Age and aerobic performance in deer mice
Department of Biology, University of California, Riverside, CA 92521, USA
* Author for correspondence (e-mail: chappell{at}citrus.ucr.edu)
Accepted 22 January 2003
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Summary |
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Key words: age, basal metabolism, maximal oxygen consumption, aerobic capacity, thermogenesis, ventilation, mammal, deer mouse, Peromyscus maniculatus
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Introduction |
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As well as being interesting from a functional perspective, an
understanding of age effects is relevant for field studies of adaptation
especially those that hinge on performance comparisons between
contrasting environments or selective regimes because population
demographic structure is often complex and it is usually difficult to
determine the age of free-living animals. Without data on age effects and
demography, results from inter-population comparisons may be difficult to
interpret. In this paper, we use a small mammal, the North American deer mouse
Peromyscus maniculatus, as a model system to examine age effects on
several frequently measured aspects of aerobic performance: basal metabolism
(BMR), maximum aerobic capacity in exercise
(O2max) and thermogenesis
(
O2sum), and
ventilatory traits that support the initial stages of oxygen uptake. We also
explore age-related changes in body size, composition and organ mass, in order
to put our data on aerobic performance into an appropriate physiological
context.
Aerobic performance in deer mice has been intensively studied. Much is
known about aerobic capacity changes in relation to temperature acclimation or
acclimatization (Hayes and Chappell,
1986,
1990
; Hayes,
1989a
,b
),
and considerable work has focused on adaptations to oxygen availability in
P. maniculatus, which inhabit a large altitudinal range (from below
sea level to above 4000 m). Across North America, deer mouse populations show
an array of polymorphisms in the
-chains of hemoglobin that are
geographically correlated with altitude
(Snyder 1981
;
Snyder et al., 1988
),
influence blood oxygen affinity and differentially affect aerobic performance
at low and high altitude (Chappell and
Snyder, 1984
; Chappell et al.,
1988
). Field studies at a high altitude site suggest that natural
selection favors high aerobic capacity in thermogenesis (Hayes,
1989a
,b
;
Hayes and O'Connor, 1999
).
Deer mice live for more than five years in captivity (Peromyscus
Genetic Stock Center,
http://stkctr.biol.sc.edu;
University of South Carolina; K. A. Hammond, unpublished data). Therefore, the
potential exists for a substantial age range in wild populations, making a
study of age-related changes in aerobic performance and morphology an
important component of our understanding of altitude adaptation in these
mice.
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Materials and methods |
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Our experimental design was cross-sectional (i.e. we used measurements from only one age for each mouse). For most ages, we used a randomly chosen subset of the available animals in our colony, but for the oldest mice (>1300 days), we tested every available individual. If an animal was measured at two different ages (as was the case for all animals older than 1700 days), we used only the final set of measurements in analyses.
Oxygen consumption measurements
We used open-flow respirometry to determine basal and maximal exercise and
thermogenic aerobic performance as rates of oxygen consumption
(O2). Changes in
O2 concentration were measured with Ametek/Applied Electrochemistry
S-3A analyzers and recorded on Macintosh computers equipped with National
Instruments A-D converters and custom software (Warthog Systems,
www.warthog.ucr.edu).
Gas flow was regulated with Tylan and Applied Materials mass flow controllers
upstream from the metabolism chambers; we used flow rates that maintained
O2 concentrations above 20.4% in all measurement conditions.
Approximately 100 ml min-1 of sample gas was scrubbed of
CO2 and water vapor (soda lime and drierite) and routed through the
oxygen sensors. We calculated
O2 (in ml
min-1) as:
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Basal metabolism
Basal metabolic rate (BMR) was measured during the animals' inactive phase
(07.00 h-16.00 h local time) after overnight fasting (>10 h), which is
sufficient to empty the gut (K. A. Hammond, unpublished data). Metabolism
chambers (lucite boxes, volume 525 ml) were maintained at 30-32°C (within
the thermal neutral zone of deer mice;
Chappell, 1985) in an
environmental cabinet. A small quantity of wood shavings was provided as
bedding, and airflow rates were 500-600 ml min-1 STP. 3-min
reference readings were obtained automatically every 45 min with a solenoid
manifold operated by the computer. Measurement periods were 1.5-4 h (depending
on how quickly animals became quiescent), after which mice were removed from
chambers and fed. We computed BMR as the lowest
O2 averaged over
continuous 5-min intervals during periods when
O2 was low and
stable.
Aerobic capacity in exercise
Maximum O2
during exercise
(
O2max) was
determined by running mice in an enclosed motorized treadmill
(Chappell, 1984
;
Chappell and Snyder, 1984
;
Hayes and Chappell, 1990
). The
treadmill's working section was 6 cm wide, 7 cm high and 13.5 cm long, and the
total enclosed gas volume was approximately 970 ml. We used a flow rate of
2100 ml min-1 STP of dry air. To begin a test, we placed a mouse in
the treadmill's working section and allowed a 1-2-min adjustment period before
starting the tread at low speed (approximately 0.3 m s-1). We
increased tread speed in increments of approximately 0.1 m s-1
every 30-60 s (depending on how well the animal ran) until the mouse could no
longer maintain position and
O2 did not
increase with increasing speed, at which time the tread was stopped. After the
end of exercise, we continued to monitor metabolism until
O2 had clearly
begun to decrease. All mice showed behavioral signs of exhaustion at the end
of exercise, but none was injured. Tests lasted 6-17 min (2-13 min of tread
movement). Reference readings of incurrent gas were obtained at the start and
end of measurements.
Because of the relatively large volume of the treadmill and the short
duration of exercise tests, we applied the `instantaneous' correction
(Bartholomew et al., 1981) to
compensate for mixing characteristics and to resolve short-term changes (BMR
and thermogenic
O2 were
determined using steady-state equations). Effective volume of the treadmill
respirometer, calculated from washout curves, was 903 ml. We computed
O2max as the
highest instantaneous
O2 averaged over
continuous 1- and 2-min intervals (Chappell
and Snyder, 1984
; Chappell et al., 1998).
Thermogenic capacity and ventilation
Maximal thermogenic
O2, or summit
metabolism
(
O2sum), was
measured by exposing mice to moderately low temperatures in heliox (21%
O2:79% He by volume). Heat loss rates are several times higher in
heliox than in air (Rosenmann and
Morrison, 1974
), and we could quickly elicit
O2sum at ambient
temperatures (Ta) between 0°C and -10°C, depending
on the size and thermogenic capacity of the mouse. Use of these relatively
warm temperatures minimized the risk of cold injury (no animal suffered
frostbite during our study).
The metabolic chamber was constructed of lucite and contained a small
amount of wood shavings. Chamber volume was 460 ml and heliox flow was 1700 ml
min-1 STP. We started runs at a Ta of 0°C
to -5°C and monitored
O2 as
Ta dropped at a rate of approximately 1 deg.
min-1. When
O2 began to
decline, or if it remained constant over a 5°C drop in
Ta, we terminated the test and returned the mouse to its
cage. Measurements lasted 6-15 min. As for
O2max, we took
reference readings at the start and end of measurements and computed
O2sum as the
highest
O2
averaged over continuous 1- and 2-min intervals.
We used the heliox metabolism chamber as a whole-body plethysmograph to
monitor ventilation frequency (f) and tidal volume
(VT) when animals attained
O2sum.
High-resistance orifices in incurrent and excurrent gas lines increased the
chamber's time constant for pressure fluctuations to a value considerably
longer than the duration of inspiration and expiration. This permitted
simultaneous measurements of ventilation and
O2
(Malan, 1973
;
Bucher, 1981
). Pressure changes
were detected by an Omega PX 164-010 transducer, amplified and sampled at 125
Hz by a computer, providing 10-11 data points breath-1 at the
highest observed f. A water manometer measured the difference
(0.5-0.9 kPa) between chamber and ambient pressure. For each mouse, the system
was calibrated by injecting 10-12 boluses of gas (1.0 ml) into the chamber at
rates yielding pressure change kinetics similar to those during inhalation.
For VT calculations, we assumed lung temperature
(TL) was 35°C (based on body temperature measurements
from a subset of individuals), ambient water vapor pressure was equivalent to
saturation values (0.3-0.7 kPa at a Ta between -10°C
and 0°C) and alveolar gas was 100% saturated with water vapor. Based on
the accuracy of TL estimates and calibration injections,
and noise levels in the plethysmograph signal, maximal errors in computed
VT were <8%. The analysis software calculated
f over 20-70 sequential ventilation cycles, with a maximal error of
<2% (usually <1%). Minute volume
(
min; measured in ml
min-1) is the product of f and VT.
Oxygen extraction (EO2; measured as a
percentage) was computed as
100x
O2/(FEO2x
min).
Body composition
We obtained body composition data from a subset of animals that included
98% of the age range in the main sample
(Fig. 1). After metabolic tests
were complete, we anesthetized mice (0.07 ml of 65 mg ml-1 sodium
pentobarbitol injected i.p.) and used retro-orbital puncture to obtain blood
samples (approximately 150 ml) in two heparinized microhematocrit tubes.
Samples were centrifuged for 10 min at 1000 g, and hematocrit
was calculated as the mean proportion of packed cells relative to total sample
volume.
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After euthanization (additional 0.1 ml of 65 mg ml-1 sodium pentobarbitol injected i.p.), we removed all gut contents and measured wet and dry carcass mass. We also measured wet and dry masses of the heart and lungs. Fat was extracted from the dried carcass and organs using petroleum ether (Kerr et al., 1982) in a Goldfische apparatus to determine dry lean mass. We estimated absolute fat content by subtraction (dry carcass mass before extraction minus dry carcass mass after extraction) and computed relative fat content as percentage of wet carcass mass. Lean mass was estimated as the difference between wet carcass mass and absolute fat mass.
Analysis and statistics
We did not obtain complete data for all individuals (e.g. several mice
remained active throughout measurements and did not provide valid BMRs). Data
from animals discovered to be diseased (e.g. tumors found at dissection) were
discarded. We used covariance analysis (ANCOVA; with mass and age as
covariates) to test for differences among categorical variables (sex), and
multiple regression to test relationships among continuous variables. Bounded
data (EO2, hematocrit, fractional lean tissue
and fat content) that were not normally distributed were arcsine square-root
transformed prior to analysis.
The relationship between age and several morphological, metabolic and
ventilatory variables appeared to change abruptly between 1 and 2 years of age
(Figs 2,
3). For such data (including
mass, O2max,
O2sum,
VT and
min), we searched for
`breakpoint' ages with a piecewise regression algorithm that iteratively
adjusts the breakpoint in a two-phase regression until the overall sum of
squares is maximized (Nickerson et al.,
1989
; Statistica instruction manual, Statsoft, Inc., Tulsa, OK,
USA). The critical significance level
was 0.05; we used a sequential
Bonferroni correction to adjust
in multiple simultaneous tests
(Rice, 1989
). Statistics were
performed using JMP and Statistica software for the Macintosh (SAS Institute,
Inc., Cary, NC, USA and Statsoft, Inc., respectively) and a custom-written
Bonferroni correction program.
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Results |
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Size effects
Mass was strongly correlated to BMR,
O2max,
O2sum,
VT and
min, but not to f
or EO2
(Table 1). As is typical for
mammals, the metabolic rates of our deer mice scaled as power functions of
body mass, with mass exponents across all ages combined of 0.762 for BMR (mean
after accounting for gender differences; see below), 0.732 for
O2max and 0.573
for
O2sum.
However, across the body mass range in this study (10.4-41.9 g), power
functions fit the data only slightly better than least-squares
regressions.
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Two-phase regressions between body mass and metabolism revealed inflection
points at an age of approximately 485 days
(Fig. 2; see below). In young
mice (<485 days), mass exponents were 0.834 for BMR, 0.915 for
O2max and 0.812
for
O2sum. In
older mice, mass exponents decreased: 0.690 for BMR, 0.693 for
O2max and 0.522
for
O2sum.
Sex differences
Our protocol was not designed to test for gender differences in life span,
but there were few apparent differences in survivorship between males and
females. Our small sample of the oldest animals suggests better survivorship
in males: of 10 mice that reached 1350 days (3.7 years), five were females,
but of the five that exceeded 1750 days (4.8 years), only one was a
female.
Mice of both sexes increased body mass as they aged, and males averaged approximately 13% heavier than females (Fig. 2; F1,205=24.5, P<0.00001; ANCOVA with age as the covariate). However, after correction for age and body mass, neither hematocrit nor any measured body composition variable (heart mass, lung mass, lean mass, fat mass and fractional lean and fat content) differed significantly between males and females (P>0.1 in all cases).
An ANCOVA with age and body mass as covariates revealed few sex differences in metabolism and ventilation. Only BMR and f were significantly affected by gender. After correcting for age and mass, female BMRs were approximately 9% higher than those of males [0.780 ml min-1 and 0.716 ml min-1 at a standard (mean) mass of 22.4 g, respectively; F1,201=8.2, P=0.0046]. Mass exponents for male and female BMR did not differ significantly. Male f was approximately 6% higher than that of females (8.21 breaths s-1 and 7.77 breaths s-1 at standard mass, respectively; F1,200=7.8, P=0.0057).
Age effects
The piecewise regression algorithm identified growth rate breakpoints at
469 days (females) and 492 days (males). In mice older than the breakpoint
age, the relationship between age and mass was significant in females
(r=0.33, P=0.01, with a growth rate of approximately 0.0022
g day-1) but not in males (r=0.06, P=0.60). In
younger mice, the corresponding relationships were significant (females:
r=0.45, P=0.0024; males: r=0.33, P=0.036),
with growth rates for both sexes averaging approximately 0.0118 g
day-1.
Because mass changed with age, we included mass as a covariate in all
analyses of age effects. There were significant age effects on both
O2max and
O2sum but not on
BMR (Table 2). Maximal
O2 decreased
with age, with 5-year-old mice having approximately 22% and 30% less
mass-adjusted aerobic capacity than 100-day-old mice in exercise and
thermogenesis, respectively. As for growth rate, the decline in mass-adjusted
maximal
O2 with
age began abruptly (Fig. 2).
Piecewise regression found breakpoints at 485 days and 483 days in
O2max and
O2sum,
respectively (Figs 2,
4; we assume the difference in
breakpoints for growth rate,
O2max and
O2sum are
statistical artefacts and not real differences). Since no animals in the data
set were between 444 days and 492 days of age and all breakpoints (for mass,
O2max and
O2sum) were at
or between these ages, we refer to mice aged <485 days as `young' and mice
aged >485 days as `old'. After correction for mass changes, age was not a
significant predictor of
O2max or
O2sum in young
deer mice but had a strong effect in old mice
(Table 2).
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Breathing frequency during maximal thermogenesis (f) was
correlated with age but not with
O2sum in
females, while the reverse was true in males
(Table 3). Oxygen extraction
(EO2) was independent of mass but declined with
age in both sexes. However, there was no apparent inflection point in the
relationship between age and either f or
EO2 (Fig.
3). Two ventilatory variables (VT and
min) changed abruptly at
approximately 485 days (Fig.
3). However, this may have been a consequence of the relationship
between age, mass and
O2sum; after
accounting for the effects of
O2sum and mass,
VT and
min were not correlated
with age in either sex.
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Relationships among metabolic and ventilatory indices
After correction for mass and age, BMR approached significance as a
predictor of
O2max for old
mice (partial r=0.174, P=0.058, N=122) but was not
correlated with
O2max in young
mice or with
O2sum in either
age class (partial r=0.10, P
0.15, N=82-204).
The mean
O2sum
was 12% and 8% higher than
O2max in young
and old mice, respectively (Fig.
4), and the ratio between the two indices showed considerable
variance (Fig. 5) that was not
affected by either age or sex (P=0.10 and P=0.15,
respectively; interaction, P=0.50). Nevertheless,
O2max was
strongly correlated to
O2sum in both
young mice (partial r=0.30, P=0.0066, N=82) and old
animals (partial r=0.53, P<0.00001, N=121).
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Body mass did not influence VT and
min, but these variables
were significantly correlated to
O2sum
(Table 3). After correcting for
age and mass, f did not affect VT (partial
r=-0.07, P=0.31, N=199); thus, more rapid breathing
did not necessitate reduced VT (within the measured range
of f and VT). Similarly, VT
was not correlated to lung mass after correcting for
O2sum, age and
body mass (partial r=0.11, P=0.42, N=55).
Body composition
Animals used for body composition studies showed the same general
relationship between aerobic performance and age seen in the complete data
set: after mass correction, age had no effect on BMR or on maximal
O2 in the 28
animals younger than 485 days. In old mice, both
O2max and
O2sum declined
significantly with age (r=-0.382, P=0.041 and
r=-0.465, P=0.011, respectively).
Simple correlations with body mass were significant for heart, lung, fat
mass and lean mass. Heart and lung masses were correlated, and fat content (as
a percentage of body mass) was positively correlated to
O2max in young
animals and to
O2sum in old
animals. However, after correction for both age and lean tissue mass, fat
content and lung and heart mass were not significantly correlated to any
metabolic variable except for
O2max in young
animals (Table 4).
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Aside from its effects on body mass, age had no influence on body
composition in young deer mice, but several aspects of body composition tended
to change with age in old animals (>485 days;
Table 5). Therefore, we tested
whether age-related declines in aerobic performance in old mice could be
explained by age-related changes in body composition. Other things being
equal, maximal performance should be positively correlated to fractional lean
tissue content and negatively correlated to fractional fat content. Because
O2max and
O2sum declined
with age in deer mice, that hypothesis predicts a decline in fractional lean
tissue content with age. However, we found a different pattern: fractional
lean tissue tended to increase with age, while fractional fat content declined
with age (although neither relationship was significant after Bonferroni
correction; Table 5). Also,
after correcting for mass and fractional fat and lean content, we found no
influence of age on
O2max,
O2sum or BMR for
young mice or for all ages combined (Tables
6,
7), but an identical test in
old mice revealed negative correlations between age and both
O2max and
O2sum (again,
neither relationship was significant after Bonferroni correction). Taken
together, these findings suggest that the decline in performance with age is
not simply a result of body composition changes.
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Discussion |
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We found no change in aerobic physiology with age in young deer mice
(<485 days old) other than mass scaling due to increases in body size with
age. Within this age group, the three measured aerobic indices (BMR,
O2max and
O2sum) had mass
exponents (0.812-0.915) close to those reported in interspecific studies
across a wide range of body mass (e.g.
Seeherman et al., 1981
;
Calder, 1984
). Young deer mice
grew continuously, gaining about 4.8 g between 50 days and 485 days of age (a
total mass increase of approximately 28%; mean for both sexes combined).
Growth slowed in older animals (with no significant mass change in old
males) but we did not see the declines in body mass that often occur in the
later part of the life span in laboratory rodents
(Sprott and Austad, 1996).
More importantly, we found a substantial decline in mass-adjusted whole-animal
performance in old mice (Fig.
4). Relative to a 100-day-old deer mouse weighing 22.5 g, a
5-year-old individual of the same mass has approximately 22% less aerobic
capacity in exercise
(
O2max=4.92 ml
O2 min-1 vs 3.84 ml O2
min-1) and 30% less aerobic capacity in thermogenesis
(
O2sum=5.46 ml
O2 min-1 vs 3.81 ml O2
min-1). Interestingly, these changes in maximal aerobic power
output were not reflected in mass-adjusted BMR, which showed no significant
change with age (see also O'Connor and
Buffenstein, 2000
). Consequently, the factorial aerobic scope in
exercise
(
O2max/BMR)
declined from 6.4-6.5 in 100-day-old mice (means for males and females,
respectively) to 4.9-5.8 in 1800-day-old animals, a reduction of 10-25%.
Corresponding values for thermogenic scope were 7.2-7.3 (100 days) and 5.0-5.9
(1800 days), a decline of 19-31%.
There are surprisingly few reports of aerobic performance changes across
the life span in small mammals, but there is an extensive literature on the
effects of age on human performance, including aerobic capacity and athletic
competition. These data serve as a useful frame of reference for our results
with Peromyscus. As for deer mice, human aerobic capacity declines
considerably with age: between the third and the seventh decade of life, the
O2max of both
athletes and untrained males decreases by 35-45%
(Goldberg et al., 1996
).
Similarly, maximal work rate during bicycle ergometry declines by
approximately 1.3% annually (Stones and
Kozma, 1985
) or a 40% reduction over 40 years. Human athletic
performance in long-duration races that are highly dependent on aerobic power
output shows similar trends. For example, in distance running events (0.8-42
km), slopes of loge-transformed race times on age are about 0.01
for men and 0.02 for women (Stones and
Kozma, 1985
), which equates to speed decreases of roughly 30-50%
over 40 years. Comparable reductions occur in strength tests (e.g. a 30%
decline in maximum handgrip force over 40 years;
Stones and Kozma, 1985
). When
normalized to fractions of life span, the magnitude of age-related performance
changes in humans (30-50% declines in several indices between the third and
seventh decade) are somewhat greater than those seen in deer mice (22-30%
reduction of aerobic capacity between 100 days and 1800 days).
As a second frame of reference, it is instructive to compare the impacts of
age on aerobic performance with the magnitude of two other factors that are
known to affect deer mouse aerobic physiology: phenotypic plasticity in
temperature acclimation and genetic adaptation of hemoglobins to different
altitudes. In Peromyscus and many other small rodents, exposure to a
cold environment in the laboratory or the field induces large increases in
thermogenic capacity (e.g. Rosenmann et
al., 1975; Heimer and
Morrison, 1978
; Wickler,
1980
). The
O2sum of deer
mice held at 3-5°C for 3 months was 31% greater than that of controls held
at 20-22°C (Hayes and Chappell,
1986
), and in wild deer mice in California, winter acclimatization
increased
O2sum
by up to 50% (Hayes,
1989a
,b
).
Thus, the impact of age (up to a 30% reduction in
O2sum in very
old mice) is equivalent to a substantial fraction of the effects of
temperature acclimation on thermogenic capacity.
Deer mice have a diverse array of -globin polymorphisms that are
geographically correlated with altitude
(Snyder et al., 1988
) and
affect blood oxygen affinity (Chappell and
Snyder, 1984
). Studies of genetically standardized laboratory
lines and wild-caught samples (comprised primarily of young animals) indicate
that mice with the `correct' hemoglobin for either low or high altitude (in
these tests, 340 m vs 3800 m) have a performance advantage of
approximately 10% in both
O2max and
O2sum
(Chappell and Snyder, 1984
).
That difference which was proposed as a selective mechanism for the
evolution of the hemoglobin polymorphisms is considerably less than
the potential effects of age on aerobic performance in these mice.
Body composition and performance changes
Decreases in age-related aerobic performance in mice older than 485 days
could have several functional explanations. At the whole-animal level, they
could result from a decline in the mass-specific power output capacity of
central `supply' organs (heart, lungs, etc.) or peripheral effectors (skeletal
muscle or, for thermogenesis, brown adipose tissue). Declines with age in
muscle fiber force generation per cross-sectional area in laboratory mice and
rats (Thompson and Brown,
1999; Gonzalez et al.,
2000
) are consistent with this hypothesis. Alternatively,
mass-specific activities of central and peripheral organs could be unchanged
with age, but overall body composition (e.g. the proportions of fat
vs lean tissue or the proportion of lean tissue allocated to
different organs) could differ.
Our results with deer mice are most consistent with the first hypothesis (a
decline in mass-specific lean tissue function with age). We found no
consistent age-related changes in lean tissue mass, heart mass or lung mass in
old mice (other than those in proportion to changing body mass;
Table 4), indicating that the
relative size of these organs did not decline as the mice grew older and
whole-animal maximal power output decreased (in fact, the fraction of total
body mass comprising lean tissue tended to increase with age;
Table 4). In this respect, deer
mice apparently differ from humans: age-related declines in human exercise
performance are in large part due to reductions in proportional muscle mass
(summarized in Stones and Kozma,
1985), although a number of other factors are also important
(summarized in Goldberg et al.,
1996
).
Ecological and evolutionary considerations
In terms of behavior and ecology, the effects of 22-30% decreases in
aerobic capacity are likely to be highly significant for old deer mice.
Running speed in mammals is a linear function of metabolic power output
(Taylor et al., 1970), so the
maximum sustainable running speed of a 5-year-old deer mouse will be
approximately 20% lower than that of an equal-sized young mouse. It is also
likely that endurance at high exercise intensities will be concomitantly
reduced in old animals. Although deer mice seem unlikely to depend on
endurance performance for very critical behaviors (such as escaping from
predators), sustainable locomotor capacity is an important component of their
ecology. Wild deer mice in a high-altitude population in the White Mountains
of eastern California (from which our colony originated) routinely travel
hundreds of meters during nocturnal activity periods
(Hayes, 1989a
;
Hayes and O'Connor, 1999
), so
a decrease in exercise capacity could have a significant impact on home range
size and hence resource availability.
Age-related declines in thermogenic capacity may be even more important to
deer mouse ecology. Previous calculations from lab studies
(Chappell and Snyder, 1984;
Chappell and Holsclaw, 1984
)
and data on field metabolic rates (Hayes,
1989a
,b
)
suggest that at typical nighttime temperatures at our White Mountains field
site (approximately 0-5°C in summer and -5°C to -20°C in winter),
deer mice are operating close to their maximal aerobic capacity. Therefore,
the age-related decline we found in
O2sum would
seriously constrain their capacity for activity at low temperatures.
Consistent with that estimate, Hayes and O'Connor,
(1999
), working at the same
site, found evidence of selection favoring high thermogenic
O2 in wild deer
mice (survivorship was positively correlated to
O2sum). An
important caveat for these conclusions stems from lack of cold acclimatization
in our test animals. As discussed above, long-term cold exposure induces large
increases in
O2sum in deer
mice. It is unknown if the age-related decline in
O2sum we found
in warm-acclimated mice is also evident after cold acclimation, but the
simplest assumption is that it is.
Despite their potential for substantial impacts on important ecological
factors, it is doubtful that age-related aerobic performance declines have
tangible evolutionary significance for deer mice. This seemingly contradictory
conclusion stems from population age structure: most rodents (including deer
mice) and other small mammals have very short mean life spans, even after
attaining reproductive adulthood (e.g.
Millar, 1989;
Price and Kelly, 1994
;
Duquette and Millar, 1995
). A
life table is not available for deer mice from our White Mountain source
population, but it is unlikely that more than a small fraction of wild deer
mice attain the `breakpoint' age of 485 days
(Hayes and O'Connor, 1999
).
Even fewer continue to survive long enough to experience biologically
meaningful declines in aerobic performance, and fewer still will have a chance
to reproduce at such an advanced age. This demographic structure greatly
reduces the power of selection to generate evolutionary change in heritable
performance declines that appear only in old individuals
(Williams, 1957
;
Hamilton, 1966
;
Charlesworth, 1980
;
Rose, 1991
).
One final caveat is worthy of consideration. Due to the constraints of our
`cross-sectional' experimental design, the youngest animals in our data set
were the products of several more laboratory generations (up to 5) than the
oldest individuals (generation 2). Even without intentional artificial
selection, captive breeding often results in evolutionary adaptation to
culture conditions (i.e. domestication), so it is conceivable that our results
show genetic change between generations instead of the effects of age. That
seems unlikely, since the direction of change higher performance in
younger animals from later laboratory generations is opposite to what
is expected from genetic adaptation to relatively benign laboratory conditions
(a decline in performance with domestication; e.g.
Swallow et al., 1998).
Laboratory rearing appears to reduce the aerobic performance of deer mice:
wild-caught individuals had higher performance than lab-bred mice even after
the latter were acclimated to local altitude and temperature
(Chappell and Snyder, 1984
;
Hayes,
1989a
,b
;
Hammond et al., 2002
).
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Acknowledgments |
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References |
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