J. therm. Bid. Vol. 20, No. l/2, pp.

23-33, 1995
Copyright 0 1995 ElsevierScienceLtd
Pergamon 0306-4565(94)00023-9 Printed in Great Britain. All rights reserved
0306-4565/95 $9.50 + 0.00

EFFECTS OF TEMPERATURE CHANGE ON ECTOTHERM

METABOLISM AND EVOLUTION: METABOLIC AND
PHYSIOLOGICAL INTERRELATIONS UNDERLYING THE
SUPERIORITY OF MULTI-LOCUS HETEROZYGOTES IN
HETEROGENEOUS ENVIRONMENTS

ANTHONYJ. S. HAWKINS
Plymouth Marine Laboratory, Prospect Place, Plymouth PLl 3DH, U.K.

Abstract-l. Metabolic sensitivity to environmental temperature change increases in positive exponential

relation with initial acclimated rates of energy expenditure, and is influenced by the relative rate with which
intracellular amino acids are being mobilised by protein turnover.
2. Greater metabolic sensitivity results in greater physiological variability with fluctuating temperatures,
higher energy costs incurred during the response to temperature change, and reduced viability upon
exposure to extreme high temperatures.
3. These interrelations help explain the faster production and greater viability of multi-locus het-
erozygotes experimentally exposed to increased temperature and other stressors, as well as ecogeographical
associations indicating the superiority of multi-locus heterozygotes in heterogeneous environments.
4. Implications are discussed for understanding the effects of temperature change on ectotherm
metabolism and evolution.

Key Word Index: Temperature sensitivity; Q,, value; temperature tolerance; protein synthesis; protein
turnover; multi-locus heterozygosity; environmental heterogeneity; physiological evolution; ectotherms

INTRODUCTION work evolves that helps to further understand how

temperature change affects ectotherm metabolism,
One of the most pressing requirements for effective and how genotype influences performance within
resource management is an improved understanding heterogeneous environments.
of the processes effecting physiological evolution
(Prosser, 1955; Bradshaw, 1984; Sibly and Calow,
THE GENETIC REGULATION OF ECTOTHERM
1986; Calow, 1987). These processes may either entail METABOLISM
neutral consequences of mutation, genetic drift and
migration (Kimura and Ohta, 1974), or functional A genetic basis for production is not in question.
consequences of natural selection (Koehn, 1983; But numerous past comparisons of reciprocal trans-
Nevo, 1983). In recent years, mechanistic understand- plants, selected lines and genetically manipulated
ing of how genotype may affect physiological per- animals have provided little insight into the mecha-
formance has been advanced mainly from the study nistic basis of genotype-dependent performance. In-
of multi-locus heterozygosity (Koehn and Shumway, stead, that understanding has mainly developed from
1982; Hawkins et al., 1986; Koehn and Bayne, 1989; relatively recent studies of the metabolic basis
Hawkins, 1991; Koehn, 1991). Environmental tem- whereby, among individuals from natural outbred
perature also exerts a major influence on ectotherm populations, those with higher multi-locus het-
performance, and is of major concern given the erozygosity show faster production in a wide variety
climatic shifts expected with current global warming. of animal and plant species (Mitton and Grant, 1984;
It is therefore timely to synthesize new understanding Zouros and Foltz, 1987). Among ectotherms, faster
of the genetic basis for quantitative physiological production in more heterozygous individuals has
traits with long-established influences affecting the been shown to result from lower mass-specific energy
temperature dependency of metabolism (Fry, 1957; requirements for maintenance metabolism in shellfish
Prosser and Brown, 1961; Newell and Northcroft, (Koehn and Shumway, 1982; Garton et al., 1984;
1967; Bayne, 1973; Newell and Bayne, 1973; Diehl et al.. 1986; Hawkins et al., 1986, 1989), finfish
Newell, 1979). From this synthesis, a common frame- (Danzmann et al., 1987) and salamanders (Mitton

23
24 ANTHONYJ. S. HAWKINS

et al., 1986). Further, it has been shown that most of Nielson, 1988; Wilbur and Hilbish, 1989). Following
those reduced energy requirements for maintenance the acute effects of temperature change, active adjust-
in faster-growing individuals result from savings ments to a new steady state occur over a period of
associated with decreased intensities of protein acclimation or compensation that may last many
turnover, defined as the renewal and replacement of days. Thermal compensation is complete if the rate of
intracellular proteins (Hawkins et al., 1986, 1987, production at this new steady state is similar to that
1989). Reduced protein turnover and maintenance preceding the temperature change. But if production
costs have also been described within many species of remains at a lower rate, then compensation is not
mammal selected for high growth rate (Hawkins, complete, resulting in impaired performance and
1991). Collective findings therefore suggest that possible death (Vernberg and Vernberg, 1972;
differences in animal production result from genetic Prosser, 1973; and other reviews above).
differences in maintenance metabolism. And given Each of these processes differ between species and
that reduced maintenance costs leave more energy populations according to animal size, physiological
available for other processes, those differences have status, nutrition, thermal history and other factors.
other functional consequences for physiological en- Responses also vary according to the rate and ampli-
ergetics and performance (Hawkins, 1991; Koehn, tude of temperature change. Interrelations between
1991; Hawkins and Bayne, 1992). many of these variables have been widely studied (see
It is known that the strength of heterozygosity reviews by Gunter, 1957; Kinne, 1970; Naylor, 1965;
relations may vary according to age, reproductive Bayne, 1976; Newell, 1979). Yet the complexity of
behaviour, environmental influences, and back- many different responses has meant that few
ground genetic effects (Gaffney et al., 1990; Pecan common patterns have been recognised, with little
Slattery et al., 1993). But we have yet to establish the understanding of the genetic or metabolic basis to
biochemical basis by which heterozygosity varies with that variability.
maintenance metabolism. It is possible that the stud- Oxygen consumption has normally been deter-
ied alleles are acting as markers of heterozygosity at mined as the most convenient and relevant measure
linked loci affecting metabolism, in the so-called of metabolic responses to temperature. As a result of
“associated overdominance hypothesis” (Zouros those studies, activity level and nutritional state have
et al., 1988). Alternatively, phenotypic effects of been recognised as the two principle influences among
heterozygosity may be influenced by the metabolic factors affecting the temperature-dependence of
significances of each studied allele product (Watt, metabolism (see reviews by Fry, 1957; Prosser and
1985). Support for this latter view has been docu- Brown, 1961; Newell and Northcroft, 1967; Bayne,
mented by Koehn et al. (1988), who concluded that 1973; Newell and Bayne, 1973; Newell, 1979). To
the effects of heterozygosity on growth are locus- summarize, oxygen consumption is reduced in
specific, independent of heterozygosity per se, and response to starvation and physical inactivity. And
related to the function of the enzyme either in protein with a very few exceptions, fed and/or active animals
catabolism or glycolysis. These findings are consistent show high (“routine”) rates of oxygen consumption
with data indicating that energetic consequences as- that may vary logarithmically according to
sociated with differences in protein turnover underly Arrhenius’s law in immediate response to tempera-
relations between heterozygosity and performance ture change over the normal environmental range.
(Hawkins, 1991) and that rates of glycolytic flux are Alternatively, starved inactive animals show a low
lower in pigs selected for high growth rate (Campion (“standard”) rate of oxygen consumption that reflects
et al., 1983). energy expenditure for maintenance metabolism
alone, and which is relatively insensitive to tempera-
ture change over much of the normal environmental
temperature range. The relative insensitivity of main-
METABOLIC INFLUENCES UPON RESPONSES TO
ENVIRONMENTAL TEMPERATURE CHANGE tenance metabolism is recognised as an essential
prerequisite for survival of ectotherms within any
Ectotherms may modulate their biochemistry and environment subject to rapid temperature change
physiology to compensate for any reduction in per- (Newell and Northcroft, 1967).
formance stemming from the acute (“immediate”) These generalizations have been based mainly
effects of environmental temperature change (see upon comparisons that have dismissed variation
reviews by Kinne, 1970; Prosser, 1973; Vernberg and between individuals as negligible and/or irrelevant.
Vernberg, 1972; Weiser, 1973; Somero and Recent work at Plymouth Marine Laboratory has
Hochacka, 1976; Newell, 1979; Newell and Branch, focused upon that variation between individuals,
1980; and papers by Thompson and Newell, 1985; comparing aspects of protein metabolism and
 Temperature change on ectotherm metabolism 25

physiology to further understand both the genetic 41 \’

regulation and metabolic basis of different responses

to environmental temperature.
In one of two experiments, mussels (Mytilus
edulis L.) of similar size (6.0-7.0 cm) were acclimated
to laboratory seawater at 12.0 f l.O”C, whilst fed the
alga Phaeodactylum tricomutum at a ration that was
sufficient to sustain low rates of growth (Hawkins,
Smith, Arrive and Bayne: unpublished data). Oxygen
consumption was measured in each of 20 individuals
both before and immediately after transfer from 12 to
EFFICIENCY OF PROTEIN
5°C as well as at 2-3 day intervals over the following
DEPOSITION WHEN ACCLIMATED
30 days whilst animals continued to be fed at AT 10°C
5.0 * l.O’C. Linear regressions of rates of oxygen Fig. 2. Q,, values for oxygen consumption immediately
consumption over time following the temperature upon transfer of individual Myti/us edulis from 10 to 20°C
change enabled estimation of the time required for in relation to efficiencies of protein deposition [(net protein
balance/total protein synthesis) x 1001 among those same
complete acclimation of respiration, as well as of the
individuals when previously acclimated at 10°C. Data are
total cumulative (integrated) reduction in oxygen from Hawkins et al. (1987), standardised per g total dry
consumption throughout that period of acclimation. tissue wt. Lines (f95% CL) are fitted by least-squares
Of interest here, the Q,, for oxygen consumption in regression.
each individual varied in significant positive relation
with oxygen consumption when fully acclimated
before the reduction from 12 to 5-C (Fig. la). Fur- incurred the largest cumulative reduction in oxygen
ther, there was no clear relation between Q,, and consumption throughout cold acclimation (Fig. lb).
subsequent rate of respiratory acclimation, so that Our other experiment compared relative responses
mussels with the highest initial oxygen consumption of individuals to increased rather than to reduced
temperature (Hawkins et al., 1987). Mytilus edulis of
similar size (7.0-7.5 cm) were acclimated to labord-
tory seawater at 10.0 + l.O”C, whilst fed the alga
Phaeodactylum tricomutum at a ration that was
sufficient to maintain low rates of growth as in the
experiment described above. Each physiological
component of budgets for both energy and pro-
tein-nitrogen, as well as whole-body protein syn-
thesis, were then measured in 15 individuals both
/ I
5 10 15 20 before and within 48 h of transfer from 10 to 20°C.
z
Oxygen consumption was also monitored at l-2 day
(b)
r* = 0.523 intervals over the following 12 days whilst animals
” = 20
continued to be fed at 20.0 + 1.O”C. Finally, the same
mussels were subjected to a further abrupt increase in
temperature from 20.0 to 28.5 + 1.5”C, and time to
death monitored for each individual. Results
confirmed previous findings (refer above) that faster
growth of individuals acclimated at 10°C derived
d 5 10 15 20 primarily from reduced energy requirements associ-
OXYGEN CONSUMPTION WHEN ated with lower intensities of protein turnover. But
ACCL equally significant was that Q,, values for the immedi-
Fig. 1. (a) Q,,, values describing the immediate response in ate increase in oxygen consumption following trans-
oxygen consumption upon transfer of individual Myti[us fer from 10 to 20°C were proportionally greater
edulis from 12 to 5°C and (b) the total cumulative reduction among individuals with lower efficiencies of protein
in oxygen consumption during respiratory acclimation at deposition [(net protein balance/total protein syn-
SC, both in relation to initial acclimated oxygen consump-
thesis) x 1001 and thus higher intensities of protein
tion at 12’C. All data are standardised per g total dry tissue
wt, and lines (+95% CL) fitted by least-squares linear
metabolism when previously acclimated at 10°C
regression (Hawkins, Smith, Arrive and Bayne; unpublished (Fig. 2). Similarly, coincident increments of whole-
data). body protein synthesis varied in positive relation-
26 ANTHONYJ. S. HAWKINS
ship with oxygen consumption when previously
acclimated at 10°C (Fig. 3).
These findings comparing the temperature re-
sponses of individual mussels show intriguing simi-
larity to the pattern of sensitivities that has been
recognised upon comparing the metabolic responses
of many species according to differing levels of nutri-
tion and activity (refer above). Most significantly,
higher intensities of metabolism when acclimated to
a constant temperature are consistently associated
with greater metabolic sensitivities to temperature
change (Figs la, 2 and 3).
Newell and colleagues have convincingly explained
this general pattern of response in terms of intra-
cellular substrate concentration and membrane per-
meability (Newell and Bayne, 1973; Newell, 1979;
Newell and Branch, 1980). Temperature-dependent
reaction rates occur when high substrate levels exceed
the &,-value for a particular enzyme (Hochachka and
Somero, 1973; Somero and Hochachka, 1976). Con-
versely, if substrate levels are below that &,-value,
then reaction rate is controlled by enzyme-substrate
affinity, and reduced enzyme-substrate affinity as
temperature increases may maintain reaction rate
essentially independent of environmental tempera-
ture (Somero, 1969; Hochachka and Somero, 1973).
80
r2 = 0.38
60 n = 12
P = 0.033
40
20
/ with increased protein metabolism accounted for
5 10
r’ = 0.27 (b)
n = 12
P = 0.082
. consumption varied in significant positive relation
A .. ??
5 10
OXYGEN CONSUMPTION WHEN
ACCLIMATED AT 10°C
(pmoles 0, he’g-’ tdw)
Fig. 3. (a) Absolute changes and (b) Qlo values for whole-
body protein synthesis immediately upon transfer of individ-
ual Myrilus edulis from 10 to 20°C in relation to oxygen
consumption among those same individuals when pre-
viously acclimated at 10°C. Data are from Hawkins et al.
(1987), standardised per g total dry tissue wt. The reduction
from n = 15 in Fig. 2 to n = 12 here reflects samples lost
during the measurement of protein synthesis. Lines (k 95%
CL) are fitted by least-squares regression.
0 20 40 60
ABSOLUTE CHANGE IN WHOLE-BODY
PROTEIN SYNTHESIS UPON
TRANSFER FROM 10 TO 20°C
(mg d-’ g-’ tdw)
Fig. 4. Absolute changes in oxygen consumption’immedi-
ately upon transfer of individual Myti/us edulis from 10 to
20°C in relation to the coincident absolute changes in
whole-body protein synthesis. All data are standard&d per
g total dry tissue wt, and lines (*95% CL) fitted by
least-squares linear regression (redrawn from Hawkins
et al., 1987).
The same interrelations may explain the different
responses that we have observed between individual
mussels. First, a strong positive relation suggests that
the majority (62%) of inter-individual differences
between absolute changes in oxygen consumption
initially accompanying transfer from 10 to 20°C were
explained by corresponding absolute changes in pro-
tein synthesis (Fig. 4). So requirements associated
most of the higher costs measured as oxygen con-
sumption at 20°C. Secondly, whilst increases in
15 whole-body protein synthesis upon transfer to 20°C
correlated positively with oxygen consumption when
??
initially acclimated at 10°C (Fig. 3) Q,, values de-
.
scribing coincident proportional increases in oxygen
with the proportions of whole-body protein synthesis
that were effecting turnover rather than net depo-
sition (Fig. 2). One of the main functions of protein
turnover is to mobilize amino acids for selective
15
catabolism or redistribution (Hawkins, 1991). Our
collective findings therefore suggest that increased
energy expenditure at 20°C was mostly incurred
through energy demands associated with protein
synthesis, influenced by the relative rate with which
intracellular amino acids are being mobilized by
protein turnover. Other factors are known to involve
mechanisms for transporting amino acids, membrane
permeability, phospholipid metabolism, heart and
ventilation rates, and swimming speeds (Saenger and
Holmes, 1992).
 Temperature change on ectotherm metabolism
Figure 4 also reflects different mechanisms effecting
a range of individual responses. Reductions in pro-
tein synthesis may have resulted from temporary
overshoots in compensatory processes (Precht et al.,
1973) that include conformational changes and
modulation of enzyme-substrate and/or enzyme-
regulator interactions (Hoffmann, 1983). Alterna-
tively, even in mussels that showed the greatest
metabolic increases, complete acclimation back down
to the rates initially measured at 10°C was achieved
within 15 days (Hawkins et al., 1987). Figure 5
illustrates a strong positive relation between those
rates of respiratory acclimation, measured as the
daily change in pmol O2 consumed day-‘, and initial
rates of whole-body protein synthesis at 20°C.
Mussels were each suffering net losses of pro-
tein-nitrogen, so that all protein synthesis was effect-
ing turnover. This therefore confirms the role of
protein turnover in metabolic adaptation, enabling
more rapid adjustment that may either be quantitat-
ive, resulting in altered specific activity, or qualitative,
associated with changes in the relative abundance of
thermoisozymes (Somero and Hochachka, 1968;
Hazel and Presser, 1974; Gilles, 1975; Thebault and
Bernicard, 198 1; Hoffmann, 1983).
Although daily rates of respiratory acclimation
following transfer from 10 to 20°C were greater in
mussels with higher initial metabolic rates at 2O”C,
the total cumulative increase in oxygen consumption
throughout up to 1S-day respiratory acclimation was
much larger among individuals with the highest
r2 = 0.81
” = 12
P c 0.001
0 20 40 60
INITIAL WHOLE-BODY PROTEIN SYNTHESIS
FOLLOWING TRANSFER FROM 10 TO 20°C
(mg d-’ g-’ tdw)
Fig. 5. Daily rates of respiratory acclimation following
transfer of individual Myfilus e&is from 10 to 20°C in
relation to initial rates of whole-body protein synthesis
immediately following that same transfer. Data are from
Hawkins et al. (1987), standardised per g total dry tissue wt.
Lines (&95% CL) are fitted by least-squares regression.
21
/ I I
I2 = 0.84 /
n = 11
P < 0.001
.
. .
.
1
??
/ .
/
/ I I
0 1 2 3 4
Q,, FOR OXYGEN CONSUMPTION
UPON TRANSFER FROM 10 TO 20°C
Fig. 6. The total cumulative increase in oxygen consumption
during respiratory acclimation of individual Mytilus edulis
following transfer from 10 to 20°C in relation to Q,, values
for the immediate increases in oxygen consumption upon
that same transfer. These are previously unpublished data of
Hawkins et al. (1987), standardised per g total dry tissue wt.
Lines (k 95% CL) are fitted by least-squares regression.
associated Q,, values (Fig. 6). As described above, the
same was true for mussels subjected to a temperature
decrease from 12 to 5°C (Fig. lb). Therefore, both
experiments confirmed that the greatest long-term
metabolic costs were incurred by individuals showing
larger initial responses to temperature within the
normal environmental range.
Under more stressful conditions, slower-growing
individuals with faster intensities of protein turnover
when acclimated at 10°C were the first to die soon
after exposure to 28.5”C (Hawkins et al., 1987).
Presumably, greater metabolic sensitivity in those
individuals acted to amplify demands further beyond
a critical threshold, resulting in reduced viability at
this extreme temperature.
THE METABOLIC AND PHYSIOLOGICAL BASIS OF
HETEROZYGOTEADVANTAGEAS A FRAMEWORKFOR
UNDERSTANDINGEVOLUTIONARYRESPONSES TO
ENVIRONMENTALTEMPERATURECHANGE
Interrelations between protein turnover, energy
metabolism and production in the second study of
individual mussels described above (Figs 2-6)
80 (Hawkins et al., 1987) were similar to those under-
lying increased production with higher average mul-
tiple-locus heterozygosity (Hawkins et al., 1986;
Hawkins, 1991). We therefore interpreted these
findings as being genotype-dependent, concluding
that higher intensities of maintenance metabolism
in relatively homozygous individuals are associated
with amplified metabolic responses to temperature
change (Hawkins et al., 1987). A genetic influence
28 ANTHONYJ. S. HAWKINS

upon those responses should be expected, given the temperature change has been obtained under
evident role of protein metabolism in metabolic controlled laboratory conditions. Multi-locus het-
responses to temperature. However, energy expen- erozygotes generally show a growth advantage under
diture and protein turnover also vary in response to experimental conditions of sub-lethal stress at elev-
a wide variety of endogenous and environmental ated temperatures (Rodhouse and Gaffney, 1984;
influences (Hawkins, 1991; Houlihan, 1991). There- Scott and Koehn, 1990). In addition, parallel re-
fore, whether comparing genetic differences between sponses in gene frequency to the same conditions but
individuals, or comparing differences stemming among different species help to confirm selection for
from levels of nutrition and/or activity, it is likely specific genotypes. Among ectotherms generally,
that different responses to temperature change stem differential tolerance of temperature has consistently
from the same metabolic interrelations. Findings been linked to genotypes for esterase in a freshwater
considered here suggest that metabolic sensitivity to fish (Koehn et al., 1971) and a marine gastropod
temperature varies in positive exponential (Q,, values (Ushakov et al., 1989). The same has been shown for
indicate factorial increments) relation with total phosphoglucose isomerase (PGI) in a sea anemone
energy metabolism, that most of the resulting (Hoffmann, 1983) and a butterfly (Watt et al., 1983).
change in metabolic expenditure is associated with Whilst any functional implications of different
protein synthesis, and that the scale of that change isozymes have yet to be resolved for esterase, PGI
is influenced by the relative rate with which intra- occupies a crucial branch region between glycogen
cellular amino acids are being mobilized by protein storage, the pentose shunt and glycolysis itself. The
turnover. And perhaps most important, our data findings of Watt and co-workers are particularly
confirm that greater metabolic sensitivity results in convincing, showing how the interaction of PGI
higher long-term energy costs and an associated genotypes with environmental temperature is central
reduction in the ability to survive extreme thermal to selection at this locus (Watt, 1985).
stress. It has been proposed that heterozygote superiority
This section will emphasize the apparent ecological in heterogeneous environments may either stem from
and evolutionary relevance of these interrelations. superiority over their multimeric enzymes (Clark,
Much of the genetic polymorphism in animals is 1979) or from greater resistance to environmental
non-random, displaying ecogeographical patterns perturbations (Lerner, 1954). The latter is consistent
(Levinton and Lassen, 1978; Koehn, 1983; Singh and with higher developmental stability (King, 1985; Mit-
Green, 1986). Of these relations, many are between ton and Koehn, 1985) and an enhanced ability to
protein diversity and ecological heterogeneity in resist experimental stressors (Koehn and Shumway,
space and time (Nevo et al., 1984; Nevo, 1988a, b), 1982; Rodhouse and Gaffney, 1984; Mork and Sund-
and include changing heterozygosity along macro- nes, 1985; Blot and Thiriot-Quievreux, 1989; Nevo
geographic clines of temperature and humidity (Nevo et al., 1986; Scott and Koehn, 1990). But most
and Bar, 1976). Within the marine environment, important here, is that the metabolic and physio-
animal multi-locus heterozygosity decreases with logical interrelations described above provide a
depth of habitat in the water column or sediment mechanistic explanation of that greater resistance.
(Levinton, 1973) and increases with intertidal ex- Koehn and Bayne (1989) have described how high
posure (Koehn et al., 1973; Lavie and Nevo, 1986). maintenance energy expenditure means that net pro-
Similarly, heat resistance is known to decrease with duction is maintained across a narrower environmen-
depth of habitat in the water column (Schlieper et al., tal range, with the result that tissue wasting occurs
1967) or sediment (Wilson and Elkaim, 1991) and to under conditions that deviate less from those
increase with height on the shore (Wilson and enabling maximal production, and physiological vari-
Elkaim, 1991). On a wider scale, the genetic variabil- ability is greater. Such a response is illustrated for the
ity of fish appears higher in tropical and temperate- mussel Mytilus edulis in Fig. 7, where the effects of
pelagic species than in temperate-demersal species temperature increase are compared for two individ-
(Saenger and Holmes, 1992). uals with different rates of respiration when initially
Ecogeographical associations with heterozygosity acclimated at 15°C assuming the same temperature
have often been suggested as evidence for natural dependency of metabolism (Q,, = 2.0), with increases
selection. However, similar patterns may also result in oxygen consumption that are designated as Rl and
from functionally or structurally associated genes, R2. The individual with higher initial energy expendi-
or through parameters of population structure and ture will maintain production over a smaller range of
history (Lewontin, 1974; Lavie and Nevo, 1986). temperature increase (range 1 vs range 2 in Fig. 7).
Unambiguous evidence for the influence of enzyme However, in making the above point, Koehn and
polymorphisms upon ecological consequences of Bayne (1989) assumed that Qlo values for oxygen
 Temperature change on ectotherm metabolism
I decrease towards similar minimal levels (Fig. 7).
3
Gl
$ IQ,,
B (Q,. = 2.0)
5
:_~y...A.- :
t-3-+: : ated changes in energy absorption. And it is not yet
/ -4-t II 1 I
0 5 10 15 20 25 30
ENVIRONMENTAL TEMPERATURE
(0a
Fig. 7. Curves representing the immediate effects of tem-
perature increase on rates of both energy absorption (Al
and A2) and energy expenditure through respiration (Rl,
R2 and R3) in the mussel Myrilus edulis previously accli-
mated at lS”C, where Al (-) and Rl (B--m) are based on
responses described by Bayne (1973), imposing a Q,,, value
for respiration of 2.0. R2 (0-O) illustrates the effect of a
20% increase in energy expenditure, as observed in slower-
growing and relatively homozygous individuals (refer text),
but with a similar Q,, of 2.0. R3 (0-a) shows the effect
of the same 20% increase in energy expenditure, but with a
higher Q,, of 3.5 as is emphasized in this paper (refer text).
A2 (. . .) illustrates the effect of a 10% reduction in energy
absorption, as has been reported for slower-growing and
relatively homozygous individuals (refer text).
consumption and rates of energy absorption were
both independent of weight-specific differences in
acclimated maintenance expenditure. Given the com-
mon pattern of sensitivities recognized in the present
paper, then increasingly amplified metabolic re-
sponses to temperature, with a maximal Q,, of at least
3.5 (Figs la and 2b), represent a further disadvantage
associated with the higher rates of acclimated energy
expenditure in less heterozygous individuals. This
means that the actual increase in respiration with
temperature will be even greater (R3), and the tem-
perature range for net production further reduced
(range 2 vs range 3 in Fig. 7). Significantly faster rates
of tissue wasting would also compromise survival at
high temperatures which, although within the normal
environmental range, may ultimately prove lethal.
It is notable that the consequences for relative
performance of increasingly amplified metabolic
responses with higher initial acclimated rates of
metabolism are not as great following a reduction in
temperature. Each individual remains in a condition
of net production, whilst the higher Q,, value in the
individual with higher initial rate of acclimated
metabolism means that energy expenditure quickly
29
converges with that of the individual with lower
initial rate of acclimated metabolism, as both
Nevertheless, there may be significant changes in
relative production, depending both upon the degree
of temperature decrease and relative Q,, values for
energy expenditure. For a relatively homozygous
= 2.0)
individual exposed to falling temperature, it is con-
ceivable that despite a faster initial intensity of main-
tenance metabolism, the higher metabolic sensitivity
may result in lower energy expenditure and greater
net production. But this will depend upon any associ-
known whether the form of the relationship between
35
rate of absorption and temperature may change with
maintenance expenditure or heterozygosity.
We do, however, know that rates of feeding and
energy absorption may be greater in faster-growing
and/or heterozygous individuals with reduced main-
tenance requirements (Garton, 1984; Garton et al.,
1984; Hawkins et al., 1986, 1989; Halley and Foltz,
1987). Assuming that the form of the relationship
between energy absorption rate and temperature
remains unchanged, then this difference in absorption
may not represent a significant influence upon the
range over which net production can be maintained
during the response to falling temperature (Fig. 7).
Alternatively, with rising temperature, slower absorp-
tion by individuals with greater initial rates of accli-
mated energy expenditure and higher QIO values
further reduces the range of temperature increase
over which net production can be maintained, and
acts to accentuate the relative advantage of
heterozygotes (range 3 vs range 4 in Fig. 7).
These interrelations help to explain geographical
associations whereby both animal multi-locus het-
erozygosity and heat resistance decrease with depth
of habitat in the water column or sediment, and
increase with intertidal exposure (refer above). A
further possible disadvantage of high maintenance
energy expenditure during the immediate response to
changing environmental conditions has been
suggested by Mitton et al. (1986) who reported that
higher maintenance requirements in less heterozygous
salamanders allow smaller absolute increments be-
tween standard and active levels of metabolism, thus
representing a reduced potential “scope for activity”.
This may be of general significance. However, similar
findings have yet to be reported in any other animal,
and little is yet known of how maximal active metab-
olism may vary between individuals among organ-
isms generally. More certain, is that the consequence
whereby lower maintenance energy expenditure re-
sults in net production over a wider environmental
range is potentially significant in the response to
30 ANTHONY J. S. HAWKINS
stressors generally. But among ectotherms, tempera-
ture is one of the most important environmental
influences, acting directly upon metabolism, and dis-
playing great variability in space and time. Therefore,
the relations recognised here whereby metabolic re-
sponses to temperature increase exponentially with
prior rate of acclimated energy expenditure, and
energy expenditure decreases with multi-locus het-
erozygosity, must be of particular significance for
comparative performance and evolution within
heterogeneous environments.
CONCLUSIONS
Interrelations described above whereby mainten-
ante metabolism links genotype with physiological
performance represent a theoretical framework with
which to help understand the effects of temperature
change on ectotherm metabolism and evolution. The
intensity of maintenance metabolism is genetically
determined, decreasing with both multi-locus
heterozygosity and growth rate. With fluctuating
environmental temperature, greater energy flux and
faster mobilization of amino acids may result in
reduced potential “scope for activity”, a smaller
range of temperatures over which net production may
be maintained, and amplified metabolic responses to
temperature change. Consequences include a relative
inability to capitalize upon favourable conditions,
greater physiological variability with fluctuating tem-
peratures, higher energy costs incurred during the
response to temperature change, and reduced
viability upon exposure to extreme temperatures.
These consequences comprise the basis upon which
natural selection can act, and underly the superiority
of multi-locus heterozygotes within heterogeneous
environments. Given associations with heterozygos-
ity, the same consequences may also underly the
enhanced growth and viability normally associated
with “hybrid vigour” or “heterosis” (e.g. Mitton and
Grant, 1984; Zouros and Foltz, 1987), as well as with
triploid animals induced by blocking meiosis I
(Hawkins et al., 1994). Potential implications are
therefore diverse, with relevance to strategies of selec-
tive breeding and genetic manipulation, and to under-
standing physiological evolution and ecogeographical
distributions. Results also emphasize the need to
consider maintenance processes within any detailed
attempt to understand the interrelations between
physiology and evolutionary processes.
Production is controlled by complex interplay
between endogenous influences that are inherent to
the organism, and environmental factors (Hawkins
and Bayne, 1992). For example, oxygen consumption
(Newell, 1979) and protein turnover (Fauconneau,
1985; Reff, 1985) are both higher per unit tissue
weight in younger animals, which may help explain
why younger animals generally display narrower
ranges of temperature tolerance (Saenger and
Holmes, 1992). Further, the phenotypic consequences
of heterozygosity are environmentally dependent,
becoming clearest under conditions of food limitation
or other stressors (Gaffney et al., 1990; Ushakov
et af., 1989; Pecan Slattery et al., 1993). It is also
likely that seasonal changes in metabolic sensitivity
to temperature change (e.g. Newell and Pye, 1970;
Worrall & Widdows, 1984) are influenced by associ-
ated changes in the relative intensities of protein
turnover (e.g. Hawkins, 1985). Future work should
thus assess how environmental factors such as food
availability interrelate with heterozygosity, protein
turnover and other endogenous influences to affect
the integrated physiological response to temperature.
Other comparisons are required both to confirm
the generality of relations identified here, and to
establish the relative effects of temperature change on
species from different environments. In particular,
there is a general positive relationship between habi-
tat temperature and standard metabolic rate among
marine ectotherms (Clark, 1991; Johnston et al.,
1991). Given findings presented above, this implies
that metabolic sensitivity to temperature change and
other stressors may be greater among tropical than in
polar species.
Acknowledgements-This work represents part of Individ-
ual Research Project 4 (“Ecological Energetics and Growth
of Marine Molluscs”) of the Plymouth Marine Laboratory,
a component of the U.K. Natural Environment Research
Council. I thank both Brian Bayne and John Widdows for
helpful comments upon this manuscript.
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