Clinal colour variation within a panmictic population
of tree squirrels, Tamiasciurus douglasii (Rodentia:
Sciuridae), across an ecological gradient
ANDREAS S. CHAVEZ* and G. J. KENAGY*
Burke Museum and Department of Biology, University of Washington, Seattle, WA 98195, USA
Received 11 March 2014; revised 20 May 2014; accepted for publication 20 May 2014
Local adaptation occurs when a population in a heterogeneous environment experiences divergent ecological
selection but only if selection is stronger than the homogenizing effects of gene flow. The forest environments of
Oregon vary along a physical and biotic gradient from a wet, closed-canopy forest near the coast to a drier
open-canopy forest eastward across the Cascade Mountains. The present study explores patterns of local adapta-
tion in Douglas squirrels (Tamiasciurus douglasii) in relation to these transitions in forest structure and ecology.
We test for the presence of morphological clines in relation to gene flow and, more specifically, whether any such
character clines correspond with environmental clines. We sampled animals at six locations (10 specimens each)
and evaluated environmental parameters across a 240-km west-to-east transect. Population structure analysis of
18 microsatellite loci indicates a single, panmictic squirrel population across the entire transect. Coalescent-based
estimates show bidirectional gene flow at similar west–east intensities between squirrels in coastal and interior
forests. Of the four skull traits examined, none shows a significant clinal transition. By contrast, ventral fur colour
shows a strong clinal transition, from deep-orange in coastal forest to whitish–yellow in the interior forest. This
pattern of phenotypic divergence coincides with the gradient in tree-canopy cover. Ventral fur colour of T. douglasii
exemplifies a gradation of continuous phenotypic variation maintained despite ongoing gene flow in a panmictic
population. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 536–546.
ADDITIONAL KEYWORDS: cline analysis – coloration – divergent selection – gene flow – local adaptation
– microsatellites – phenotypic variation – skull morphology.
INTRODUCTION
Patterns of phenotypic variation within continuously
distributed populations suggest that local adapta-
tion is common in nature: as exemplified by the
ecogeographical ‘rules’ of Gloger (1833), Bergmann
(1847), and Allen (1877). Such patterns of environmen-
tally driven phenotypic variation can be associated
with spatial differences in the selective environments
experienced by continuously distributed populations
(Endler, 1977; Martínez et al., 2014; Souto-Lima &
Millien, 2014). Local adaptation is the consequence of
local selection pressures that favour different traits in
populations that occupy different environments. When
selection is sufficiently strong, divergence can occur
even when gene flow is strong enough to homogenize
the populations at neutral loci (Kawecki & Ebert,
2004). Ecological selection plays an important role in
adaptation and also potentially in speciation, either
because divergent selection favours the prevalence
of locally beneficial alleles or because closely linked
loci contribute to reproductive incompatibilities that
become fixed in genetically divergent populations
(Maynard Smith & Haigh, 1974; Felsenstein, 1981;
Barton, 2000; Nosil, Funk & Ortiz-Barrientos, 2009;
Lenormand, 2012).
Huxley (1938) coined the term ‘cline’ to describe
geographical gradations of phenotypes within or
between species, and this term can also apply to
changes in allele frequencies (Slatkin, 1985). One of
the most direct ways to measure the strength of
selection in nature is to measure the rate of change
in frequencies of genes or phenotypes across a cline *Corresponding author. E-mail: aschavez@uw.edu
Biological Journal of the Linnean Society, 2014, 113, 536–546. With 2 figures
© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 536–546 536
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