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Contents lists available at ScienceDirect

General and Comparative Endocrinology

journal homepage: www.elsevier.com/locate/ygcen
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Physiological exibility in an avian range expansion

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Lynn B. Martin a,, Andrea L. Liebl a,b

a
b

University of South Florida, Department of Integrative Biology, SCA 110, Tampa, FL 33620, United States
University of Exeter, Centre for Ecology and Conservation, Penryn TR10 9EZ, UK

a r t i c l e

i n f o

Article history:
Received 22 April 2014
Revised 13 June 2014
Accepted 20 July 2014
Available online xxxx
Keywords:
Stressl
Plasticity
Homeostasis
Invasion

a b s t r a c t
The mechanisms that enable animals to colonize new areas are little known, but growing evidence
indicates that the regulation of stress hormones is important. Stress hormones probably inuence invasions because they enable organisms to adjust their phenotypes depending on environmental context.
Often, studies of stress hormones are based on single or a few samples even though the exibility in
the regulation of such hormones is what enables them to achieve homeostasis and facilitate performance.
Here, we asked whether exibility in the regulation of one stress hormone, corticosterone, was related to
colonization success in one of the worlds most successful avian invaders, the house sparrow (Passer
domesticus). We studied Kenyan house sparrows, as the species was recently introduced there (around
1950) and has since expanded northwestward. Previous work in this system revealed that younger populations released more corticosterone during a restraint stressor than older populations. Our rst goal
was to discern whether such population differences were xed or exible in adulthood; our second goal
was to determine whether individual identity explained any variation in corticosterone regulation. As
before, we found that corticosterone responses to short-term restraint (i.e., stress responses), but not
baseline corticosterone, were larger in younger populations. We also found that both baseline and
stress-induced corticosterone measures were exible; both metrics became similar among sites after
one week of captivity. For stress responses, we also found that individual identity was important.
Altogether, the present data suggest that the colonization of Kenya by house sparrows might have been
facilitated by stress hormone regulatory exibility.
2014 Published by Elsevier Inc.

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1. Introduction

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Introduced species are among the greatest threats to native

ecosystems, and they cost billions of dollars annually to control
(Mack et al., 2000). However, introduced species also present
unique opportunities for understanding important biological phenomena, such as how organisms expand their ranges and adjust
to environmental novelty. Particular factors mediate organismal
invasion success (Parker et al., 2013) such as reproductive life history (Sol et al., 2012), behavioral innovation (Sol et al., 2005, 2002),
propagule pressure (Colautti et al., 2006), and genetic admixture
(Kolbe et al., 2007, 2008). Whether variation in these and other
traits arises via selection, plasticity, or both (Richards et al.,
2006) remains mostly unresolved, especially for vertebrates. Selection is undoubtedly important, especially over long time scales.
However, plasticity is probably impactful too because invasions
commonly involve genetic bottlenecks, which can restrict

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Corresponding author. Fax: +1 813 974 3263.

responses to selection (Allendorf and Lundquist, 2003), and

plasticity can match the phenotype to the environment faster than
selection (Ghalambor et al., 2007).
Phenotypic plasticity is usually dened as the ability of a genotype to express different phenotypes depending on the environment (Agrawal, 2001). In plants, plasticity is related to invasion
and introduction success (Davidson et al., 2011). In animals, the
importance of plasticity in range expansion is less understood,
especially with regards to physiology. Physiological plasticity is
of likely great importance to range expansions though (Atwell
et al., 2012) because of the importance of homeostasis to performance and tness (Wingeld, 2013a). Indeed, homeostasis itself
is a form of plasticity (Crespi et al., 2013; Woods, 2009); for physiological stasis to occur, one or more physiological processes must
change when environments change (Sterling, 2012; Woods and
Wilson, in press). Physiological plasticity occurs on at least three
time scales: during development (West-Eberhard, 2003), between
seasons (Jacobs and Wingeld, 2000), and over short time frames
(Piersma and Drent, 2003) such as across days or months. Epigenetic mechanisms, maternal effects, early-life experiences, and

E-mail address: lbmartin@usf.edu (L.B. Martin).

http://dx.doi.org/10.1016/j.ygcen.2014.07.016
0016-6480/ 2014 Published by Elsevier Inc.

Please cite this article in press as: Martin, L.B., Liebl, A.L. Physiological exibility in an avian range expansion. Gen. Comp. Endocrinol. (2014), http://
dx.doi.org/10.1016/j.ygcen.2014.07.016

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L.B. Martin, A.L. Liebl / General and Comparative Endocrinology xxx (2014) xxxxxx

habituation all shape these plasticities, particularly the regulation

of homeostasis mediators (Ledn-Rettig et al., 2013; Love et al.,
2013; Martin et al., 2011b; Schoech et al., 2011). In the present
study, we sought to determine whether plasticity occurring over
short time scales, called phenotypic exibility (Piersma and
Drent, 2003) or activational plasticity (Snell-Rood, 2013), inuences population differences in glucocorticoid regulation, perhaps
by facilitating mosaics of adaptive traits (Woods, 2014).
To investigate the role of physiological exibility in range
expansions, we have been studying the house sparrow (Passer
domesticus) in Kenya. House sparrows are exemplary invaders,
now being one of the most broadly distributed animals in the
world (Anderson, 2006). The Kenyan invasion is particularly
intriguing because house sparrows were introduced there recently
(1950; Summers-Smith, 1988), and distance from the initial site
of introduction (Mombasa) is a good predictor of genetic and phenotypic variation among populations (Liebl and Martin, 2012,
2013, 2014; Martin et al., 2014). Also, the observed patterns of variation (in combination with the absence of other known introductions to east Africa and the recency of the introduction to
Mombasa) implicate plasticity as inuential in the Kenyan range
expansion (Martin et al., 2014). Indeed, microsatellite data indicate
that Kenyan house sparrows are genetically less diverse than other
populations (Schrey et al., 2011), and genotypes common at the
site of introduction (in Mombasa) are also found at the western
range edge > 850 km away (Schrey et al., 2014).
Glucocorticoids are integral mediators of organismal performance (Crespi et al., 2013; Love et al., 2013), serving basal metabolic functions but also enabling individuals to endure or recover
from stressors (Boonstra, 2013; Wingeld, 2013b). In most studies,
glucocorticoid actions are inferred from just a few samples, but
whether so few measures capture the complexity and dynamism
of glucocorticoid regulation is questionable. Indeed, a major part
of what enables glucocorticoids to facilitate homeostasis and
coping with various stressors is that their regulation is quite exible. Subsequently, it might be informative to consider how critical
aspects of glucocorticoid regulation (i.e., their baseline levels and
responses to stressors) change with environments. By using a classic reaction norm approach (i.e. measuring glucocorticoid traits
several times across an environmental gradient), one might better
capture the regulatory exibility that allows these hormones to
achieve their diverse functions. At the same time, one might determine whether regulatory exibility is consistent within-individuals, which is often assumed but rarely tested in eld studies of
glucocorticoids.
Here, we used a reaction norm study design to ask whether the
glucocorticoid proles of birds from the oldest Kenyan population
(Mombasa) would come to resemble birds from some of the newer
populations (Nairobi and Nakuru) when birds were held in captivity for one week. We focused on glucocorticoids because we found
previously that distance from the site of introduction predicted the
magnitude of corticosterone (the main avian glucocorticoid) stress
responses (i.e. corticosterone in response to restraint) (Liebl and
Martin, 2012); the nearer birds occurred to range edges, the stronger their stress responses. We used captivity as an environmental
gradient because we found previously that keeping house
sparrows captive for short periods alters corticosterone regulation
(Martin et al., 2012, 2011a); in that study, baselines were elevated
and stress responses damped after a period of captivity. By
measuring corticosterone repeatedly in captivity, we could assess
whether populations would come to resemble each other if all
individuals experienced similar conditions. A second motivation
of our study was to discern whether individual regulatory personalities (Dingemanse et al., 2010; Nussey et al., 2007; Williams,
2008) occurred and/or inuenced plasticity across populations,

and we used random regression to test these expectations

(Dingemanse and Dochtermann, 2012).

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2. Methods

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2.1. Bird capture, care and morphometrics

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Wild, adult Kenyan house sparrows (n = 29; Mombasa = 8 (6M,

2F), Nairobi = 14 (6M, 8F), Nakuru = 7 (4M, 3F)) were captured in
mist nets in MayJuly 2012; the oldest site was Mombasa where
birds were introduced 1950, whereas the newest was presumed
to be Nakuru, with Nairobi intermediate in age. 50 lL of blood
was collected within 3 min of capture from the brachial vein, and
sex was recorded for each individual. Birds were then held in cloth
bags in the shade for 30 min when a second blood sample (50 lL)
was taken; the difference between this value and the initial baseline sample was considered the stress response. Birds were then
returned to bags where they were held singly (2.5 h maximum)
until they were transferred to and housed singly in conventional
songbird cages (35 cm wide  27.5 cm deep  47.5 cm high) for
7 days. Each cage included two perches, ad libitum access to mixed
seeds (red and white millet, rice, and sorghum) and water treated
with anti-coccidian medication (to prevent mortality due to naturally occurring infections). For the duration of captivity, birds
remained isolated from human disturbance except a <10 min period daily when food and water were checked and replaced as
needed. However, all birds were allowed to see and hear each other
throughout the study. Photoperiod and climate conditions were
maintained at ambient levels for the study duration. Three days
post capture (around 0800 h), each bird was caught from its cage,
and 50 lL of blood was taken from the brachial vein within 3 min
of researcher entry into the room; birds were then placed individually in cloth bags, and 30 min later, another 50 lL blood sample
was taken. Immediately afterwards, birds were returned to their
cages and maintained as above. At 7 days post-capture, birds were
bled at 3 min and 30 min similarly to day 3; after the last blood
sample, birds were released near their site of capture. To ensure
samples were collected within 3 min in captive birds, multiple
researchers entered the housing room simultaneously. Blood was
centrifuged (<2 h post-collection) and plasma was removed from
samples and stored in liquid nitrogen until return to the USA,
where they were stored at 40 C. All procedures met guidelines
for the use of animals in research and were approved by the USF
IACUC (#W3202) and the Kenya Ministry of Science and Technology (NCST/RRI/12/1/MAS/15).

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2.2. Corticosterone assay

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An EIA kit (Enzo Life Sciences, Ann Arbor, MI; cat# 900-097)
was used to measure total plasma corticosterone (CORT) Breuner
et al., 2006; Liebl and Martin, 2012; Martin et al., 2012. Briey,
10% steroid displacement reagent (5 ll) was added to 5 ll of
plasma and 5 min later, assay buffer (240 ll) was added to each
sample, vortexed, and aliquoted in duplicate (100 ll per well) to
plates. In addition, a standard curve (ranging from 200,000 to
32 pg) was measured in duplicate on each plate. Samples and standards were then incubated with conjugated CORT and antibody for
2 h at room temperature while being shaken. Wells were emptied
and washed 3 times before substrate was added to all wells; plates
were incubated an additional 1 h at room temperature without
shaking. Stop solution was then added, and each plate was read
at 405 nm (corrected at 590 nm to minimize background absorbance). Average intra-assay variation was 7.8% and inter-assay
variation was 7.0%.

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Please cite this article in press as: Martin, L.B., Liebl, A.L. Physiological exibility in an avian range expansion. Gen. Comp. Endocrinol. (2014), http://
dx.doi.org/10.1016/j.ygcen.2014.07.016

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2.3. Data analysis

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We used random regression (Dingemanse and Dochtermann,

2012; Dingemanse et al., 2010; Westneat et al., 2011) in SPSS
(v21) to analyze corticosterone measures of Kenya house sparrows.
We rst log10 transformed corticosterone data, which eliminated
non-normality (assessed with 1-sample KolmogorovSmirnov
tests). We then used a model-selection approach to identify the
best predictors of corticosterone starting from full models. We analyzed dependent variables (baseline and restraint-induced levels of
corticosterone) separately, as each has a functionally different role.
Our full models included distance from Mombasa (our surrogate
for population age), time in captivity and their interaction as xed
effects with all factors treated as continuous variables. We
included individual as a random effect to account for repeated
measures and to assess the effect of random intercepts on corticosterone. Persistence of random intercepts in best-t models would
indicate support for regulatory personalities. Our rst attempts at
model simplications involved selection of covariance structure
for random effects starting with scaled identity followed by
unstructured options; we selected the variant that minimized the
corrected Akaike Information Criteria (AICc) scores but did not
prevent model convergence. We minimized models further rst
by dropping random terms then dropping xed effects, beginning
with the interaction term. We calculated and report Akaike
weights for the top models and the full models (Table 1). Additionally, as we have found that glucocorticoid receptor expression
differs among sites (Liebl and Martin, 2013), we transformed corticosterone data to percentages of values at time of capture and
again performed model selection; proportional data were also
transformed prior to analysis to normalize distributions. Finally,
to address whether corticosterone regulatory plasticity at one time
scale (e.g., stress response in wild) covaried with regulatory plasticity at another scale (e.g., baseline response to captivity), we calculated linear slope coefcients for individuals and used Spearman
correlation analyses to ask whether values were related. As time
constraints associated with rapid mist netting and bleeding prevented us from collecting body mass data from all individuals,
we could not investigate potential roles of body condition on
corticosterone. We did not detect effects of sex on dependent
variables in preliminary analyses, but small sample sizes within
sites prevent us from making strong claims about any effects of

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sex. We also asked whether a quadratic effect of captivity better

explained corticosterone than a linear one; the untransformed variant was more informative, although results were similar. Subsequently, neither sex nor time2 effects are reported below.

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3. Results

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3.1. Baseline corticosterone

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The best-supported model for baseline corticosterone included

only time in captivity (Table 1); in that model, baseline corticosterone increased over time in captivity (time: F1, 82 = 28.9, P < 0.001;
Fig. 1a). However, two other models received support: one
included a random intercept for individual (Wald Z = 0.13,
P = 0.90); another included city as a xed effect (F1, 81 = 0.30,
P = 0.59). The top model for %-transformed baseline corticosterone
revealed a similar pattern (Table 1). Again, the best-t model
included only time in captivity (F1, 81 = 14.4, P < 0.001; Fig. 1b).
However, another model including a random intercept for individual (Wald Z = 1.0, P = 0.30) received support; a third supported
model included city as a xed effect (F1, 81 = 0.05, P = 0.82).

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3.2. Stress response

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For stress responses, the top model included time in captivity

(F1, 57.6 = 12.9, P = 0.001; Fig. 2a) and the random intercept term
for individual (variance = 0.003 0.002, Wald Z = 1.94, P = 0.05).
As variance attributable to the repeated-measures effect was
0.008 (0.001), the intra-class correlation coefcient for individual
was 0.283. Thus, 28% of the variance in stress response corticosterone was due to individual. The second-best model likewise
included time in captivity (time: F1, 58.0 = 13.2, P = 0.001) as a xed
effect and individual intercept as a random effect (Wald Z = 1.68,
P = 0.09), but also included city (Table 1). As observed in a prior
study (Liebl and Martin, 2012), stress responses increased from
oldest to youngest cities (F1, 28.0 = 5.28, P = 0.03; b = 0.04 0.02).
For stress responses adjusted to at capture values (%-transformation), time in captivity (F1, 58.0 = 8.3, P < 0.005; Fig. 2b) and individual intercept (variance = 0.005 0.003, Wald Z = 1.92, P = 0.06)
were the sole predictors in the top-model (Table 1). In this model,
individual explained 27.1% of stress response variation (repeatedmeasures variance = 0.014 (0.003)). The second-best model,

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Table 1
Best-t models for corticosterone regulation in Kenyan house sparrows.
Variable

Version

Model

Fixed effects

Random effects

ka

Di

wi

Baseline

Raw

1
2
3
4
Full

Time
Time
Time + city
Time + city
Time + city + city * time

Intercept

Intercept
Intercept

3
4
4
5
6

57.5
59.6
61.4
63.5
71.4

0
2.1
3.9
6
13.9

0.648
0.227
0.092
0.032
0.001

% At capture

1
2
3
4
Full

Time
Time
Time + city
Time + city
Time + city + city * time

Intercept

Intercept
Intercept

3
4
4
5
6

50.7
51.4
54.9
55.4
59.0

0
0.7
4.2
4.7
8.3

0.516
0.364
0.063
0.049
0.008

Raw

1
2
3
4
Full

Time
Time + city
Time + city
Time
Time + city + city * time

Intercept
Intercept

Intercept

4
5
4
3
6

140.4
139.2
137.1
136.4
132.9

0
1.2
3.3
4.0
7.5

0.526
0.289
0.101
0.071
0.012

% At capture

1
2
3
4
Full

Time
Time
Time + city
Time + city
Time + city + city * time

Intercept

Intercept

Intercept

4
3
5
4
6

88.0
84.2
82.9
78.9
71.4

0
3.8
5.1
9.1
16.6

0.807
0.121
0.063
0.009
0.000

Stress response

AICc

k Denotes number of parameters in each model.

Please cite this article in press as: Martin, L.B., Liebl, A.L. Physiological exibility in an avian range expansion. Gen. Comp. Endocrinol. (2014), http://
dx.doi.org/10.1016/j.ygcen.2014.07.016

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30

Mombasa
Nairobi
Nakuru

100

corticosterone
(ng ml-1)

corticosterone
(ng ml-1)

Mombasa
Nairobi
Nakuru

20
10
time:

80
60
40
20

= 0.23 +/- 0.04

time:

0
0

Time (days in captivity)

Time (days in captivity)

b
time:

corticosterone
(ng ml-1)

b
1000

= 0.15 +/- 0.04

800
600
400
200

300

time:

= 0.05 +/- 0.02

200
100
0

0
0

Time (days in captivity)

% change in corticosterone
(ng ml-1)

= 0.04 +/- 0.01

-100
0

Time (days in captivity)

Fig. 1. Comparisons of baseline corticosterone responses to captivity in Kenyan
house sparrows: (a) raw baseline corticosterone over a week of captivity; (b) %
change in baseline relative to value at capture from the wild. Bars are means 1SE;
betas denote effects of xed factors in best-t models.

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which received little support, included only time as a xed effect

(Table 1).

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3.3. Covariation

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Spearman correlation analyses revealed little evidence that

forms of corticosterone regulatory plasticity were related within
individuals. Individual slope coefcients of stress responses at
the time of capture were unrelated to slope coefcients of the
effects of captivity on baseline corticosterone (Fig. 3a) and stress
responses (Fig. 3b). Likewise, baseline corticosterone and stress
response slopes in response to captivity were unrelated (Fig. 3c).

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4. Discussion

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We expected corticosterone regulation to be more exible in

newer Kenyan house sparrow populations, but we expected that
regulatory personalities among individuals might constrain population-level plasticity. Our expectations were not supported
though, mostly because corticosterone regulation was so exible
among all sparrows. As in a previous study, we found that population age and stress responses were related; birds from the newest
sites had stronger responses than birds from the oldest site. However, all birds exhibited plasticity in baseline corticosterone and
stress responses. Even though individual identity explained >25%
of variation in stress response plasticity to captivity (for both
raw and adjusted data), after a week of captivity birds from the
oldest sites came to resemble birds from the newest sites. Furthermore, correlation analyses indicated that individual corticosterone
responses to captivity (changes in baseline corticosterone and
stress responses over time) were unrelated to their restraint

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Fig. 2. Comparisons of corticosterone response to a restraint stressor over a week of

captivity in Kenyan house sparrows: (a) raw delta corticosterone (30 min postrestraint minus baseline); (b) % change relative to value at capture from the wild.
Bars are means 1SE; betas denote effects of xed factors in best-t models. For
both (a) and (b), random effects of individual (intercepts only) were maintained in
best-t models (see Table 1).

induced stress responses at the time of capture. In other words,

within individual sparrows, exibility in one type of corticosterone
regulation was unrelated to exibility in others. Below, we discuss
how such regulatory exibility might impact vertebrate range
expansions generally, including the likely sources of variation in
this integral homeostatic process.

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4.1. Physiological personalities

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Perhaps one of the most rapidly growing areas in behavioral

ecology is the study of individual variation (Bell, 2007; Sih et al.,
2004). We are learning that individuals tend to have consistent
patterns of behavior (i.e., personality), and we are learning that
the context-dependency of behaviors (i.e., plasticity) is more variable in some individuals than others (Dingemanse and Wolf, 2013).
We are also nding that personality and plasticity often covary,
constraining the diversity of behaviors used by some individuals
(Carter et al., 2012). Altogether, this nascent sub-discipline is
revealing new insight into individuality (Dingemanse and Wolf,
2010) and its ramications for key ecological and evolutionary processes (Sih, 2013). It is surprising then that physiological equivalents of personality and plasticity have been so little considered
(Lessells, 2008; Williams, 2008), especially in wild animals
(Ouyang et al., 2013). Whether individuals are physiologically consistent is rarely studied, even though consistency and exibility is
integral to homeostasis. Part of the reason for so few studies probably stems from the large sample sizes required to estimate accurately individual plasticity (Martin et al., 2011), which is why it
was not addressed in the present study. Nevertheless, steroids,

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Please cite this article in press as: Martin, L.B., Liebl, A.L. Physiological exibility in an avian range expansion. Gen. Comp. Endocrinol. (2014), http://
dx.doi.org/10.1016/j.ygcen.2014.07.016

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Mombasa
Nairobi
Nakuru

slope of captivity effect on BL CORT

a
8
6
4
2
0
-2
0

slope of stress resp in wild

slope of captivity effect on stress resp

b
20
10
0
-10
-20
-30
0

slope of stress resp in wild

slope of captivity effect on stress resp

15
10
5
0
-5
-2

slope of captivity effect on BL CORT

Fig. 3. No relationship between various forms of HPA plasticity: (a) slope of wild
stress responses versus slope of captivity effect on stress responses; (b) slopes of
captivity effects on BL and stress responses; and (c) slope of wild stress responses
and captivity effect on BL corticosterone. Points depict linear slope estimates from
individual sparrows.

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neuropeptides, and other physiological parameters so often mediate individual phenotypic variation through complex and regulated
changes (Koolhaas et al., 1999; Sih et al., 2004), and physiological
processes so often covary (Cockrem, 2007; Korte et al., 2005;
Martin et al., 2011b; Ricklefs and Wikelski, 2002), that there are
strong reasons to expect a predominance of physiological personalities in nature. Here, we provide some of the rst evidence that
wild individual birds exhibit corticosterone regulatory personalities (Carere et al., 2010).
To reveal consistency in corticosterone regulation in Kenyan
sparrows, we repeatedly measured captive individuals because a
similar approach in free-living individuals could have obscured
our ability to detect true plasticity (Dingemanse et al., 2010). If
we had studied wild individuals, individuals most or least sensitive

to initial capture could have been differently represented at later

time points. Nevertheless, some subtle differences in study design
notwithstanding (i.e., length of time in captivity), our data reveal
uniqueness in the regulation of corticosterone in Kenyan house
sparrows compared to other populations and species. In most other
avian studies, baseline corticosterone tends to increase and remain
elevated over weeks (Dickens et al., 2009; Fokidis et al., 2011;
Kuhlman and Martin, 2010) sometimes subsiding to levels slightly
higher than at capture. Stress responses tend to diminish over captivity, perhaps because the steroidogenic capacity of the adrenals
becomes exhausted (Romero et al., 1998). These observations elicit
the following questions: why do Kenyan sparrows continue to
escalate corticosterone concentrations in response to perceived
adversity; would corticosterone regulation come to resemble other
populations given more time; and, how do Kenyan sparrows protect their tissues from sustained high corticosterone? Answers to
these questions might lie in the complexity of glucocorticoid regulation (Wingeld, 2013b). We already know that Kenyan populations differ in levels of hippocampal expression of glucocorticoid
receptors (Liebl and Martin, 2013); range-edge birds express proportionally fewer mineralocorticoid receptors (MR) than glucocorticoid receptors (GR), which may facilitate negative feedback
control of corticosterone relative to birds from older sites
(Sapolsky et al., 2000). Perhaps populations (or individuals) also
vary in the degree of plasticity of GR or MR expression. It would
be intriguing (but technically challenging) to investigate this possibility, as well as if levels of steroid binding globulins (Breuner
et al., 2013) and enzymes that convert corticosterone to lowactivity or inactive forms (Sapolsky et al., 2000). Finally, additional
measurements of corticosterone (i.e., time points >7 days postcapture) might reveal that Kenyan birds simply take longer to
adjust to captivity than other species.
Another type of answer lies in the relative value of elevated corticosterone to range edge versus resident birds. In regards to baseline corticosterone, we cannot make a strong case that elevations
in captivity are adaptive, as we did not expect to see such strong
and persistent increases. Other captive birds begin to reduce baseline corticosterone by 7 days post-capture (Cavigelli and
McClintock, 2003; Hau et al., 2010; Smith and Blumstein, 2008),
but levels typically remain elevated (relative to wild baseline levels) for long periods thereafter. Whether the same would have
occurred in Kenyan sparrows if they were given more time is
unknown. Our focus in this study mostly revolved around stress
responses though, because baseline corticosterone did not differ
among sites. Instead, previous work revealed that range-edge birds
have stronger stress responses (Liebl and Martin, 2012) than corecaught birds, and we expected that birds from older populations
might come to resemble range edge birds if held captive. That outcome was observed, but a corticosterone rise in range edge birds
was also observed; we expected increases in stress responses in
all populations, but not near-doublings even in the population with
already strong responses. Ongoing work is attempting to link
changes in corticosterone to cognitive performance among populations and individuals. As with many other studies, we face the
conundrum whether the same concentration of hormone has the
same consequence for individuals from different locales (Bonier
et al., 2009; Breuner et al., 2008; Martin et al., 2005), which is
why we report percent changes in corticosterone as well as raw
values.

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Glucocorticoid traits are heritable (Almasi and Jenni, 2010;

Evans et al., 2006), so genetic variation and selection thereof probably explains some differences in corticosterone regulation among
sites and individuals. However, given the strong bottleneck that

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dx.doi.org/10.1016/j.ygcen.2014.07.016

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occurred in Kenya (Schrey et al., 2011), the recency of the introduction (Summers-Smith, 1988), extensive anthropogenic movement
of birds throughout Kenya (Schrey et al., 2014), and observations
in other systems (see below), we expect that various forms of phenotypic plasticity is probably also important (Snell-Rood, 2012).
First, in birds, early-life experiences can (but do not always) alter
corticosterone regulation into adulthood (Lynn et al., 2010;
Schoech et al., 2011; Spencer et al., 2009). Thus, corticosterone regulatory capacity might be programmed in early-life; for some personalities, high exibility might persist into adulthood whereas in
others, early-life experiences may x HPA responsiveness permanently (Dingemanse and Wolf, 2013). Second, in rodents, some
enduring alterations to the hypothalamuspituitaryadrenal
(HPA) are epigenetically mediated (Weaver et al., 2004). Such
epigenetic changes can be trans-generationally heritable via methylation of promoters of key genes (e.g. hippocampal GR). We have
not determined whether epigenetic mechanisms (Ledn-Rettig
et al., 2013), heritable or not, explain differences in corticosterone
regulation in Kenyan house sparrows, but whole-genome level epigenetic variation is very high among individuals (Liebl et al.,
2013a). Third and most generally, phenotypic variation in many
species can be extensive in spite of minor genetic variation, but
this reality has been greatly under-emphasized until recently
(West-Eberhard, 2003). Indeed, if a single genotype can encode
both a tadpole and an adult frog (Martin et al., 2011b), many house
sparrow genotypes might produce an invasive phenotype given the
right environment (Earley et al., 2012; Snell-Rood, 2012).
One likely lucrative area to explore in regards to the development of regulatory exibility is trait covariation. We found that
individual identity contributed substantially to stress response
variation (Table 1). However, the lack of correlations between
individual slope coefcients for different types of corticosterone
plasticity (Fig. 3) and the comparative lack of consistency in baseline corticosterone reveal that corticosterone regulatory processes
experience few constraints in Kenyan house sparrows. Although
covariation and constraint have been much discussed in ecophysiology (Hau, 2007; McGlothlin and Ketterson, 2008; Sinervo and
Calsbeek, 2003), neither has been evaluated (to our knowledge)
in the manner used here, so we cannot discern whether our results
are exceptional or typical. Indeed, corticosterone responses may be
similarly unconstrained in many taxa, but rarely is corticosterone
studied in the manner of our study, even though it is plasticity in
these hormones that makes them homeostasis mediators [95].
One study we conducted recently (using a different approach)
revealed that long-term resident house sparrows (Tampa, FL,
USA) exhibited seasonal dependency in covariation among glucocorticoid regulatory elements (Liebl et al., 2013b); during molt,
corticosterone regulatory traits were correlated, but during breeding they were not. These data, which come from a long-term resident population, suggest that Kenyan birds may indeed be special
in term of corticosterone exibility, but as the study design is quite
distinct, such a conclusion would be premature.

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5. Conclusion

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As stress hormones and their effects on performance vary over

seconds to minutes up to hours to days (Martin, 2009), it is important to learn whether regulatory exibility at different time scales
is constrained and whether and how any covariation impacts
organismal performance (Woods and Wilson, in press). Likewise,
interactions among physiological systems warrant more attention,
as these interactions too are likely to impact the ecology and evolution of phenotypes (Cohen et al., 2012; Martin and Cohen, in
press). In the future, we advocate for assessments of physiological
exibility across multiple contexts and spatiotemporal scales
(Dingemanse and Wolf, 2013); inclusion of state/condition/health

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into such studies could be illuminating too (Carere et al., 2010;

Wada et al., 2008). Personality-plasticity covariation within individuals may often manifest because of differential investments in
insurance (Mathot and Dingemanse, in press) or because feedback
loops once instigated reinforce individual differences (Sih and Bell,
2008). We expect that the regulatory variation we detected is
adaptive (Wolf et al., 2008), but we hope to test this expectation
in the future. Likely, individuals that are less guided by environmental stimuli and readily develop rigid phenotypic traits (i.e.,
proactive) are competitive late in invasions whereas individuals
that are more guided by environmental stimuli and hence more
plastic (i.e., reactive) are competitive at range edges (Dingemanse
and Wolf, 2013; Mathot and Dingemanse, in press). Corticosterone
regulation is costly (McEwen and Wingeld, 2003), and any costly
form of phenotypic plasticity should enable frequency-dependent
selection to maintain multiple personalities in populations
(Dingemanse and Wolf, 2013). Thus, over time, we expect that this
extensive exibility will subside, which is perhaps why older populations in the US (Liebl et al., 2013b) seem to exhibit much less
plasticity than the birds now in Kenya.

481

Acknowledgments

501

We thank members of the Martin lab for discussions of the data,

Onesmus Kioko, Vincent Otieno, and Ronald Mulwa for help in the
eld, two anonymous reviewers for comments to a previous verQ3
sion of the manuscript, and NSF funding to L.B.M. (IOS-0920475) Q4
and A.L.L. and L.B.M. (IOS-1209747). The authors have no conicts
of interest in publishing this work.

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Please cite this article in press as: Martin, L.B., Liebl, A.L. Physiological exibility in an avian range expansion. Gen. Comp. Endocrinol. (2014), http://
dx.doi.org/10.1016/j.ygcen.2014.07.016

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Please cite this article in press as: Martin, L.B., Liebl, A.L. Physiological exibility in an avian range expansion. Gen. Comp. Endocrinol. (2014), http://
dx.doi.org/10.1016/j.ygcen.2014.07.016