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First published online December 14, 2007
Journal of Experimental Biology 211, 35-41 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.012658
Development partly determines the aerobic performance of adult deer mice, Peromyscus maniculatus
1 Department of Biology, University of California at Riverside, Riverside, CA
92521, USA
2 Integrative Ecology Group, Estación Biológica de Doñana,
CSIC, Apdo. 1056, E-41080 Sevilla, Spain
* Author for correspondence (e-mail: gruss001{at}student.ucr.edu)
Accepted 24 October 2007
 |
Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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O2max) between
high and low altitude populations of small mammals. However, it remains
unclear to what extent development at different oxygen partial pressures
(PO2) can affect aerobic performance during
adulthood. Here we compared the effects of development at contrasting
altitudes versus effects of acclimation during adulthood on
O2max. Two
groups of deer mice were born and raised for 5 weeks at one of two altitudes
(340 and 3800 m above sea level). Then, a subset of each group was acclimated
to the opposite altitude for 8 weeks. We measured
O2max for each
individual in hypoxia (PO2=13.5 kPa, 14%
O2 at 3800 m) and normoxia (PO2=20.4
kPa, 21% O2 at 340 m) to control for
PO2 effects. At 5 weeks of age, high altitude
born mice attained significantly higher
O2max than low
altitude born mice (37.1% higher in hypoxia and 72.1% higher in normoxia).
Subsequently, deer mice acclimated for 8 weeks to high altitude had
significantly higher
O2max regardless
of their birth site (21.0% and 72.9% difference in hypoxia and normoxia,
respectively). A significant development x acclimation site interaction
comparing O2max
in hypoxia and normoxia at 13 weeks of age suggests that acclimation effects
depend on development altitude. Thus, reversible plasticity during adulthood
cannot fully compensate for developmental effects on aerobic performance. We
also found that differences in aerobic performance in previous studies may
have been underestimated if animals from contrasting altitudes were measured
at different PO2.
Key words: acclimation, aerobic performance, hypoxia, developmental canalization, phenotypic plasticity, O2max
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Guderley and St-Pierre, 1996),
high salinity (Tay and Garside,
1975) and hypoxia (Hochachka,
1988; Singer,
1999; West, 1991).
Recently, much attention has focused on how humans and other mammals cope with
the rigors of montane and other high altitude environments (e.g.
Hochachka et al., 1982;
Curran et al., 1998;
Hammond et al., 1999;
Hammond et al., 2001;
Hammond et al., 2004;
Hayes, 1989a;
Hayes, 1989b;
Hayes and Shonkwiler, 1996;
Hayes and O'Connor, 1999;
Rezende et al., 2001;
Rezende et al., 2005;
Sheafor, 2003). In particular,
small mammals living at high altitude face several important challenges
because of their size. Energy demands increase because they are active in low
ambient temperatures, but hypoxia limits aerobic metabolism so it is harder to
fuel these needs. Additionally, primary productivity is often low at high
altitude so there are fewer resources to fuel higher demands
(Hammond et al., 2004).
Studies comparing populations from high and low altitudes have reported a
variety of physiological differences that were initially interpreted as
adaptations (in a Darwinian sense) to different altitudes and oxygen partial
pressures (PO2). However, subsequent studies
have shown that chronic exposure to high altitude (i.e. acclimation or
acclimatization) can result in important physiological responses (e.g.
McClelland et al., 1998;
McClelland et al., 2001),
suggesting that differences between populations might be partly determined by
phenotypic plasticity. Although some studies have attempted to control for
acclimatory effects when comparing aerobic performance across populations or
species inhabiting different altitudes (e.g.
Rezende et al., 2001;
Hammond et al., 2001), the
role of development as a source of variation has not been previously addressed
(but see Chappell et al.,
2007). Disturbances of the developmental process, whether genetic,
environmental or phylogenetic, may not be reversible (developmental
canalization) and can result in significant variability within a species
(Spicer and Gaston, 1999;
Dzialowski et al., 2002;
Spicer and Burggren,
2003).
Therefore, we tested whether developmental effects can contribute to
variation in aerobic metabolism during adulthood. We focused on maximum
aerobic performance during exercise
(O2max) because
of the large role aerobic exercise plays in an organism's everyday life,
particularly at high altitude (Pough,
1980; Hayes and Shonkwiler,
1996). We used the North American deer mouse (Peromyscus
maniculatus Le Conte) as a model for study for several reasons. Deer mice
inhabit a wide altitudinal range, from below sea level to above 4000 m
(Hock, 1961) and are North
America's most widespread mammal. They also display an array of polymorphisms
in the 
-chains of their hemoglobin that are geographically correlated
with altitude (Snyder, 1981;
Snyder et al., 1988),
influence blood oxygen affinity, and differentially affect aerobic metabolism
at low and high altitude (Chappell and
Snyder, 1984; Chappell et al.,
1988). Finally, field studies at high altitude suggest that
natural selection favors high aerobic capacity during thermogenesis in P.
maniculatus (Hayes and O'Connor,
1999), hence our results are certainly relevant in an evolutionary
context.
|
|
)] are partly responsible for variation in aerobic performance
during adulthood, we expect that reversible acclimation cannot fully
compensate for the effects of developmental acclimation. |
MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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All mice were housed individually in plastic shoebox cages (27 cm x
21 cm x 14 cm) at 23–25°C. They were given ad lib
food (23% protein, 4.5% fat, 6% fiber, 8% ash and 2.5% minerals), water and
bedding. In the lab, they were maintained on a photoperiod cycle that
approximates the natural cycle at Barcroft during the summer months (i.e.
14 h:10 h L:D in mid-July).
O2max during exercise
Maximum O2
was determined using open flow respirometry by running mice in an enclosed
motorized treadmill. The treadmill's working section (the portion of the total
enclosed gas volume that the mouse was constrained to) was 6 cm wide, 7 cm
high and 13 cm long, and the enclosed total gas volume was approximately 970
ml. We used a flow rate of approximately 2100 ml min–1,
standard temperature and pressure (STP) of dry air. Gas flow was
regulated with Tylan and Applied Materials mass flow controllers (Santa
Clarita, CA, USA) upstream from the treadmill. Approximately 100 ml
min–1 of excurrent gas was scrubbed of CO2 and
water vapor (using soda lime and drierite, respectively) and routed through
the oxygen sensors. Changes in O2 concentration were measured with
Ametek/Applied Electrochemistry S-3A analyzers (Naperville, IL, USA) and
recorded on a Macintosh computer with a National Instruments A–D
converter (Austin, TX, USA) using custom-made data acquisition software
(http://warthog.ucr.edu).
We calculated O2
(in ml min–1) as:
 |
is the flow rate (ml
min–1; STP) and
FIO2 and
FEO2 are the fractional oxygen
concentrations of incurrent and excurrent gases, respectively.
To begin a test, after measuring body mass, we placed a mouse in the
treadmill's enclosed chamber and allowed for a 3–5 min adjustment period
before starting the tread at low speed (approximately 0.1 m
s–1). We continued to increase speed in increments of 0.1 m
s–1 every 30 s until the mouse could either no longer
maintain position on the tread or
O2 did not
increase with increasing speed, at which time the tread was stopped. At the
end of the exercise we confirmed that
O2 fell rapidly;
all mice showed signs of exhaustion but none were injured. Tests lasted a
total of 6–20 min. Reference readings of incurrent gas were obtained at
the beginning and end of the trial.
Due to the treadmill's relatively large volume, we applied the
`instantaneous' correction (Bartholomew et
al., 1981) to compensate for mixing characteristics and to resolve
short-term changes in metabolic rate. The effective volume of the treadmill
respirometry chamber, calculated from washout curves, was 903 ml. We computed
O2max as the
highest instantaneous
O2 averaged over
continuous 1 min intervals (Chappell et
al., 1995).
Measurements of aerobic performance for each individual were carried out at
the end of the developmental period (5 weeks of age) and after acclimation (13
weeks of age), at two different PO2 to obtain
comparable measurements simulating high and low altitudes. In Riverside,
measurements were performed with ambient air (normoxia,
PO2=20.4 kPa) and employing a gas mixture of
14% O2 and 86% N2 (hypoxia,
PO2=13.5 kPa). Similar
PO2 values were obtained in Barcroft employing
ambient air (hypoxia) and a mixture of 32% O2 and 68% N2
(normoxia). Despite the mix appearing hyperoxic, these testing conditions
approximate the `normoxic' conditions encountered in Riverside. Ambient
PO2 in Riverside (340 m above sea level) is
20.4 kPa, but at Barcroft (PO2 13.5
kPa), a PO2 of 20.4 kPa can only be achieved by
exposing the animal to a fractional O2 content of 0.32; in this
instance, barometric pressure must be taken into account to know the true
amount of oxygen available to the animal. From here on, we will refer to
measurements made at 20.4 kPa as normoxic and measurements made at 13.5 kPa as
hypoxic.
Analyses and statistics
We initially assessed how body mass and aerobic performance of our mice
changed with age, controlling for effects of developmental and acclimatory
altitudes (below). This was carried out using repeated-measures ANOVA
comparing body mass and aerobic performance obtained at 5 weeks
versus 13 weeks of age. Because aerobic performance was measured at
two different PO2, we performed separate
repeated-measures ANOVAs for hypoxia and normoxia. In addition, we performed
pairwise Pearson correlations between residuals controlling for development
and acclimation site (and for mass differences in the case of
O2max) to
determine whether body mass and aerobic performance were repeatable across
ages and different PO2.
Subsequently, several analyses were performed to disentangle the effects of development and acclimation. To estimate developmental effects in aerobic performance at 5 weeks of age, we compared the aerobic performance of mice born at high versus low altitude with an analysis of covariance (ANCOVA), with birth altitude as the main effect and body mass as a covariate. Because mice were tested twice at different PO2, separate ANCOVAs were performed for measurements in hypoxia and normoxia. To determine whether responses to different PO2 varied as a function of birth site, we employed a repeated-measures ANOVA comparing the aerobic performance of each individual in hypoxia versus normoxia, with birth site as a between-subject factor.
We then compared aerobic performance obtained at 13 weeks of age (5 weeks
of development followed by 8 weeks of acclimation) for the same individuals,
to partition the effects of development versus acclimation in
O2max. We
employed an ANCOVA with both birth altitude and acclimation altitude as main
effects and body mass as a covariate (analyses were performed separately for
hypoxia and normoxia). To determine whether individuals within groups showed
different responses to PO2 during aerobic
performance measurements as a function of development and/or acclimation, we
performed a second repeated-measures ANOVA with birth site and acclimation
site as between-subject factors. Unless stated otherwise, F values
are from these statistical tests and we used an alpha value of 0.05 for
statistical significance.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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O2max measured
in hypoxia, but not in normoxia, was significantly correlated after 8 weeks of
acclimation (P=0.001 and P=0.28, respectively;
Table 2). After accounting for
body mass differences,
O2max in hypoxia
and normoxia was not repeatable over the 8 weeks of acclimation
(Table 2).
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Effects of birth altitude and PO2 at 5 weeks of age
In hypoxia (PO2=13.5 kPa), mice born at high
altitude had a 37% higher
O2max that those
born at low altitude (F1,36=64.1, P<0.0001;
Table 1). When tested in
normoxia (PO2=20.4 kPa), mice born at high
altitude had a 72% higher
O2max than mice
born at low altitude (F1,36=50.7, P<0.0001;
Table 1). Accordingly, the
repeated-measures ANOVA shows that animals born at high altitude attained a
significantly higher
O2max than mice
born at low altitude, regardless of PO2
(between-subject effect, F1,37=36.87,
P<0.0001). Nonetheless, PO2 effects
were more pronounced in animals born at high altitude
(Fig. 2), which is supported by
the significant PO2 x site of birth
interaction in this analysis (F1,37=70.64,
P<0.0001).
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Effects of birth versus acclimation altitude at 13 weeks of age
Regular ANCOVAs comparing
O2max as a
function of birth site and acclimation altitude show that high altitude
acclimated mice attained significantly higher
O2max than
animals acclimated at low altitude in hypoxia and normoxia
(F1,33=22.4, P<0.0001 and
F1,33=56.47, P<0.0001, respectively;
Fig. 3). Although the main
effects of birth site were not significant in these analyses
(P>0.21 in both cases), there was a significant birth altitude
x acclimation altitude interaction for
O2max in both
hypoxia and normoxia (F1,33=6.82, P=0.013 and
F1,33=10.5, P=0.003, respectively). Among animals
acclimated to low altitude, those born at low altitude attained lower
O2max than those
born at high altitude, whereas the opposite pattern was observed among mice
acclimated to high altitude. In other words, mice acclimated to their `native'
altitude had consistently lower
O2max than those
that were switched to the opposite altitude at 5 weeks of age
(Fig. 3).
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Age effects between 5 and 13 weeks
Body mass increased about 4 g during the 8 week duration of the acclimation
(within-individual effect, F1,36=166.13,
P<0.0001). Neither birth altitude nor acclimation altitude
significantly affected growth rate (F1,36=0.34,
P=0.56 and F1,36=0.32, P=0.58,
respectively), and there were no significant interactions (P>0.45
in all cases; Fig. 4).
|
As for aerobic performance,
O2max measured
in hypoxia changed significantly during the 8 weeks of acclimation
(within-individual effect, F1,36=28.2,
P<0.0001; Table 1).
Acclimation altitude was a significant between-individual effect, with
O2max being
significantly higher in mice acclimated at high altitude regardless of their
birth site (F1,36=4.84, P=0.03). Nonetheless, all
interactions were statistically significant (P<0.005 for age
x birth altitude, age x acclimation altitude, and age x
birth x acclimation altitude), showing that the magnitude of change
during the 8 weeks of acclimation depends on birth altitude, acclimation
altitude and the interaction between both
(Fig. 4). Results were
qualitatively identical for measurements in normoxia.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) over the course of 3 months. Chappell et al.
(Chappell et al., 1995)
reported high exercise aerobic performance repeatability in Belding's ground
squirrels (Spermophilus beldingi) over short periods (2 h) and over
months or years in adult animals, but noted no repeatability when animals were
tested as juveniles and later as adults. This measurement period was
significantly longer than ours (1–2 years versus 8 weeks), but
we do point out that physiological traits may not be repeatable across
ontogenetic stages (but see Nespolo and
Franco, 2007). Conversely,
O2max measured
at the same age in different PO2 was
significantly repeatable, suggesting that the physiological basis underlying
this trait remains relatively the same in a given time period (despite the
testing PO2).
PO2 effects on aerobic performance
Several studies have compared
O2 between high
versus low altitudes employing measurements at ambient
PO2 (e.g.
Hammond et al., 2002;
Calbet et al., 2003;
Chappell et al., 2007).
However, this approach does not fully control for
PO2 effects during measurements: whereas mice
from high altitudes were measured in a hypoxic atmosphere, animals from low
altitudes would have been measured in normoxia. Thus, it remains unclear how
phenotypic (anatomical and physiological) responses to chronic exposure to
different PO2 affected aerobic performance,
because acute effects of ambient PO2 were not
accounted for. Our results suggest, for instance, that not accounting for
PO2 may underestimate the degree of
physiological accommodation following high altitude acclimation. Whereas
differences in aerobic performance between groups controlling for
PO2 ranged between 21% and 73%, comparisons
between high altitude mice measured in hypoxia versus low altitude
mice measured in normoxia resulted in differences of around 14% (see middle
two bars in Fig. 2 and
Fig. 3 top panel). As such,
most studies in humans (Gonzalez et al.,
1998; Calbet et al.,
2003; Ventura et al.,
2003) and in small mammals like deer mice
(Hammond et al., 2002;
Chappell et al., 2007) report
significantly higher aerobic performance in high
PO2 environments than in low
PO2 environments. These results, however, might
not reflect the acclimatory physiological responses to chronic exposure to
different PO2. This study controls for
differences in PO2 across different altitudes
by testing animals in multiple PO2
environments, and using this approach we were able to focus on the
physiological accommodations made at high altitude and how they affect aerobic
performance.
Developmental effects versus reversible plasticity during adulthood
We have shown that deer mice residing at 3800 m have a higher
O2max, both
early (Fig. 2) and later in
life (Fig. 3). However, in
terms of aerobic performance, does development at high altitude manifest
itself differently from acclimation as a low-born adult? Apparently, it does.
Our results from regular ANCOVAs and repeated-measures ANOVA show that aerobic
performance during adulthood is partly determined by site of development and
birth. In this context, main effects of birth site were not significant,
suggesting that being born at high or low altitude per se does not
determine whether mice will have a high or a low
O2max during
adulthood. However, the significant interaction term between birth site and
acclimation highlights that the outcome of acclimation to different altitudes
depends on where mice were born and raised (Figs
3 and
4).
These results suggest that developmental canalization partly accounts for
aerobic performance during adulthood, but additional studies are necessary to
disentangle which factors underlie the patterns described here. Mice born at
low altitude apparently have a larger flexibility to increase
O2max when
acclimated to high altitude (Fig.
4), which was quite unexpected and apparently counterintuitive.
This result demonstrates that high PO2 during
in utero development and growth might ultimately enable animals born
at low altitude to attain an increased
O2max compared
with highlander natives following acclimation to high altitude. In this
context, it is worth emphasizing that responses associated with developmental
canalization are not necessarily beneficial or adaptive in a Darwinian sense
(see Wilson and Franklin,
2002). Instead, they might reflect constraints associated with
growing in a more restrictive environment, as might be the case at higher
altitudes with lower PO2. Interestingly, mice
born at high altitude cannot decrease
O2max following
low altitude acclimation to levels comparable with those of animals born at
low altitude. This result reflects `developmental canalization' in a more
traditional sense (Wilson and Franklin,
2002), suggesting that development at high altitude leads to a
constrained degree of plasticity in aerobic performance during adulthood.
To our knowledge, this is the first study to report significant
developmental effects on aerobic performance during adulthood. Future studies
with similar experimental designs may help in elucidating the physiological
basis underlying our results. Aerobic performance is a complex trait that
depends on a variety of subordinate traits in the O2 cascade, hence
it is possible that developmental effects may be detected in subordinate
organs as we have reported here for whole-individual
O2max.
Additional research should primarily focus on traits that are known to be
affected by acclimation at different altitudes. For example, Hammond et al.
(Hammond et al., 1999;
Hammond et al., 2001) reported
that both heart and lung mass were 17% higher in deer mice born at and
acclimated to high altitude when compared with deer mice maintained at low
altitude. Additionally, after acclimation to 3800 m, deer mice increased
hematocrit by 9% (Hammond et al.,
1999; Hammond et al.,
2001) (G.A.R. and K.A.H., unpublished data). All else being equal,
mice with larger cardiopulmonary organs and higher hematocrits should have a
higher aerobic performance (Bishop,
1997; Rezende et al.,
2006). Thus, it would be worth addressing how subordinate traits
at different levels in the O2 cascade might be affected by
different environmental conditions during development
(Burggren and Crossley, 2002).
For instance, it is possible that mice can develop larger hearts when
developing in normoxia, and this might ultimately explain why mice from low
altitude attained the highest
O2max following
acclimation to high altitude.
Summary and perspectives
Deer mice perform better in normoxic PO2
than they do in hypoxic PO2, which is
consistent with previous results in this species. Here, we show this trend is
consistent, regardless of the altitude at which mice reside. This result is
important because it illustrates that previous studies, which have cited
decreased aerobic performance at high altitude, might be reporting the
confounding effects of decreased PO2, not the
real changes in the functional machinery that ultimately determines individual
aerobic performance.
Our data also suggest that mice that have undergone gestational development
at high altitude might have experienced early, rapid growth of the organs and
organ systems that contribute to aerobic performance, and this was manifested
functionally as a high aerobic performance at 5 weeks of age. Low-born mice
acclimated to high altitude late in life were able to generate a high aerobic
performance, especially in normoxia. High-born mice did not experience an
increase in aerobic performance in response to 8 additional weeks of exposure
to high altitude. In this context, although acclimation during adulthood was
able to partly compensate for differences attained during development (see
also Chappell et al., 2007),
we have detected significant and apparently irreversible effects associated
with in utero development and growth at a given altitude. Therefore,
differences between populations inhabiting high and low altitudes can now be
attributed to at least three sources of variation: genetic variation,
phenotypic plasticity during adulthood and developmental effects. Future
studies should therefore address which subordinate traits in the O2
cascade are more susceptible to canalization during development, which traits
are `hard-wired' and not open for modification by the environment
(Spicer and Gaston, 1999), and
how physiological heterokairy of different subordinate traits might ultimately
translate into differences in aerobic performance during adulthood.
|
Acknowledgments |
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