Biological Journal ofthe Linnean Society (1996), 58: 471-482
Conservation strategies: adaptation to stress
and the preservation of genetic diversity
P.A. PARSONS'
Faculty $Science and Technology, &$th
University, flathan, QU. 41 I I , Australia
Receiued 21 March 1995, acceptedfor pubhiation I8 S e p h b a 1995
The level of genetic diversity in free-livingpopulations is not normally restrictive for conservation, since
it tends to be enhanced in stressed outlier populations. At the physiological level, this enhancement is
supported by the favouring of heterozygotes, especially when energy demands needed to adapt to stress
are high. Therefore ecophysiological considerations are important for conservation strategies, whereby
survival depends upon the metabolic potential of organisms to counter the energy cost of stress in their
environments. While abiotic stresses are primary, biotic stresses, in particular competition, can be
consolidated into this model as second-ordereffects. Irrespective of levels of genetic diversity, any species
can be incorporated into this approach to conservation. I therefore regard the monitoring of stress
response traits to be primary to the preservation of genetic diversity in developing conservation
strategies. In arriving at this conclusion, Fisher's 1930 discussions of the environment and consequences
for adaptation, as presented in the 77u Genetical 7hcov offlatural Selection, play an initiating role.
01996 The Linnean Society of London
ADDITIONAL KEY WORDS: -heterozygote advantage energy cost - aridity - sexual selection metabolic potential - competition - fitness - biodiversity.
~
CONTENTS
Introduction . . . . . . . . . . . . .
Heterozygote advantage, stress and sexual selection
Electrophoretic loci and stress . . . . . . .
Stress, metabolic potential and conservation . . .
Biotic stress, especially competition . . . . . .
Concluding comments . . . . . . . . . .
Acknowledgements . . . . . . . . . . .
References . . . . . . . . . . . . . .
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INTRODUCTION
A key contribution to evolutionary biology in the long career of R.A. Fisher was
irhe Genetical irheo9 offlatural Sehction published in 1930. This book had a long
gestation time, in excess of ten years. Sewall Wright, in reviewing the book for the
'Present address: Department of Genetics and Human Variation, La Trobe University, Bundoora, Vic. 3083,
Australia. Correspondence, PO Box 906 Unley, SA 5061 Australia.
A version of this paper comprised the Third Sir Ronald Fisher Lecture, University of Adelaide, on 8th March,
1995.
002&4066/96/080471
+ 12 $18.00/0
47 1
01996 The Linnean Society of London
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P. A. PARSONS
Journal OfHerediQ, commented that it is “certain to take rank as one of the major
contributions to the theory of evolution”, and J.B.S. Haldane said it laid the
foundations of a new branch of science (Bennett, 1983). However, we should be
warned, since in the Preface Fisher comments that “No effort of mine could avail to
make the book easy reading”. This is certainly true, but equally no book has had a
greater influence in the development of modern evolutionary biology. In this paper,
I will show this remains true with respect to his discussion of the environment and
consequences for adaptation, in relation to conservation strategies.
In his book Fisher (1930) wrote: “If therefore an organism be really in any high
degree adapted to the place it fills in the environment, this adaptation will be
constantly menaced by any undirected agencies liable to cause changes to either
party in the adaptation”.
A major objective of conservation biology is to accommodate the above m a c e ,
and so preserve biological resources at orders of complexity ranging from genes to
ecosystems. Conservation biology rated little in the late 1920s when Zh Genetical
Zhory was being written, yet in the Dover Edition published in 1958, Fisher
considered that “owing to the rapid changes which man is making in his
environment”, there will be special difficulties in determining and interpreting
consequential fitness changes.
In consequence, I look here at the major emphases of conservation biology in the
light of the constantly changing environments to which free-living populations are
normally exposed.
In contrast, a major topic in conservation biology concerns genetic problems faced
by endangered populations. There have been extensive and continuing discussions
on the maintenance of genetic variation to preserve evolutionary potential (e.g.
Frankel & Soulk, 1981).Recent examples continue this trend (e.g. Prober & Brown,
1994; Raijmann et al., 1994). On the other hand, some species show extremely low
levels of genetic variation. A celebrated example is the endangered cheetah, Acinonyx
jubatus (O’Brien, 1994), although other species of terrestrial carnivores have even
lower levels and are almost completely homozygous (Merola, 1994).
However, many conservation strategies are devised to avoid high levels of
homozygosity, because of the well-documented phenomenon of inbreeding depression, whereby fitness falls as inbreeding increases. A useful monitor of fitness is
fluctuating morphological asymmetry, FA, since it can be used comparatively across
taxa. FA tends to increase under genetic stress such as inbreeding in a typically
outbred species, and under environmental stresses such as extreme temperatures
which tend to occur at some species borders (e.g. Zakharov, 1989; Parsons, 1990).
Yet, FA measures appear not to support the hypothesis that the cheetah is suffering
genetic stress from inbreeding (e.g. Kieser & Groeneveld, 1991). This implies that the
largely homozygous genetic constitution of the cheetah does not threaten the survival
of this species (Merola, 1994). Extrapolating more widely, levels of genetic variation
appear to be species-specific, so that the level characteristic of a particular species will
reflect a balance between selection favouring heterozygosity and any historical events
depleting genetic variation. Furthermore, the heterozygosities of parents and
offspringare necessarily correlated (Mitton et al., 1993)which would help to maintain
this balance.
The exceedingly low genetic variation in cheetahs directs attention to causes other
than the depletion of genetic variation as the underlying cause of extinction. For
instance, ecological factors such as predation, the abandonment of cubs by mothers,
CONSERVATION STRATEGIES, STRESS AND DIVERSITY
473
and abiotic perturbations may play a more direct role in their conservation than does
low genetic variation (Caro & Laurenson, 1994). This appears to imply that genetic
variation may be the ultimate limiting factor determining whether free-living
populations can adapt to changing environments, but that ecological factors
including responses to stress may provide more proximate explanations.
Emphasizing ecological factors, Hoffmann & Parsons (199 1) summarized a diffuse
literature on abiotic stress in living and fossil populations, and concluded that
responses to stress underlie much evolutionary change (and extinctions). Furthermore, inadequate nutrition is usual in free-living populations. Because of this,
White (1 993) argues that animals normally struggle to exist in a hostile environment.
Consequently, many organisms are born but few survive due to a combination of
physical stresses, principally of climatic origin, interacting with and causing
nutritional stress.
HETEROZYGOTE ADVANTAGE, STRESS AND SEXUAL SELECTION
Under laboratory environments that are demonstrably extreme, heterozygotes
derived from inbred strains tend to be favoured with respect to fitness measures
(Parsons, 1959; Barnett & Coleman, 1960). Such experimental data imply that
heterozygote advantage should be a feature of polymorphisms in natural populations
under extreme environments (Parsons, 1971). Conversely, inbreeding depression
should be more pronounced in a stressful environment. For instance, in Drosophila
melanogaster, inbreeding effects can be increased when organisms are exposed to
stressful temperatures and intense competition (Miller, 1994). Similarly, survival
following heat shock declined with increasing inbreeding in D.buzzati (Dahlgaard,
Krebs & Loeschcke, 1995). Furthermore, in the white-footed mouse, Peromyscus
leucopus noveboracemis, inbreeding had an especially detrimental effect on the
survivorship of mice when released into nature flimknez et al., 1994). In the wild,
inbreeding depression was expressed during the abiotic stress of severe winter
population bottlenecks in song sparrows, Melospiza melodia (Keller et al., 1994).
Turning to plants, Van Treuren et al. (1993) and Latta & Ritland (1994)
summarized examples indicating that inbreeding depression is influenced by the
environments in which plants are grown. They concluded that it was accentuated in
stressful environments, for example field-sown progeny under competition, and in
habitats to which plants are poorly adapted (see also Schmitt & Gamble, 1990;
Montalvo, 1994). These results are consistent with earlier laboratory results showing
an enhancement of inbreeding depression for growth rate under temperature
extremes in Arabidopsis thliana (Langridge, 1962) and <eu mays (McWilliam &
Grimng, 1965). Numerous additional studies of selection differentials in plant
populations discussed in a conservation context, provide support for the hypothesis
that viability selection favours heterozygotes, especially in small populations under
stress (Lesica & Allendorf, 1992). Further examples in plants and animals are
reviewed by Mitton (1993a).
In contrast, most laboratory experiments are carried out under relatively benign
circumstances, but in spite of these limitations, the level of heterozygosity of
individual organisms in populations tends to correlate with fitness measures, in
particular growth rate and developmental stability (Mitton & Grant, 1984). Enzyme
loci influencing metabolism and contributing to the amount of energy available for
474
P. A. PARSONS
development and growth, show the most significant positive associations with
heterozygosity (Mitton, 1993b). This is clearest under extreme conditions when the
energy demands from the environment would be highest. Since one direct effect of
stress is to increase the expenditure of metabolic energy (Odum, Finn & Franz,
1979), this suggests that heterozygotes may have the maximum genetic potential to
withstand the energy costs of any stress.
In the coot clam, Mulinia lateralis, there is a negative correlation between growth
rate and routine metabolic costs as the level of heterozygosity increases (Garton,
Koehn & Scott, 1984). In mussels, Mytilus edulis, heterozygotes have lower energy
requirements than homozygotes apparently because of greater efficiency in protein
synthesis, which releases energy for ingestion and absorption (Koehn & Bayne,
1989). These observations suggest that heterozygous individuals with a high level of
metabolic efficiency can maintain growth and reproduction under a wider range of
environmental conditions than individuals with a lower level of efficiency, because
they can continue to grow and reproduce as stress increases under resource
limitations. Examples of heterozygote advantage under energy stress include the
juvenile manure worm, Eismia foetida, under limited food and low moisture (Diehl,
1988),Mulinia lateralis, under temperature and salinity stress (Scott & Koehn, 1990),
and the oldfield mouse, P. polionotus, under low food quality (Teska, Smith & Novak,
1990). Similarly, based on a recent literature review covering many additional
examples, Hawkins (1 995) concluded that heterozygote advantage is “environmentally dependent becoming clearest under conditions of food limitation or other
stresses”.
Turning to stress from parasites, in feral rock doves, Columbia livia, lice reduced
feather and host body mass, and increased thermal conductance and metabolic rate
indicating an energy cost. This is exacerbated in a deteriorating abiotic environment
during winter (Booth, Clayton & Block, 1993). Similarly de Lope et al. (1993) found
that the ectoparasitic house martin bug, Oeciacius hirundinis, had larger negative effects
on the reproduction of its host, Delichon urbica, when nutritional conditions were poor
during the second compared with the first clutch in the season. In the lizard,
Sceloporus occidentalis, Schall& Sarni (1987) found that the time males spend in social
behaviours is reduced when infected with the malarial parasite, Plasmodium mexicanum,
and furthermore infected males perch more often in shade. Hence, the energy cost
from parasites reduces social behaviours and stressful microhabitats are avoided.
Under these stressful situations, selection should favour heterozygotes. For example,
a direct relationship between disease resistance and multilocus heterozygosity occurs
in the rainbow trout, Oncorhynchus mykiss, following exposure to bacterial gdl disease,
a potentially lethal epizootic in freshwater fishes (Ferguson & Drahushchak, 1990).
If natural populations experience recurrent stresses, heterozygous advantage
should therefore maintain genetic variation. There are a number of additional outlier
examples, where the energy cost from stress is demonstrably extreme.
(1) In a population of Soay Sheep on Hirta, St. Kilda, Scotland, population
crashes occur periodically, primarily following winter starvation. At these times
of nutritional stress, heterozygotes at the adenosine deaminase locus had the
lowest parasite burden, and so were least likely to die (Gulland et al., 1993).
(2)Aridity stress plays a major role in adaptation of the mole rat, Spalax ehrmbqi,
in Israel and neighbouring locations. Average heterozygosity increases as
aridity stress and climatic unpredictability increase. In particular, in outlier
CONSERVATION STRATEGIES, STRESS AND DIVERSITY
475
steppe and desert habitats, where climates are most unpredictable and variable
than elsewhere in the distribution of mole rats, population sizes are typically
< 100, but genetic diversity is much higher than on any expectation based
upon history, demography, gene flow or inbreeding (Nevo, Filipucci & Beiles,
1994).
(3) Viewed energetically, mating is an extremely expensive process. Since there is
a limit to the amount of energy that can be assimilated from food (Weiner,
1992), there is an upper limit to total behavioural activity. In parallel, oxygen
consumption increases to meet a high demand for ATP production, but the
maximum possible oxygen consumption is ultimately limiting (Bennett, 1991).
Consequently fitness, assessed by mating success, is often relatable to available
metabolic energy. Heterozygotes should be favoured at times of high energy
demands during mating, and this has been found in a number of species,
especially insects and fish (Thornhill & Gangestad, 1993).
On top of the cost involved in mating, some organisms develop and maintain
energetically costly sexual ornaments. Fisher (1930) argued that without any
check, a runaway process is expected and consequently the sexual ornament is
continuously exaggerated in dimensions. However, in some birds, sexual
ornamentation is restricted to the breeding season, indicating a substantial
energetic cost. This suggests a tradeoff, whereby the compounded energy cost
underlying the development and maintenance of ornaments of increasing size, is
countered by the cost of abiotic stress, especially when resources are limiting.
Since secondary sexual traits are extremely exaggerated versions of ordinary
traits, they are close to their limits of production and maintenance. Thus,
elaboration of secondary sexual traits can bring individuals to the energetic brink,
when stress-resistant genes should be favoured (Parsons, 1995a).
Under such extreme energetic circumstances, viability selection will favour
metabolic efficiency to enable survival. These are circumstances when the size of
ornaments should be associated with heterozygote advantage in natural
populations. For instance, in bighorn sheep, Ozk cunadensls, at year 7 of life, which
is around the time of onset of breeding, 2 1 '1'0 of variation in horn volume of rams
was attributable to an association with heterozygosity, but in young rams this
association was not apparent. Therefore, when energy demands from the
development and maintenance of horns and from the mating process itself are
high, heterozygote advantage is maximal (Fitzsimmons, Buskirk & Smith,
1995).
These examples suggest that under highly stressed situations in free-living
populations, genetic variation is likely to be enhanced. This is in accord with a
substantial body of laboratory data indicating increased mutation, recombination,
developmental variability, and phenotypic variability as stresses approach levels
where extinctions become a possibility (Parsons, 1987; Hoffmann & Parsons,
1991).
ELECTROPHORETIC LOCI AND STRESS
To what extent does genetic variation at specijic loci underlie adaptation to
changing conditions? There is much evidence that gene frequencies involving
476
P. A. PARSONS
electrophoretic variants can be correlated with temperature and other variables at
the geographic level. Some of these studies have demonstrated phenotypic
differences under extreme conditions reducible to the gene locus level (e.g. Piazza,
Menozzi & Cavalli-Sforza, 1981; Watt, 1985; Riddoch, 1993).
At the phosphoglucose isomerase, PGI, locus, the more anodal allozyme/isozyme
is favoured under stressful conditions including high temperature, high salinity,
anoxia and desiccation in data covering a wide range of animal and plant taxa. This
suggests at least one locus in natural populations of major importance in determining
resistance to stress (Riddoch, 1993). This particular situation is not surprising, since
in vitro biochemical studies of PGI allozymes suggest that this enzyme, which
catalyzes a metabolic reaction and regulates flux through glycolysis, is a direct target
of selection of such stresses (Watt, 1985).
Therefore, direct associations of stress with particular electrophoretic loci can
occur. In addition, the PGI locus provides the clue that it may be important to
consider the effect of stress on the energy balance of alternative genotypes, or more
broadly, at the level of the metabolic potential of organisms. Aridity, or desiccation
stress in the laboratory, appears to fulfil this role. In contrast, climatic stresses are
more typically expressed in terms of temperature shifts than aridity. However,
hydrological extremes of drought and deluge can have long and short term effects
that appear more direct and local as selective agents than temperature (Parsons,
1995b), so that aridity is the main stress under discussion in this paper.
STRESS, METABOLIC POTENTIAL AND CONSERVATION
Nevo et aZ(1994)found that molecular genetic data in mole rats, S.ehren6ergi, show
parallel patterns across habitats with data at the nuclear and mitochondrial DNA
levels as well as the organismic level. Ecological factors with an emphasis on aridity
stress underlie these patterns. The convergence of the organismic and molecular
levels to give parallel patterns, suggests that much of the total metabolic potential of
mole rats is assayed which is reflected at the organismic level, and is revealed by
desiccation stress as an environmental probe. This would be compatible with the
target of selection of desiccation stress at the level of energy carriers.
Furthermore, the inference that stress resistance is associated with metabolic
potential implies that in extreme environments, the preservation of organisms having
maximum metabolic potential to withstand the energy costs of stress should be at a
premium. Therefore, stress applied at the organismic level is likely to have
evolutionary consequences at the physiological and molecular levels. In this case, the
connection is indirect, since an extensive coverage of 36 electrophoretic loci and
nuclear and mitochondrial DNA, should involve sufficient of the complete metabolic
potential of organisms, that associations become apparent across levels of
organization from the molecular to the organismic.
This suggests that the survival of a species in its environment depends upon
possessing the metabolic potential to survive the energy costs of stress of that
environment. Under the stressful scenario, the habitats of organisms can be
expressed in terms of an interaction between stress intensity, magnitude of
environmental fluctuations, and energy available from resources as a first
approximation (Parsons, 1994a). The interaction of stress of various types causing
energy costs with energy gained from resources is a central tradeoff. Therefore, as
CONSERVATION STRATEGIES, STRESS AND DIVERSITY
477
conditions deviate from optimal, energy costs increase (Porter & Gates, 1969),so that
physical conditions can limit the occurrence of organisms to particular habitats. This
approach implies that the distribution and abundance of organisms should, in
principle, be relatable to energy balances (Hall, Stanford & Hauer, 1992), derived
from the costs of various abiotic (and biotic) stresses interacting with gains from
resources.
The difficulty in using the preservation of genetic variation as a primary strategy
in conservation follows from the point that natural selection acts primarily at the
organismic level. The approach outlined here is based upon the potential for
adaptation of organisms to the abiotic stresses to which they are normally exposed in
free-living conditions. This is a reductionist model (Parsons, 1992) based upon a
primary target of selection at the level of energy carriers. The extent to which the
model is reductionist to the gene level in the sense of Williams (1985) needs further
study, although the analysis of Riddoch (1 993) is suggestive.
Since environmental perturbations increase energy costs, adaptation to a
permanent increase in stress should involve selection for reduced energy costs often
via a lowered metabolic rate, with a range of concomitant effects for life-history
traits. This has been observed experimentally in D. melanogash by selecting for
desiccation resistance (Hoffmann & Parsons, 1989, 1991). Furthermore, reduced
fecundity and behavioural activity are direct indicators of a fall in fitness following
selection. The cost of this process therefore reduces the potential for further
adaptation, and a limit is likely at species borders when the cost can become totally
restrictive (Parsons, 1991). It is under these outlier conditions that heterozygotes may
be favoured, because of their greater efficiency of protein synthesis which releases
energy for ingestion and absorption. This effect should be maximal under the most
extreme environmental conditions when energy demands are highest. Therefore,
under the variably stressful environments of free-living populations, there should
normally be a premium on the conservation of genetic diversity. Hawkins (1995)
argues that under circumstances of heterogeneous and stressful environments, the
metabolic potential of multi-locus heterozygotes tends to ensure their superiority. In
this way adaptation to extreme environments can be enhanced (Koehn & Bayne,
1989).
In comparisons among species, levels of genetic variation range from predominantly homozygous at one limit, so that the favouring of heterozygotes under stress
cannot be universal. In contrast, irrespective of the level of variation, I argue that an
assessment of traits for stress resistance is an important primary strategy in
conservation biology for all species. This leads to direct predictions concerning the
survival of species during periods of environmental change. Unfortunately, this
phenotypic approach is more time consuming than studies of genetic diversity, but
there is a strong case for parallel experiments based on stress response traits of
ecological significance whenever this is feasible.
BIOTIC STRESS, ESPECIALLY COMPETITION
Fisher (1930) in Chapter VI of irhe Gmtical Zieoly wrote: “Any environmental
heterogeneity which requires special adaptations, which are either irreconcilable or
dimcult to reconcile, will exert upon the cohesive powers of the species a certain
stress.” He goes on to argue that speciation can occur under sufficiently strong
478
P.A. PARSONS
selection in terms of geographical distance. It is a remarkably modern statement,
since Wilson (1992) argues that “differences between species originally originate as
traits that adapt them to the environment”. He was emphasizing droughts, sea level
changes, and island environments.
However, in Chapter I1 Fisher (1930)comments: “Probably more important than
the changes in climate will be the evolutionary changes in associated organisms. As
each organism increases in fitness, so will its enemies and competitors increase in
fitness.”
This statement parallels Darwin’s (1 859) emphasis on biotic interactions, as being
dominant in underlying evolutionary change. In the one book, therefore, Fisher
discusses the environment in a way that represents the transition from Darwin to the
harsher world I am now assuming. Can these approaches be reconciled? An answer
comes from energy considerations. This means incorporating biotic stresses, in
particular competition, into the context of the energy costs of abiotic stresses.
Witter (1995) recorded that in the European starling, Sturnus vulguni, an
experimental increase in the level of competition at feeding sites decreases the
number of prey items which starlings carry back to the nest. A simple interpretation
is reduced fitness consequent upon the energy cost of competition. Indeed, there are
situations indicating that combinations of biotic and abiotic stress can push the
physiological state of organisms closer to lethality that can abiotic stress alone. An
example occurs in suspension-feeding venerid bivalves where a history of crowding
increased susceptibility to sedimentation stress (Peterson & Black, 1988). This means
that the energy cost of competition can decrease the stress resistance of organisms,
so reducing the range of physical conditions under which habitats could be
occupied.
However, the heritability of stress resistance can be very high, while that of
competitive ability is often barely distinguishablefrom zero (Mather & Cooke, 1962;
Parsons, 1973). This suggests that competitive ability can be viewed as a secondorder effect compared with stress as factors underlying evolutionary change.
This conclusion implies that the development of competitive relationships can only
be expected in abiotically rather benign habitats. In such restricted circumstances,
the energy cost of accommodating abiotic stress is relatively low, and a premium on
energy efficiency could select for diversification to exploit differing resources
(Parsons, 1994a), perhaps assisted by competition. Similarly, laboratory conditions
where temperature is controlled, represent a situation where energy costs from
environmental perturbations should be low compared with unstable field situations.
Under these conditions, intraspecific competition has been demonstrated in insects
such as Luciliu cuprinu and Drosophila (e.g. Nicholson, 1957; Mueller, 1988).
In any case, this approach shows that competition can be accommodated into
energy budgets (Parsons, 1996), as can abiotic stress, so that the varying approaches
to the environment, as presented by Darwin, Fisher and those mentioned in this
paper, can be reconciled. Competition becomes almost a special case in the longer
term, since severe abiotic perturbations occur unpredictably and sporadically on
time scales ranging from the seasonal to El Nifio events, and ultimately on the
geological scale. Under such stressful circumstances, complex communities appear
likely to be particularly vulnerable. In an increasingly stressed world, conservation
strategies appear to be most realistically developed assuming substantial stress, so
that biotic effects and interactions can normally be assumed to be relatively
unimportant.
CONSERVATION STRATEGIES, STRESS AND DIVERSITY
479
CONCLUDING COMMENTS
I suggest that the emphasis of conservation biology on preserving genetic
variability be reviewed, in terms of two central points: (1) the need to assume a
realistically stressful environment for free-living populations, and (2) the energy costs
for organisms to survive and reproduce in this environment.
These are direct effects with no obvious consequences for genetic diversity, except
that under very extreme circumstances an enhancement is likely. Fisher (1930) did
not discuss energy budgets, although in developing the Fundamental Theory of
Natural Selection, he noted that fitness could be considered in thermodynamic
terms. This is the approach taken in a number of recent publications. For instance,
Van Valen (1991) argues that energy provides a secure foundation for fitness, and
removes various anomalies from a purely genetical approach, and Brown, Marquet
& Taper (1993)define fitness in energy terms as the rate that resources, in excess of
those required for growth and maintenance of the individual, can be harvested from
the environment and used for reproduction. More generally, Torres (1991) gives a
definition of fitness based upon the distances of a given individual’s thermodynamic
parameters from their optimum values. In these terms, fitness will fall as the level of
stress increases, since stress has an energy cost.
Fisher (1930) in Chapter V of ‘The Genetical ?heoy wrote: “An evolutionary
consequence of some importance is that in general a smaller number of large species
must be increasing in number at the expense of a larger number of small species, the
continuous extinction of the latter setting a natural check to the excessive subdivision
of species which would ensue upon too fine and detailed specialization.” Here he was
apparently assuming an equilibrium, which is now under threat, and specialist
species, which tend to be stress-sensitive, face extinction. Generalist more stressresistant species would be favoured (Parsons, 1994a,b). Regarding a shift towards
ecosystem maturity as a process of increasing information, increased environmental
perturbations would reverse this trend and biodiversity would fall, forcing the
community into an earlier stage of ecological succession (Margalef, 1968).
Experimental perturbations using copper as a stress had this effect on a freshwater
plankton community (Havens, 1994). Furthermore, there is some recent evidence
suggestive of this trend in free-living populations. Since the 1950s and especially since
1980 in tropical forests of the Americas, trends in deforestation and atmospheric
change appear to be leading towards lowered precipitation, increased seasonality,
and more extreme weather (Hartshorn, 1992). Abiotic stress therefore is increasing,
and consequently the slowest growing shade-tolerant trees and tropical forest
organisms with life-cycles tied to those trees appear particularly vulnerable (Phillips
& Gentry, 1994). This may be the start of a trend from specialist diversification to
generalist uniformity. Under these circumstances competitive relationships would be
particularly vulnerable. It is a likely trend at any time when the energy cost from
stress increases, and could now be a general trend.
Therefore, the need to monitor the effect of stress in free-living populations as a
primary approach in conservation biology is reinforced. Recent examples illustrative
of this approach include the interactive effects of ambient ozone and climate, in
particular moisture stress, in reducing the growth of mature loblolly pine, Pinus taeda,
trees (McLaughlin & Downing, 1995) and changes in the breeding cycles of three
amphibian species native to Britain consequent upon recent steadily increasing
winter and spring temperatures, (Beebee, 1995).In accord with Hoffmann & Parsons
480
P. A. PARSONS
(1991) environmental extremes are significant in these examples, which appear
indicative of future emphases.
ACKNOWLEDGEMENTS
It is impossible to acknowledge all the influences over the years that have led to
this paper. However, A.R.G. Owen was a most important and helpful mentor in
Cambridge and subsequently. R.W. N a r d of the University of California at Davis
was central in helping me to appreciate that the environment of free-living
populations is much tougher than assumed by many evolutionary biologists. At the
University of AdelaideJ.H. Bennett has been of great assistance. I am grateful to all
these people, as well as to many others, including RJ. Berry, W.F. Bodmer and
A.W.F. Edwards, but most of all to R.A. Fisher. Finally,J.B. Mitton was most helpful
in improving this paper.
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