Morphological and enzymatic correlates of aerobic and burst performance in different populations of Trinidadian guppies Poecilia reticulata
1 Department of Biology, University of California, Riverside, CA 92521,
USA
2 Department of Biological Science, California State University, Fullerton,
CA 92834, USA
Author for correspondence (e-mail:
Mark.Chappell{at}ucr.edu)
Accepted 15 July 2003
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Summary |
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Organ size and enzyme activities showed substantial size-independent
variation, and both performance measures were strongly correlated to body
size. After accounting for size effects, neither burst nor aerobic performance
was strongly correlated to any organ size or enzymatic variable, or to each
other. Two principal components (PCI, PC2) in both males and females accounted
for most of the variance in the organ size and enzymatic variables. In both
sexes, heart and gill mass tended to covary and were negatively associated
with citrate synthetase and lactate dehydrogenase activity. In males (but not
females), variation in aerobic performance was weakly but significantly
correlated to variation in PC1, suggesting that heart and gill mass scale
positively with
O2max. Neither
of the component variables and no single morphological or enzymatic trait was
correlated to burst speed in either sex.
Evolutionary changes in important life history traits occur rapidly in guppy populations subjected to different predation intensities (high mortality in downstream sites inhabited by large predatory fish; low mortality in upstream sites lacking large predators). We found significant differences between stream drainages in all morphological variables and most enzymatic variables, but only the mass of the swimming motor and LDH activity were significantly affected by predation regime. Overall, our data show that microevolution has occurred in the physiological foundations of locomotor performance in guppies, but evolutionary changes in physiology do not closely correspond to the predation-induced changes in life history parameters.
Key words: locomotion, swimming, predation, life history, burst speed, aerobic capacity, guppy, Poecilia reticulata, trade-off, lactate dehydrogenase, myofibrillar ATPase, citrate synthetase
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Introduction |
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We examined these questions in a system that offers particularly clear
insights into microevolutionary change: the cluster of guppy populations
(Poecilia reticulata Peters) on the island of Trinidad. Life history
evolution in these fish has been extensively studied by David Reznick, John
Endler and their colleagues. Guppies are native to rainforest drainages
throughout the mountain ranges of Trinidad, and occur even in very small
tributaries (Reznick and Endler,
1982). Local habitats range from shallow, slow-moving, low-volume
pool- and-riffle systems (often interspersed with barrier waterfalls) to
large, deep, fast-flowing rivers. Variation in stream topography, along with
other factors, results in striking interpopulation differences in predation
regimes and mortality rates (large guppy predators occur in high-volume
downstream habitats but are absent above barrier waterfalls). In turn,
differences in predation are associated with large and genetically determined
differences in life history parameters such as age at first reproduction and
offspring number and size (Reznick,
1982
; Reznick and Endler,
1982
; Reznick et al.,
1996
). Experimental manipulation of predation in natural habitats
has revealed surprisingly rapid evolutionary change in life history traits
(Reznick and Bryga, 1987
;
Reznick et al., 1990
,
1997
).
Given the variation in stream hydrodynamics, large and genetically based
differences in life history, and quick response to selection in guppy
populations, a natural question is: has whole-animal physiological performance
also evolved in these fish and, if so, what are the mechanistic causes of
performance differences? Previous studies have reported population differences
in some aspects of locomotor performance
(Cullum and Bennett, 1995;
Odell and Chappell, in press
).
In this paper we use within- and between-population variation to examine
several physiological characters underlying aerobic capacity (the metabolic
foundation of sustainable swimming) and burst speed (presumably crucial in
escape from predators and other emergency responses). Both traits require the
effective and coordinated functioning of a suite of enzymes, organelles,
cells, tissues, organs and organ systems, and hence are useful integrative
physiological indices. We studied burst and aerobic performance at several
levels of integration, from the intact animal (size and shape) to organ
systems (heart, gill and swimming motor mass) to several muscle enzymes
commonly used as indicators of aerobic and anaerobic capacity
(Childress and Somero, 1979
;
Dickson et al., 1993
;
Gibb and Dickson, 2002
). We
also examined the effects of natural predation regimes (defined as the
presence or absence of large guppy predators such as the pike cichlid
Crenicichla alta; Reznick and
Endler, 1982
) on morphology and enzyme activity.
We tested four specific hypotheses. (1) Variance in aerobic capacity should
be positively correlated with variance in the size of the heart and gills (key
organs in oxygen uptake and delivery) and with citrate synthetase activity (an
indicator enzyme for oxidative metabolism and hence for the amount of
slow-twitch 'red' muscle in the swimming motor). (2) Variance in burst
performance should be positively correlated with variance in the size of the
swimming motor (comprising mainly fast-twitch glycolytic fibers;
Veggetti et al., 1993) and
with lactate dehydrogenase (an indicator enzyme for glycolytic ATP production
and fast-twitch muscle) and myofibrillar ATPase activities. (3) Due to
trade-offs, there should be a negative correlation between aerobic and
glycolytic traits. (4) Because of pleiotropic interactions with life history
traits and direct selection by predators, organ size and enzyme activities
should differ consistently in upstream (low-predation) and downstream
(high-predation) populations. The numerous natural population replicates of
guppies, and their amenability to laboratory culture, allowed us to use a
'common-garden' approach to control for environmental effects and reveal
genetic differences.
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Materials and methods |
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All F2 and F3 offspring were reared under
standardized conditions (water temperature 24.5±1°C and an ad
libitum diet of commercially available granular food and liver paste;
Reznick and Bryga, 1987). For
each generation, two fry were collected daily from stock tanks (to provide
roughly equal representation of offspring from each wild-caught ancestor). Fry
were reared together in population-specific 18 liter tanks until mature, and
then individually housed in 7.25 liter tanks during the measurement period.
Females were not gravid during experiments. All aspects of the care and use of
animals in this study were approved by the institutional animal care and use
committee of the University of California, Riverside, USA.
Because of logistical constraints, we simultaneously reared upstream and downstream populations from the same drainage, while populations from different drainages were reared sequentially. That design allows robust comparisons between upstream and downstream (low- and high-predation) habitats, but the temporal separation in rearing fish from different drainages introduces the possibility of uncorrected 'block' effects in comparisons among drainages.
Whole-animal performance
Aerobic performance and burst speed were measured for each animal
(Odell, 2002;
Odell and Chappell, in press
).
Briefly, we measured maximal oxygen uptake rates
(
O2max) during
forced exercise using closed-system respirometry. The cylindrical respirometry
chamber contained an adjustable magnetic stirbar, which generated a variable
current that the fish swam against. Current speed was increased in a stepwise
fashion every 2 min until fish began to swim unsteadily and fatigued (i.e.
failed to maintain position). Output from an oxygen microelectrode
(Strathkelvin Instruments, Glasgow, Scotland) was sampled by a computer and
converted to oxygen content. Oxygen saturation remained above 84% in these
tests and validation studies revealed no decrease in exercise performance at
O2 saturations as low as 60-70%
(Odell and Chappell, in
press
). Oxygen consumption rate
(
O2) was
calculated as the time derivative of oxygen content, and we computed
O2max as the
highest continuous average
O2 over a 1 min
period during forced swimming, using custom software ('LabAnalyst';
http://warthog.ucr.edu).
The
O2max
measured in this way is repeatable over periods of 7 and 90 days
(Odell and Chappell, in
press
).
Burst performance during the escape response (C-start) was measured as
maximum speed over a short interval (we used maximum speed because it is less
prone to measurement error than other burst indices such as acceleration or
rates of body bending; Walker,
1998). Guppies were filmed at 500 frames s-1 with a
MotionScope camera (RedLake Instruments, San Diego, CA USA); C-starts were
initiated by tapping on the side of the tank with a small metal object. Video
recordings were captured to a Macintosh computer and digitized over 50-100
sequential frames (100-200 ms). Within that interval, we determined the
maximal forward velocity of the bending axis (approximately the center of
mass) over 20 ms, using custom software ('Motion Analysis';
http://warthog.ucr.edu).
This measurement is highly repeatable, at least over short inter-measurement
intervals (several minutes; Odell and
Chappell, in press
).
Morphology
After performance measurements were completed, guppies were euthanized with
a lethal dose of MS-222. Wet mass M and standard length SL
were determined and fish were bisected transversely immediately posterior to
the anus. Tail portions were weighed (to ±0.1 mg) and immediately
frozen in liquid nitrogen for use in enzyme analyses. Anterior portions were
preserved in 5% formalin. Hearts (ventricle tissue only) and gills were
dissected from preserved fish under a 20x microscope, placed
individually in the wells of plastic microtiter plates, dried overnight at
55°C, and weighed to the nearest µg using an electrobalance (Cahn C-41;
Cahn Instruments, Madison, WI, USA). We were particularly careful to harvest
hearts and gills in a standardized manner to insure equivalent sampling of
these small organs in all fish. The head and viscera were removed from the
anterior portion of the carcass and the remainder was weighed to ±0.1
mg. The mass of the 'swimming motor' (primarily muscle, but also containing
bone and skin) was calculated as the sum of the masses of the eviscerated
headless anterior carcass and the tail portion.
For an index of shape differences, we used the relationship between wet mass and standard length, based on the principle that the mass of geometrically similar bodies should vary as the cube of linear dimensions. Thus, if guppies from different populations have similar shapes, they should exhibit a constant ratio of M1/3/SL, and we computed that ratio for each individual.
Enzyme activities
We assayed the swimming motor for an aerobic marker enzyme (citrate
synthetase, CS), an anaerobic marker enzyme (lactate dehydrogenase, LDH), and
myofibrillar ATPase, an enzyme with activity proportional to the speed of
fiber contraction (Barany,
1967; Johnston and Walesby,
1977
). Because we had small amounts of tissue (especially in
males), we assayed the entire post-anal tail assembly.
Tail assembly tissue was homogenized in ground-glass tissue grinders in 20
volumes (females) or 40 volumes (males) of extraction buffer containing 10
mmol l-1 Tris-HCl, pH 7.2 at 20°C, 1% Triton X-100 (w/v), 5
mmol l-1 ETDA, 100 mmol l-1 KCl. The crude homogenate
was centrifuged for 10 min at 7500 g, and the supernatant was
assayed for CS and LDH activity. To obtain myofibrils
(Watkins, 2000), the pellet
was washed and resuspended in 2 ml of extraction buffer and centrifuged again
for 10 min at 7500 g. This procedure was repeated three times,
each time discarding the supernatant. After the third centrifugation, the
pellet was resuspended in 500 µl of rinse buffer (30 mmol l-1
Tris-HCl, 150 mmol l-1 KCl, pH 7.2 at 0°C) and assayed for
myofibrillar ATPase activity.
Enzyme activities were determined under saturating substrate conditions in a microplate spectrophotometer (Molecular Devices, Inc., Sunnyvale, CA, USA). In all assays, the reaction volume was 160 µl, and included 10 µl of either supernatant or myofibril suspension. Assays were performed in duplicate and with a simultaneous negative control (no substrate). In addition, a blank reaction (no enzyme) was run on each plate. Reaction mixtures were as follows. Citrate synthetase: 80 mmol l-1 Tris, pH 8.0 at 20°C, 2 mmol l-1 5,5'-dithio-bis(2-nitrobenzoic acid), 400 mmol l-1 MgCl2, 0.1 mmol l-1 acetyl coenzyme-A, 0.5 mmol l-1 oxaloacetate (omitted in control), absorbance read at 412 nm at 25°C. Lactate dehydrogenase: 3.2 mmol l-1 NADH, 500 mmol l-1 KCl, 50 mmol l-1 imidazole buffer pH 7.0 at 20°C, 1.0 mmol l-1 pyruvate (omitted in control), absorbance read at 340 nm at 25°C. Myofibrillar ATPase: a commercially available kit (EnzChek® phosphate assay kit E-6646; Molecular Probes, Inc., Eugene, OR, USA) was used to measure the presence of phosphate released by the hydrolysis of ATP. After pre-incubating the samples at 25°C for 2 min to remove endogenous phosphate, the reaction was initiated with 1 mmol l-1 ATP and the rate of change in absorbance was measured at 360 nm.
Total protein concentration (mg ml-1) was determined for both supernatants and resuspended myofibril pellets by Bradford assay (BioRad, Hercules, CA, USA), using a gamma globulin standard. We expressed enzyme activities as i.u. mg-1 protein in the sample (1 i.u. = µmol substrate converted to product per minute). Protein content variation in both phases was low and we did not reject data from any individual because of unusually high or low total protein (i.e. there were no noticeable outliers). However, a problem with protein precipitation during the purification stages compromised myofibrillar ATPase results for Yarra drainage females, and these data had to be discarded.
Statistical analyses
Performance, organ size and some enzyme activities were strongly related to
body size (Table 1), so for
most population comparisons we used analysis of covariance (ANCOVA, with size
as a covariate) or residuals of log-log mass regressions (using wet mass).
Because of minimal size overlap, the sexes were analyzed separately in most
tests.
|
We looked for patterns in combinations of organ mass and enzymatic
variables using principal components analysis (PCA) of a Pearson
product-moment correlation table. PCA creates composite variables that are
relatively independent of one another
(Tabachnick and Fidell, 1996).
Because composite variables are orthogonal, they reduce the problem of
collinear data when analyzed by multiple regression. Preliminary analysis
revealed that the overall relationships did not differ among drainages or
locales, so data for all individuals within a sex were pooled. Parallel
analysis (Franklin et al.,
1995
) was used to determine significant eigenvalues for component
retention. The contribution of each raw variable to the composite variables
was considered significant if its factor loading was
0.316, meaning that
it accounted for >10% of the variation in that component. Relationships
between whole-animal performance and retained PCA axes were examined with
multiple regression. Composite variables were also analyzed by ANOVA with
drainage and predation regime as the main effects.
Analyses were performed using JMP 4.0.4 (SAS Institute, 2000),
Statistica/Mac 4.1 (1994 Statsoft Inc.), and SAS/Mac 6.12 (1996 SAS
Institute). The significance level () was 0.05; for multiple
simultaneous tests (e.g. correlation matrices) we adjusted
using a
sequential Bonferroni correction (Rice,
1989
) to avoid Type I errors.
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Results |
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All organ size measurements (heart, gill and swimming motor mass) and both performance traits were positively correlated with body size in both sexes (Table 1), but most variables scaled allometrically with mass (Table 2).Among enzymatic variables, LDH activity scaled positively with mass in both sexes, while CS activity scaled negatively with mass in males. There were no significant effects of size on CS activity in females or on myofibrillar ATPase activity in either sex.
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The range of variation in mass-adjusted organ size and enzyme activity
indices was 5-32% (Figs 2,
3), with the lowest variation
in swimming motor mass. After removing the effects of mass
(Table 3), neither
O2max nor burst
speed was significantly correlated to any single morphological or biochemical
variable in either sex. In addition,
O2max and burst
speed were not significantly correlated to each other (i.e. there was no
evidence of a tradeoff between burst and aerobic performance). Gill and heart
mass, and CS and LDH activities, were positively correlated in both sexes but
no other mass-adjusted variables were consistently related in both males and
females.
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Relationships among groups of variables
Principal components analysis indicated that interactions among groups of
morphological and biochemical variables were complex, inconsistent between
males and females, and largely unrelated to burst or aerobic performance. PCA
yielded two significant component axes for each sex
(Table 4). The fraction of
variation in the data set accounted for by retained components was 54.6% in
males and 60.5% in females.
|
In males, the first PC axis (PC1) was described by heart, gill, swimming motor, CS and LDH residuals. Heart and gill residuals were negatively related to swimming motor mass, CS and LDH residuals. The second PC axis (PC2) was characterized by residual ATPase activity at one end, and gill, CS and LDH residuals at the other.
In females, ATPase was not included because of flawed data from Yarra fish. In the remaining 99 females, PC1 was described by a negative relationship between heart and gill residuals and the enzyme residuals (LDH and CS). The second axis described a negative relationship between swimming motor residuals and heart and CS residuals.
Multiple regression of performance on composite PC variables explained no
more than 5% of performance variation
(Table 5) and was significant
for only one analysis: in males, there was a slight but significant negative
relationship between residual
O2max and PC1,
suggesting that aerobic performance in males increases with heart and gill
mass and decreases with increasing swimming motor mass and muscle enzyme
activities.
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Population and drainage comparisons
All organ mass variables and most enzymatic variables (except myofibrillar
ATPase activity) differed significantly among drainages, and most variables in
both categories were affected by sex (Tables
6,
7). The range of variation in
drainage means (minimum to maximum) was 8% for swimming motor mass, 30% for
heart mass, 34% for gill mass, 16% for CS activity and 29% for LDH activity
(Table 8). There were numerous
significant interaction terms that included drainage effects.
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In contrast to the widespread effects of sex and drainage, only the size of the swimming motor and (with marginal significance) LDH differed between low- and high-predation populations. On average, fish from low-predation environments had slightly but significantly larger swimming motors (64.8% of body mass) than did fish from high-predation environments (63.1% of body mass), and this effect was apparent in all three drainages. Males had significantly larger swimming motors than females (67.2% versus 60.6% of body mass, respectively) but the relative magnitude of the difference between predation regimes was about the same for both sexes. LDH activity averaged about 6% higher in low-predation populations.
There was substantial variation in PC variables among populations, but
little consistency with predation regime
(Fig. 4). Male PC1 scores
differed in naturally occurring high-low predation pairs (Oropouche and Yarra
drainages). However, this pattern was not observed in the Caroni drainage,
which was field-manipulated within the last 25 years
(Reznick and Bryga, 1987).
Males from the Oropouche drainage had the highest overall PC1 scores,
consistent with greater swimming motor mass and LDH and CS activities. PC2
varied with predation regime but not between drainages. In the naturally
occurring stream pairs (Oropouche and Yarra), low-predation guppies had higher
PC2 scores, suggesting that they have increased gill mass and CS and LDH
activities. Guppies in high-predation locales had higher myofibrillar ATPase
activities.
|
Significant drainage effects occurred in both component scores in females. Females from high-predation regimes had significantly higher PC1 scores on two of the three drainages. Interestingly, this difference was strongest in the experimentally manipulated Caroni drainage. In general, females from high-predation locales had higher residual activities of CS and LDH and smaller gill and heart masses. PC2 scores differed in only the Yarra drainage, with higher PC2 scores in upstream (low-predation) fish. This suggests that low-predation Yarra females had larger hearts and higher CS activities than high-predation Yarra females. Oropouche females had the lowest overall PC2 scores, indicating that they had the highest residual swimming motor mass.
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Discussion |
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Accordingly, we began our study of guppy locomotor physiology expecting to find positive correlations between aerobic performance and aerobic organs and enzymes (heart and gill mass; CS activity), positive correlations between burst performance and glycolytic organs and enzymes (swimming motor mass; LDH and myofibrillar ATPase activities), negative correlations (trade-offs) between burst and aerobic traits, and consistent differences between morphology and enzyme activities between upstream (lowpredation) and downstream (high-predation) populations. Somewhat to our surprise, the results gave little support to any of these predictions.
Size effects on performance
Both of the measured locomotor performance indices were strongly correlated
to body size (and consequently organ size; Tables
1,
2): as expected, large guppies
have higher absolute aerobic capacities and can swim faster than small
guppies. However, after correcting for body size, there were few significant
correlations between either
O2max or burst
speed and any organ size or enzymatic variable
(Table 3), andBonferroni
correction for multiple simultaneous tests suggests that the small number of
significant individual correlations may be statistical artifacts (Type I
errors).
Aerobic and anaerobic trait associations
We found several significant associations among mass-adjusted morphological
and enzymatic traits (Table 3),
but only the positive relationships between heart and gill mass, and between
LDH and CS activities, occurred in both sexes. The correlation between heart
and gill - two organs closely associated with oxygen uptake and transport - is
not surprising, although neither organ significantly predicted locomotor
performance.
We did not anticipate the positive correlation between LDH and CS, since
these enzymes (indicative of glycolytic and oxidative muscle fibers,
respectively) were expected to exhibit a trade-off. Lack of such a trade-off
could have several causes. At the whole-animal level, amounts of oxidative and
glycolytic fibers may be positively correlated because of individual
differences in total muscle mass. However, CS and LDH remained significantly
correlated (P<0.006 in both sexes) after inclusion of swimming
motor mass in the regression (which should largely account for differences in
muscle mass). Alternatively, since glycolytic fibers are the predominant fiber
type in the guppy swimming motor (Veggetti
et al., 1993), these results may reflect a positive correlation
between LDH and CS activity within glycolytic fibers, as has been shown in
interspecific comparisons of fish muscle
(Dickson et al., 1993
;
Dickson, 1995
). Small animal
size and use of whole-muscle homogenates did not allow enzyme activities to be
assayed directly and independently from each fiber type.
Other unexpected findings were a negative correlation between LDH and
myofibrillar ATPase activities in males (both enzymes should have maximal
activities in glycolytic fibers and hence should covary;
Leonard, 1999;
Watkins, 2000
), and lack of
correlation between ATPase activity and swimming motor size.
We hypothesized that organ sizes and enzyme activities should covary according to function and therefore expected that principal components analysis (PCA) would separate clusters of distinctly anaerobic and aerobic variables, either at opposite ends of a component axis, or on different axes. The results (Table 4) provide little support for this idea. In females, there was a distinct gradient between two aerobic variables (heart and CS) and residual swimming motor mass (an 'anaerobic' trait due to the high fraction of glycolytic fibers) on the second PC axis, but a very different pattern occurred along PC1 (the extremes - gill and CS - are both aerobic traits). In males, two aerobic traits (heart and gill) were closely associated at one end of the PC1 axis, with two anaerobic traits (LDH and swimming motor mass) clustered at the other end, as expected. However, CS (an aerobic trait) and ATPase (an anaerobic trait, given its association with rapid contraction velocity and high activity in fast-twitch glycolytic fibers) were both intermediate. On PC2, there was a gradient from two aerobic traits (CS and gill) to two anaerobic traits (swimming motor mass and ATPase), but heart and LDH were not in their predicted positions. In no case did either PC axis cleanly separate all variables into the expected groupings.
In general - for both simple correlations and PCA - we did not find
evidence for functional competition between aerobic and anaerobic
morphological and enzymatic traits in guppies. In terms of whole-animal
locomotor physiology this is not surprising, since guppies apparently are not
constrained to 'trade off' aerobic and anaerobic swimming performance (as
indicated by lack of negative correlation between burst speed
andO2max after
mass correction; Table 3;
Odell, 2002
;
Odell and Chappell, in press
).
In other words, these fish may show individual variation in combined exercise
capacity (both burst and sustainable swimming), instead of being constrained
to specialize in either burst speed or aerobic performance but not both.
Similar results were reported for Atlantic cod Gadus morhua by Reidy
et al. (2000
): individuals
with high sprint speeds during escape responses also had high maximum
sustainable swimming speeds.
Mechanistic foundations of performance
Both singly and in PCA combinations, the measured organ mass and enzymatic
traits accounted for only a small fraction of the variation in mass-adjusted
aerobic performance in males (and essentially none in females), and no single
or combined variables were significantly correlated to burst speed (Tables
3,
5). This is somewhat
surprising, as similar studies in a number of species have shown substantial
size-independent performance correlates with organ size or enzyme function.
For example, aerobic performance (measured as
O2max) is
positively correlated to heart mass in house sparrows
(Chappell et al., 1999
), male
red junglefowl (Hammond et al.,
2000
), and garter snakes
(Garland and Bennett, 1990
).
Aerobic performance also correlated positively with muscle mass in house
sparrows and male junglefowl, and with muscle CS activity in the latter
(Hammond et al., 2000
).
Watkins (2000
) reported a
relationship between burst speed and myofibrillar ATPase in tadpoles. However,
some studies found little or no correlation between whole-animal performance
traits and morphology (Garland and Huey,
1987
; Garland and Else,
1987
; Bennett et al.,
1989
) or enzyme function (Gibb
and Dickson, 2002
). The absence of consistent patterns suggests
that mechanistic factors that determine performance capacity in vertebrates
may be taxon-specific or very complex.
Population differences and predation effects
In previous work we found no effect of predation regime on either burst or
aerobic performance in Trinidadian guppies, but there were small differences
in aerobic capacity between drainages
(Odell, 2002;
Odell and Chappell, in press
).
Other studies of guppy burst speed (Cullum
and Bennett, 1995
) and ability to escape capture by large
predatory fish (O'Steen et al.,
2002
) did find differences between animals from
high-versus low-predation environments. The contrast between those
results and ours may stem from differences in measurement techniques (the
superior escape ability of high-predation guppies may be due to aspects of
burst performance we did not quantify, such as response time or acceleration
during the early phases of the escape response) or acclimation (Cullum and
Bennett used wild-caught fish instead of laboratory-reared guppies). Whatever
the reason for these apparently contradictory results for whole-animal
locomotor traits, morphological and enzymatic comparisons of fish from
different drainages and predation regimes are of considerable interest.
We found strong effects of drainage on all three organ size indices and all but one of the three measures of enzyme activity (Tables 6, 7, 8). Use of F2 and F3 fish reared under identical 'common-garden' conditions makes it likely that the inter-drainage differences had a genetic basis. They may be due to genetic drift (founder effects) or to selection arising from abiotic (hydrodynamics, water chemistry, etc.) or biotic (productivity, food availability, food quality, etc.) differences between drainages. However, caution is appropriate when postulating a genetic basis for inter-drainage differences because our experimental design, although robust for comparisons of contrasting predation regimes within drainages, did not completely control for 'block' effects in comparisons between drainages.
In contrast to the numerous differences between drainages, only two
variables, swimming motor mass and LDH activity, were significantly affected
by predation regime, and the direction of change was counterintuitive for
both: fish from high-predation populations, which presumably need additional
muscle power for rapid escape from attacks, had smaller swimming motors and
lower LDH activities than fish from low-predation populations. Patterns in
data for PCA axes (Fig. 4)
suggest some differentiation among high- and lowpredation guppies. In males,
high-predation fish from both of the naturally occurring high/low predation
stream pairs in our sample (Oropouche and Yarra drainages) had lower PC2
scores than their low-predation upstream counterparts, suggesting that
high-predation fish had increased myofibrillar ATPase activity. However, this
difference was not evident in the Caroni stream pair containing an
experimentally transplanted low-predation population dating from the early
1980s (Reznick et al., 1990).
In females, individuals from two high-predation sites - including the Caroni
drainage - tended to have higher PC1 scores, an indication that they possessed
higher overall muscle enzyme activities than low-predation animals from the
same drainage. The low-predation experimental Caroni population was
established recently, so differences between these fish and their ancestors
from high-predation downstream Caroni habitats have evolved relatively
quickly.
In summary, our results show that large differences in guppy life history
traits - including those that impact the allocation of resources to
reproductive or somatic functions - can evolve with little or no concomitant
effects on locomotor and aerobic performance and its underlying physiological
mechanisms. We found only two clear contrasts between guppies from low- and
high-predation populations: small differences in the relative size of the
swimming motor and in LDH activity. Those differences - a larger swimming
motor and higher LDH activity in low-predation populations - are opposite to
what would be expected from selection on escape ability (e.g.,
O'Steen et al., 2002), but fit
one prediction of life history theory (reduced somatic investment in
populations with high mortality rates).
In that context it is appropriate to emphasize the crucial role of body
size in locomotor performance as well as life history. In our study, both
measures of performance were strongly correlated with animal mass: larger
guppies swam faster and had higher aerobic capacity than smaller individuals.
Given the ecology of guppies in Trinidad, size, locomotor performance and life
history interact in complex and sometimes contradictory ways. Guppies grow
more rapidly in high-predation downstream habitats than in low-predation
upstream sites (apparently because of differences in food availability, not
genetic factors; Rodd and Reznick,
1997; Reznick et al.,
2001
). However, because of higher mortality rates
(Reznick et al., 1996
),
guppies in downstream populations are, on average, younger and hence smaller
than guppies from upstream populations
(Rodd and Reznick, 1997
). Our
data on the effects of size on swimming performance indicate that, despite
strong predator-mediated selection on escape ability
(O'Steen et al., 2002
),
guppies from high-predation downstream habitats are probably, on average,
slower in absolute burst speed than their larger counterparts from upstream
low-predation sites.
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Acknowledgments |
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Footnotes |
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