selection, fitness variation, phenotypic variation,
microevolutionary change, and a possible driver
of selection. Combining large-scale genomic and
ecological data in natural populations will substantially enhance our understanding of both the
mechanistic basis and evolutionary consequences
of natural selection.
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We thank the many researchers who collected material and data for
the Wytham study; L. Vernooij, P. de Goede, and H. Bouwmeester
for fieldwork on the Dutch populations; and C. Mateman for laboratory
assistance. The Natural History Museums in London (NHM) and
Oxford (OUMNH) kindly granted us access to great tit specimens.
R. Butlin, N. Nadeau, and P. Nosil provided helpful comments on the
manuscript. This work was supported by grants from the European
Research Council (grants 339092 to M.E.V., 250164 to B.C.S., and
202487 to J.S.), Biotechnology and Biological Sciences Research
Council (grant BB/N011759/1 to L.G.S.), and Natural Environment
Research Council (grant NE/J012599/1 to J.S.). M.B., L.G.S., M.A.M.G.,
B.C.S., M.E.V., and J.S. designed the study. M.B., L.G.S., and J.S.
analyzed the genomic data for signatures of selection. V.N.L., P.G.,
and J.S. analyzed estimated trait genetic architectures. V.N.L. performed
gene ontology analyses. A.G.G., K.M., J.P., and I.V. measured and
analyzed bills. L.G.S., E.F.C., and J.A.F. collected and analyzed bird
feeding station data. E.F.C., J.A.F., A.G.G., K.v.O., B.C.S., and M.E.V.
coordinated and collected ecological data and DNA samples. M.A.M.G.,
K.v.O., M.E.V., and J.S. coordinated collection of SNP data. M.B.,
L.G.S., V.N.L., and J.S. cleaned and quality-control checked SNP
data. M.B., L.G.S., and J.S. wrote the manuscript with input from all
other authors. The data described in the paper are archived on
Dryad with accession number doi:10.5061/dryad.p03j0.
Materials and Methods
Tables S1 to S3
Figs. S1 to S9
2 November 2016; resubmitted 19 May 2017
Accepted 12 September 2017
368 20 OCTOBER 2017 • VOL 358 ISSUE 6361
Fig. 3. COL4A5 locus on chromosome 4A. (A) Two-Mb zoom of EigenGWAS (green triangles)
and GWAS (black circles) P values at the COL4A5 region (Fig. 2A, highlighted in blue). Red
horizontal bars indicate gene locations. (B and C) Bifurcation diagram for haplotypes in Wytham,
starting from the two alleles at the most significant GWAS SNP. Shown is the extended haplotype
at the COL4A5-C-allele in (C), relative to the shorter haplotypes at the COL4A5-T allele in
(B), which is consistent with a recent selective sweep around the COL4A5-C allele in the
United Kingdom. (D) Bill length and COL4A5 genotype. The C allele is associated with longer bills
(R2 = 0.035). (E) The COL4A5-C allele is associated with greater annual fledgling production
in the UK population (R2 = 0.015). (F) COL4A5-C allele birds display greater winter feeding site
activity. The y axis is log10 transformed cumulative activity records (R2 = 0.01). Lines and shaded
areas in (D) to (F) are fitted values and 95% confidence limits from general(ized) linear
models (full data are plotted in figs. S8 and S9).
Mainland Europe UK
Year of birth
Fig. 4. Spatiotemporal variation in bill length. (A) Bill lengths of museum samples from the
United Kingdom and mainland Europe. (B) Temporal variation in bill length in the Wytham population
plotting annual means with standard error from 1982–2007. Line and (narrow) shaded area in (B) are
fitted values and 95% confidence limits from a linear regression (R2 = 0.004); there are different
scales on axes in (A) and (B).