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Intraspecific phenotypic variation among
alewife populations drives parallel
phenotypic shifts in bluegill
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Magnus Huss†, Jennifer G. Howeth‡, Julia I. Osterman and David M. Post
Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06520, USA
Research
Cite this article: Huss M, Howeth JG,
Osterman JI, Post DM. 2014 Intraspecific
phenotypic variation among alewife populations drives parallel phenotypic shifts in
bluegill. Proc. R. Soc. B 281: 20140275.
http://dx.doi.org/10.1098/rspb.2014.0275
Received: 3 February 2014
Accepted: 19 May 2014
Subject Areas:
ecology, evolution
Keywords:
alewife, bluegill, character displacement,
eco-evolutionary dynamics, life history,
trait variation
Author for correspondence:
Magnus Huss
e-mail: [email protected]
†
Present address: Department of Aquatic
Resources, Institute of Coastal Research,
Swedish University of Agricultural Sciences,
Skolgatan 6, 74242 Öregrund, Sweden.
‡
Present address: Department of Biological
Sciences, University of Alabama, Box 870206,
Tuscaloosa, AL 35487-0206, USA.
Evolutionary diversification within consumer species may generate selection
on local ecological communities, affecting prey community structure. However, the extent to which this niche construction can propagate across food
webs and shape trait variation in competing species is unknown. Here, we
tested whether niche construction by different life-history variants of the
planktivorous fish alewife (Alosa pseudoharengus) can drive phenotypic divergence and resource use in the competing species bluegill (Lepomis macrochirus).
Using a combination of common garden experiments and a comparative field
study, we found that bluegill from landlocked alewife lakes grew relatively
better when fed small than large zooplankton, had gill rakers better adapted
for feeding on small-bodied prey and selected smaller zooplankton compared
with bluegill from lakes with anadromous or no alewife. Observed shifts in
bluegill foraging traits in lakes with landlocked alewife parallel those in alewife, suggesting interspecific competition leading to parallel phenotypic
changes rather than to divergence (which is commonly predicted). Our
findings suggest that species may be locally adapted to prey communities
structured by different life-history variants of a competing dominant species.
1. Introduction
Phenotypic variation within species has largely been ignored in ecological
studies; however, it is increasingly recognized that intraspecific variation may
have a profound influence on ecological dynamics [1–3]. Furthermore, evidence
that evolution can occur over ecological time scales and can have a measurable
impact on concurrent ecological dynamics has inspired research on the feedbacks
between ecology and evolution of life-history traits [1,4,5]. There are now several
examples of the influence of evolutionary diversification within species on ecological processes, both in laboratory systems [6] and in natural systems among
fishes [7–9], zooplankton [10] and plants [11,12]. These influences have effects
ranging from changes in population growth rate [4] to ecosystem processes
such as species richness and nutrient flux [9]. Phenotypic diversification caused
by eco-evolutionary interactions may also propagate to affect other species. For
example, there is a long-standing idea that species that compete for a set of
shared limited resources should diverge in resource use and phenotype by
means of natural selection (i.e. ecological character displacement [13,14]).
One striking example of the potential impact of predator trait divergence on the
dynamics of ecological systems has been documented in coastal North American
lakes inhabited by the planktivorous fish species alewife (Alosa pseudoharengus).
Alewife populations occur in two genetically distinct life-history types: an anadromous and a landlocked form [15]. Anadromous alewives display the ancestral
life-history strategy of adults migrating into lakes in spring to spawn and youngof-the-year alewives migrating to the ocean in autumn. By contrast, landlocked
alewives remain in lakes year-round owing to physical barriers isolating these
populations from the ocean [15]. Alewife predation has been shown to change zooplankton community structure by reducing the abundance of large-bodied species;
however, the effects on zooplankton communities differ depending on prey selectivity of the two life-history forms and duration in freshwater [7]. In lakes with
& 2014 The Author(s) Published by the Royal Society. All rights reserved.
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(a) Study system
Bluegill used in experiments and the comparative field study were
captured from June to September in 2007– 2009 and 2012 by
(b) Reciprocal transplant experiments
We performed reciprocal transplant common garden experiments during July– August 2012 to investigate (i) variation in
bluegill growth rate in response to differences in prey community
structure among three lake types (i.e. no-alewife lakes, anadromous and landlocked lakes) and (ii) variation in bluegill size
selectivity among lake types. The common garden set-up
allowed us to isolate the effects of phenotypic differences from
the potential influence of community composition, density and
seasonality. As the experimental fish were wild-caught, treatment responses are the sum of genetic and plastic effects. Black
rubber stock tanks were used as experimental mesocosms. The
tanks are 81 cm wide, 61 cm high and hold 265 l, but were
only about 90% filled. A few days before the start of the experiment, the tanks were filled with water from a small no-alewife
lake (Linsley) adjacent to the tanks. All tanks were covered
with netting to prevent bird predation, colonization by insects
and accumulation of leaves. The tanks were stocked with bluegill
captured in late June/early July from three no-alewife lakes
(Black, Gardner and Hayward), three anadromous lakes (Bride,
Dodge and Gorton) and three landlocked lakes (Pattagensett,
Quonnipaug and Rogers). Until the start of the experiments, captured bluegill from each population were held separately in tanks
and fed a mixture of small and large zooplankton (collected from
Linsley and Quonnipaug lakes).
(i) Growth experiment
On day 1 of the experiment (13 July 2012), fish from each lake
(except from Bride, from which we had only enough fish for
the food selection experiment) were netted from holding tanks,
weighed and stocked into the experimental tanks in groups of
four. A full factorial design with lake type (anadromous,
landlocked or no alewife) prey community type (small- or
large-bodied zooplankton) was replicated three times per treatment and randomly assigned to the tanks. Mean total length
(64 mm) and weight (4.36 g) of bluegill at stocking did not differ
significantly between treatments (ANOVA, p . 0.05). Two fish
died within the first 24 h of the experiment. They were removed,
weighed and replaced with new fish of similar size from the
2
Proc. R. Soc. B 281: 20140275
2. Material and methods
electrofishing (a common sampling technique that uses electricity
to stun fish in bodies of freshwater) along lake shorelines in three
no-alewife lakes (Black, Gardner and Hayward), three anadromous lakes (Bride, Dodge and Gorton) and three landlocked
lakes (Pattagensett, Quonnipaug and Rogers). All lakes are located
in the state of Connecticut, USA (see map in [7]). Whereas the lakes
without alewife have been isolated from the ocean over recent geological time, the lakes with landlocked alewife became isolated
from the ocean by human-made dams approximately 300 years
ago [15]. The lakes with anadromous alewife are connected
to the ocean. There are no significant differences in lake characteristics among lakes, for example, in size and productivity
[7,19], and all lakes contain similar fish communities (besides
the lack of alewife in no-alewife lakes), with yellow perch (Perca
flavescens), bluegill and pumpkinseed (Lepomin gibbosus) being
the most common non-alewife zooplanktivorous fish [19]. Our
study species, bluegill, is a dominant fish species in many North
American lakes, often as the result of introductions (which is
likely to be the case in our study lakes; Connecticut Department
of Environmental Protection 2008, personal communication). As
for alewife, large bluegills are positively size selective and availability of large zooplankton such as Daphnia may increase their
growth rates [22], suggesting potentially strong resource competition between alewife and bluegill. Clearly, alewife is the most
important species of the two shaping the zooplankton community
as we observe high densities of large-bodied zooplankton in our
no-alewife lakes that contain high densities of bluegill [7].
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anadromous alewife, large-bodied zooplankton can re-establish
over winter, whereas landlocked alewives exert year-round predation pressure that eliminates large-bodied zooplankton [7]. As
a result, lakes without alewife (‘no-alewife lakes’) contain largebodied zooplankton, lakes with landlocked alewife (‘landlocked
lakes’) contain small-bodied zooplankton and lakes with anadromous alewife (‘anadromous lakes’) contain large-bodied
zooplankton in the spring, but small-bodied zooplankton in
summer [7]. This divergence in prey community size structure
has been shown to feed back to drive phenotypic divergence
between anadromous and landlocked alewife populations,
including foraging traits such as gape size and gill raker morphology [7,16,17]. As a result, anadromous alewives are better
adapted to feeding on large prey items than are landlocked alewives [7], and there is direct evidence for divergence in feeding
traits shaping zooplankton community structure [16]. Variation
in alewife life-history and forging traits has, in turn, caused
evolutionary life-history diversification in their zooplankton
prey [18], which has additional direct effects on lower trophic
levels [10,19].
As exemplified in the alewife system, populations themselves may drive patterns of phenotypic diversification
through their structuring effects on the environment (i.e.
niche construction, here specifically referring to the process of
populations structuring the communities and ecosystems in
which they reside, sensu [1]; see [20] for an alternative definition
that includes an evolutionary response). The implications of
these altered selective landscapes on phenotypes and fitness
of competing species are, however, not known. Here, we ask,
using a combination of common garden experiments and a
comparative field study, whether altered selective landscapes
caused by landlocked alewife may drive phenotypic divergence
and resource use in competing species. Specifically, we study
whether growth rate, size selectivity and gill raker morphology
of bluegill (Lepomis macrochirus) are linked to divergence in prey
community structure (i.e. dominance of small- or large-bodied
zooplankton), caused by alewife presence and different alewife
life-history types [1,7]. We measured gill raker morphology,
because it is important to determine the size of prey consumed.
In bluegill, as in other planktivorous fishes, smaller inter-raker
spacing typically favours the capture of smaller prey [21]. We
hypothesize that bluegill will grow better in their native
environment than in the alternative environments and thus predict that bluegill from landlocked lakes will be better adapted
for foraging on small-bodied zooplankton compared with bluegill from other lake types. Specifically, we predict that bluegill
from lakes with landlocked alewife populations will (i) grow
better when fed small zooplankton and (ii) have a gill raker
morphology better adapted for feeding on small-bodied prey,
and accordingly (iii) select smaller prey items compared with
bluegill from lakes with no alewife or anadromous alewife
populations. Our results corroborate these predictions,
suggesting that phenotypic shifts in bluegill foraging traits parallel those in the alewife populations, and show how niche
construction by different life-history types can propagate
across food webs.
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0.6
proportion
0.4
0.3
0.2
0.1
0
0.5
1.0
1.5
body length (mm)
2.0
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Figure 1. The average zooplankton length – frequency distribution added
during the growth experiment in treatments representing communities
with small- (black bars) or large-bodied (white bars) zooplankton prey.
(c) Comparative field study: gill raker morphology
same population of origin. During the experiment, bluegill were
exposed to conditions of either small-bodied (representing landlocked lakes) or large-bodied zooplankton prey (representing noalewife lakes). Note that anadromous lakes are characterized
both by small- and large-bodied zooplankton, depending on
time of year [7]. Zooplankton prey of the appropriate size were
added to the tanks every second day throughout the experiment.
Small-bodied zooplankton were collected from a landlocked lake
(Quonnipaug) and large-bodied zooplankton from a no-alewife
lake (Linsley). Zooplankton were collected by pulling a plankton
net (150 mm mesh, 60 cm diameter) behind a boat at slow speed
through the open water area (pelagic zone) of the lakes. The
amount of zooplankton collected was adjusted to obtain similar
zooplankton biomasses of small and large zooplankton (biomass
estimates were done after every sampling, and sampling efforts
adjusted accordingly). The small-bodied zooplankton samples
had a biomass-weighted mean body length of 0.44 mm and were
dominated by Ceriodaphnia lacustris (70% of total biomass). The
large-bodied zooplankton samples had a mean body length of
1.47 mm and were dominated by Daphnia pulex (more than
99% of total biomass; see figure 1 for body size distributions of
zooplankton added to the tanks). At the termination of the experiment (1 August 2012), all fish were removed, euthanized and
frozen for preservation. The fish were measured to the nearest
0.1 mm total length, blotted dry and weighted to the nearest
0.1 mg wet weight. Growth rates are expressed as specific
growth rate:
G ¼ 100 ln Wend ln Wstart ,
where G is the specific growth rate (%), and W1 and W2 are wet
weights (grams) at the start and end of the experiment. The
water temperature in the tanks was measured on three occasions
and varied between 238C and 24.38C.
(ii) Prey selection experiment
We also carried out a short-term prey selection experiment using
the same type of tanks used in the growth experiment to ask
whether bluegill from different lake types differ in their selectivity
for small and large prey items. We stocked the mesocosms for the
prey selection experiment with identical zooplankton size distributions, so we could determine relative size–selection among
bluegill from different lake types by comparing the final zooplankton size distributions among treatments. This prey selection
experiment was set up on the second to last day of the growth
experiment, using fish that had been held in the holding tanks
We collected bluegill in 2006 –2009 and 2012 to compare foraging
morphology. A subset of collected bluegill were euthanized and
placed on ice for transport to the laboratory, preserved at –208C,
and processed for size and gill raker measurements. Gill raker
measurements were made on bluegill ranging in size from 30 to
212 mm total body length. Population-level sample sizes were:
Black, n ¼ 57; Bride, n ¼ 18; Dodge, n ¼ 42; Gardner, n ¼ 46;
Gorton, n ¼ 22; Hayward, n ¼ 33; Pattagansett, n ¼ 52; Quonnipaug, n ¼ 47; Rogers, n ¼ 47. The first branchial arch of each
bluegill was removed, stained with Alizarin red [24] and preserved
in 70% ethanol. The space between the first four gill rakers on the
lower limb of the first branchial arch and the lengths and widths of
these gill rakers (from tip to base) were measured under a dissecting microscope. For bluegill more than 50 mm total length, we also
counted the number of gill rakers on the arch (small fish were
excluded owing to difficulties removing gill rakers without damaging them). The means of the three measurements for space and
four measurements for lengths and widths were calculated for
each fish.
(d) Statistical analyses
Growth rates (log-transformed to normalize the data) were
analysed with a linear-mixed model (using the lme function in
the R package nlme) using restricted maximum-likelihood estimation, with lake type and zooplankton treatment entered as
fixed effects, and replicate lake populations entered as a
random effect nested within lake type. We used ANOVA to
test whether the ratio of growth rate (arcsine-square-root-transformed to normalize the data) of bluegill fed large relative to
small zooplankton (growth experiment) differed between lake
types. Similarly, differences in zooplankton body size ( prey
selection experiment) were determined using ANOVA. Given a
strong relationship between body length and gill raker morphology, differences in gill raker morphology (log-transformed)
between lake types were determined using bluegill total body
length (log-transformed) as a covariate, with lake populations
entered as a random effect nested within lake type. The interaction term was used to test whether the slope of the
relationship between gill raker morphology and body length differed depending on lake type. When the slopes differed
significantly ( p , 0.05), we tested for mean differences within
two specific size classes (33.3 + 0.24 mm and 125 + 0.95 mm,
means + s.e.), representing young-of-the-year and adult individuals, using ANOVA. Given a significant lake-type effect,
differences among lake types were evaluated using post
hoc Tukey’s tests. Statistical analyses were performed using R
(R Foundation for Statistical Computing).
Proc. R. Soc. B 281: 20140275
0
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0.5
and fed a mixture of small- and large-bodied zooplankton for
approximately five weeks. Two fish (mean total length 67 mm)
originating from each lake (except from Black lake, from which
no fish less than 80 mm survived) were added to the tanks and
fed a mixture of small- and large-bodied zooplankton added in
similar biomasses (collected as above, with a size–distribution
similar to that in figure 1). Treatments and population of origin
were randomly assigned, and each population was replicated
twice. After 20 h, fish were removed, euthanized and frozen for
preservation. Tanks were then gently stirred, and zooplankton
were sampled using a depth-integrated sampler that collected
1.2 l of water. The collected water was filtered through an 80 mm
mesh net. Two zooplankton samples per tank were pooled and
preserved in 70% ethanol. Zooplankton were identified and
counted under a dissecting microscope. Fifteen (all if fewer) individuals from each taxon were length-measured and transformed
to dry mass using length–weight regressions [23].
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(a)
A
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20
15
10
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B
0.7
B
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0
LL
(b)
B
relative growth rate
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AN
lake type
NA
Figure 3. Biomass-weighted mean (+s.e.) zooplankton body length at the
end of the prey selection experiment in treatments with bluegill from landlocked (LL), anadromous (AN) and no-alewife (NA) lakes. The dashed line
indicates the mean zooplankton body length at the start of the experiment.
Letters indicate significant differences ( p 0.05) among lake types.
2.5
AB
2.0
1.5
communities with bluegill originating from landlocked
lakes (similar to the added zooplankton body size; see the
dashed line in figure 3) than in communities with bluegill
from anadromous or no-alewife lakes (Tukey’s post hoc test,
p , 0.05), indicating that bluegill from anadromous and noalewife lakes were positively size selective, whereas bluegill
from landlocked lakes were neutrally size selective.
A
1.0
LL
AN
lake type
NA
Figure 2. (a) Mean (þs.e.) growth rate of bluegill from landlocked (LL), anadromous (AN) and no-alewife (NA) lakes when fed small (black) and large (white)
zooplankton. (b) Mean (+s.e.) ratio of growth rate of bluegill from the different
lake types fed large relative small zooplankton in the different lakes types. The
dashed line indicates equal growth rates of bluegill-fed small and large zooplankton (values . 1 indicate faster growth when fed large zooplankton). Letters
indicate significant differences ( p 0.05) among lake types.
3. Results
(a) Growth experiment
We found a significant interaction between lake type of origin
and zooplankton treatment on bluegill growth rates (t ¼ 4.07,
p ¼ 0.007; figure 2a), but no significant main effects ( p . 0.05).
This was a result of differences in relative growth rate of bluegill fed large-bodied zooplankton relative to small-bodied
zooplankton, depending on which alewife lake type the bluegill
originated from (ANOVA, F2,7 ¼ 56.13, p ¼ 0.045, figure 2b).
Bluegill from landlocked lakes grew equally well when fed
small- and large-bodied zooplankton, but bluegill from anadromous and no-alewife lakes grew better when fed large- than
small-bodied zooplankton (Tukey’s post hoc test, p , 0.05).
(c) Gill raker morphology
There were no significant differences in the slope of number of
gill rakers (interaction term, t ¼ 2.18, p ¼ 0.091) or the slope of
gill raker width (interaction term, t ¼ 0.080, p ¼ 0.94) regressed
against bluegill body length, nor in means of gill raker numbers
(t ¼ 0.415, p ¼ 0.52) or width (t ¼ 0.168, p ¼ 0.89; figure 4). The
slope of the relationship between gill raker spacing and body
length (interaction term, t ¼ 3.31, p ¼ 0.029) and gill raker
length and body length (interaction term, t ¼ 2.88, p ¼ 0.048)
varied among lake types (figure 4). As the slopes differed significantly, we analysed mean differences for small and large
bluegill separately. Mean gill raker spacing and length were
significantly different between lake types for small bluegill
(ANOVA, spacing: F2,7 ¼ 7.83, p ¼ 0.029; length: F2,7 ¼ 10.0,
p ¼ 0.018), but not for large bluegill (ANOVA, p . 0.05).
In the small size-group, bluegill had smaller gill raker spacing
and longer gill rakers in landlocked than in no-alewife lakes
(Tukey’s post hoc test, p , 0.05). Thus, small bluegill—the size
class that most relies upon zooplankton as a resource—had
significant differences in gill raker morphology that were consistent with the differences in size selectivity we observed in
the prey selection experiment.
(b) Prey selectivity experiment
4. Discussion
There was a clear difference in the effect of bluegill lake type
of origin on zooplankton size structure (figure 3; F2,15 ¼ 9.06,
p ¼ 0.004). Mean zooplankton body size was larger in
Using common garden experiments and a comparative field
study, we have shown that the strong effects of life-history
differences among alewife populations on zooplankton
Proc. R. Soc. B 281: 20140275
zooplankton size (mm)
growth rate (%)
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–0.2
–0.4
–0.6
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gill raker width (log10)
(c)
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0
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–0.6
–0.8
–1.0
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body length (log10)
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Figure 4. Log-transformed (a) gill raker spacing, (b) gill raker length and
(c) gill raker width as a function of log-transformed total body length for
bluegill from landlocked (white circles, solid regression line), anadromous
(crosses, dotted regression line) and no-alewife lakes (black circles, dashed
regression line).
communities have propagated across the food web to influence the phenotype and fitness of a competing species. We
found that bluegill from different lake types differed in
(i) growth rates when exposed to small- or large-bodied
prey, (ii) prey size selectivity and (iii) gill raker morphology.
Our results revealed clear divergence in foraging traits
between bluegill from landlocked and no-alewife lakes, but
only weak divergence in bluegill between anadromous and
no-alewife lakes. Consistent predation by landlocked alewife
shapes the zooplankton community [7] such that it produces
strong selection for traits that increase foraging performance
on small-bodied zooplankton [16]. Consequently, we found
bluegill from replicated landlocked lakes to be better adapted
to feeding on small-bodied prey; they were less selective for
large prey than bluegill from anadromous and no-alewife
lakes, and had smaller gill raker spacing than bluegill from
no-alewife lakes. Taken together, these results suggest differences in bluegill foraging traits in response to variation in
prey size structure caused by the presence or absence of
alewife as well as life-history differences among alewife
populations. This shift in foraging traits in response to prey
size structure suggests there is a clear functional link between
bluegill trait change and resource use, as would be expected
based on theory of ecological character displacement [13,14]
(for the role of plasticity in character displacement, see [25]);
however, in contrast to most literature on character displacement, interspecific competition produced phenotypic shifts in
bluegill foraging traits parallel to those in the alewife
populations.
It has only recently been established that intraspecific
phenotypic variation may generate diversifying selection on
local ecological communities, affecting prey community
structure and ecosystem function [8,9,16]. In the alewife
system, variation in alewife life history drives divergence in
Daphnia life history that in turn alters consumer –resource
dynamics [10,18]. This study expands on these findings,
suggesting that the effects of diversifying selection may propagate across natural food webs to affect competing species.
Observed variation in bluegill growth rates when exposed
to small- and large-bodied zooplankton is consistent with
adaptation to prey communities similar to those in their
lakes of origin. Landlocked lakes are characterized by dominance of small-bodied zooplankton year-round [7]. Thus, in
landlocked lakes, selection should favour those individuals
that can perform well feeding on small-bodied zooplankton.
Accordingly, we found that bluegill from landlocked lakes
select smaller prey and grow relatively better when fed
small-bodied zooplankton than did bluegill from anadromous and no-alewife lakes. These findings are consistent
with previous studies showing persistent ecological effects
of landlocked alewife, leading to strong eco-evolutionary
feedbacks shaping alewife foraging traits [16]. Our study
shows that those ecological effects also shape bluegill foraging traits. By contrast, the lack of persistent environmental
effects of anadromous alewife limits the potential for alewife
with an anadromous life history to drive phenotypic
variation in bluegill.
The traditional focus of community ecology has been on
the influence of species identity and abundance. It is also
increasingly recognized that trait-mediated effects may be
equally important [26]; however, research on impacts of
trait variation is commonly based on species means, ignoring
variation within species. Our results suggest that niche construction by landlocked alewife, rather than by fish species
composition and abundance, drives variation in foraging
traits and performance in bluegill among lake types. This
suggests adaptive divergence in bluegill in response to the
ecological impact of a specific life-history type of a competing
species. A key question is whether the observed divergence
among bluegill populations is caused by genetic divergence
or by phenotypic plasticity. Our common garden design
showed that phenotypic differences remained when exposed to
a shared environment and congruent patterns in experiments,
and our comparative lake data suggest local adaptation is
likely, but we have no information of heritability of measured
traits in bluegill. Previous work indicates differences in gill
raker morphology are likely to have a genetic basis [27,28],
but a plastic component cannot be ruled out [29]. Whether or
not trait variation caused by niche construction among populations of competing species is the result of genetic divergence
or phenotypic plasticity would be an interesting topic for
future studies on this and similar systems.
Although the occurrence of rapid evolution in nature is
well established [4,30,31], we know little about its importance
for natural ecosystems [5,7]. Generally, the importance of
evolutionary change for ecological interactions is expected
5
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This study was conducted under our approved Yale University
Institutional Animal Care and Use Committee Protocols no. 200610734, no. 2009-10734 and no. 2012-10734. Fish were collected
under State of Connecticut Scientific Collector Permits no. 0508021,
no. SC-07015 and no. SC-11016.
Acknowledgements. We thank Monica Ague, Jakob Brodersen, Paul
Bucala, Andrew Jones, Matthew Walsh, Jerome Weis and Derek
West for help in the field.
Data accessibility. Data supporting the results in the article are deposited
at Dryad (doi:10.5061/dryad.57n5j).
Funding statement. This research was supported by Yale University, the
USA National Science Foundation (DEB no. 0717265) and a postdoctoral fellowship from the Swedish Research Council to M.H.
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