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The level of genetic diversity in free-living populations 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-order effects. 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, Fishers 1930 discussions of the environment and consequences
for adaptation, as presented in the The Genetical Theory of Natural Selection, play an initiating role.
1996 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
The Genetical Theory of Natural Selection published in 1930. This book had a long
gestation time, in excess of ten years. Sewall Wright, in reviewing the book for the
1
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.
00244066/96/080471 + 12 $18.00/0
471
472
P. A. PARSONS
Journal of Heredity, 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 menace,
and so preserve biological resources at orders of complexity ranging from genes to
ecosystems. Conservation biology rated little in the late 1920s when The Genetical
Theory 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 & Soule, 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 (OBrien, 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
offspring are 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,
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 (1991) 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 (1993) 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.
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, Eisenia 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 (1995) 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 gill 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 ehrenbergi,
in Israel and neighbouring locations. Average heterozygosity increases as
aridity stress and climatic unpredictability increase. In particular, in outlier
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, Ovis canadensis, at year 7 of life, which
is around the time of onset of breeding, 21% 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).
476
P. A. PARSONS
Nevo et al (1994) found that molecular genetic data in mole rats, S. ehrenbergi, 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
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 (1993) 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. melanogaster 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.
478
P. A. PARSONS
479
CONCLUDING COMMENTS
480
P. A. PARSONS
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. Allard 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 Adelaide J.H. Bennett has been of great assistance. I am grateful to all
these people, as well as to many others, including R.J. 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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