frequency of a diagnostic SNP at nucleotide position 16,851 in mtDNA in different groups of G. scandens and G. fortis from Daphne Major.

Extended Data Fig. 4 Normalized genetic distance in four late groups of Darwin’s finches along chromosomes 1, 4 and Z.

Nei’s genetic distance of every 50 kb non-overlapping window was calculated across the genome and only the windows showing relatively high divergence between the early groups (delta genetic distance > 0.15) are presented. Each value was normalized by the difference of the genetic distances between the G. scandens early pointed (SEP) and G. fortis early blunt (FEB) groups.

Extended Data Fig. 5 Density of allele frequencies and their correlation among six groups of Darwin’s finches.

(a) Density of allele frequency in each group across autosomes and (b) on the Z chromosome; the peak density is marked with a dashed blue line. (c) Pairwise correlation of allele frequencies among groups on autosomes and (d) on the Z chromosome. Correlation coefficients were calculated using Pearson’s correlation test, and all the values were below a significance level of 0.01.

Extended Data Fig. 6

Relative degree of introgression in G. scandens late blunt Delta FST(SLB) and G. scandens late pointed Delta FST(SLP) along the genome.

Extended Data Fig. 7

Correlation between two delta FST measures on each chromosome, and delta FST(SLB) ≈ delta FST(SLP) is expected in regions of the genome unaffected by introgression, which is indicated as a red dashed line in each plot together with the Pearson’s correlation coefficient.

Extended Data Fig. 8

Frequency of the ALX1 blunt (B) allele in each of the six groups of G. fortis and G. scandens on Daphne Major based on individual genotyping (n = 30 for each pool).

Extended Data Fig. 9

Genotypes for the most significantly differentiated SNPs (n = 6,730) (FST > 0.6) from region 2 in Fig. 4a among individually sequenced ground finches (Geospiza spp.).

Supplementary information

Reporting Summary

Supplementary Table 1

Morphological data for the G. fortis and G. scandens individuals included in this study.

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Lamichhaney, S., Han, F., Webster, M.T. et al. Female-biased gene flow between two species of Darwin’s finches. Nat Ecol Evol 4, 979–986 (2020). https://doi.org/10.1038/s41559-020-1183-9

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