Behavioral Variability and Limits to Evolutionary Adaptation under Stress

ADVANCES IN THE STUDY OF BEHAVIOK. VOL. 27

Behavioral Variability and Limits to Evolutionary Adaptation under Stress P. A. PARSONS SCHOOL OF GENETICS A N D HUMAN VARIATION LA TROBE UNIVERSITY

BUNDOORA, VICTORIA 3083 AUSTRALIA

I. INTRODUCTION A. STRESSA N D ENERGY BALANCES

Interactions between organisms and environment are central for understanding evolution. For some evolutionary biologists, the occurrence of environmental perturbations of an unpredictable nature emphasizes physical factors as the major determinants of the distribution and abundance of organisms. Even so, the effects of abiotic factors can be modulated by interactions with biotic factors (Dunson and Travis, 1991). However, the abiotic environment should be tracked more predictably than the biotic as the time scale lengthens. From a diffuse literature Hoffmann and Parsons (1991) concluded that abiotic stresses mainly of climatic origin are important in many evolutionary and ecological processes. Furthermore, inadequate nutrition is usual in free-living populations, so that animals normally struggle to exist in hostile environments. White (1993) amassed much evidence, especially in herbivores, indicating that the abundance of organisms is often determined by a shortage of protein, especially for the young. For instance, pollen digestion is important for early breeding of Darwin’s finches of the Galapagos Islands (Grant, 1996). Consequently, many organisms are born but few are expected to survive due to a combination of climatic stress interacting with and causing nutritional stress. Validity of this environmental model is suggested by the rarity of creatures that commonly die of old age in free-living populations. In any case, a reference point is provided as a boundary for comparisons with more benign environments, especially certain human populations of recent times. 155

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The assumption of substantial stress contrasts with approaches to the environment by many evolutionary biologists, whose ideas appear to be influenced by the apparent existence of adequate nutrition in many human populations today. But these populations may represent a benign environmental outlier when considered in a historical context, both past and future. One direct effect of stress is an increase in the expenditure of metabolic energy, implying a cost (Odum et al., 1979). As exposure to stress is the norm, there is a need for some energy to exist in any habitat. The habitats of organisms can then be expressed by an interaction between stress intensity, magnitude of environmental fluctuations, and energy from resources as a first approximation. The interaction of stress of various types causing energy costs and energy gains (provided from resources) is central in relating the distribution and abundance of organisms to energy balances (Hall et al., 1992). As energy costs increase as conditions deviate from optimal (Porter and Gates, 1969), physical conditions can limit the occurrence of organisms in particular habitats. Biotic variables, such as competition, can be incorporated into this model via an increase in energy costs, but these effects are usually second-order compared with abiotic stresses (Parsons, 1996a,b). Stress reduces the fitness of organisms by deflecting energy from processes such as maintenance and survival, reproduction, growth, and genetic adaptation (De Kruipf, 1991). Fitness therefore is inversely related to the stress level as a first approximation. Furthermore, the impact of environmental perturbations can be expressed as a stress gradient (Odum et af., 1979), on which the potential for genetic adaptation falls as stress increases to an extreme where survival is threatened. The net energy balance of a species should be relatively high in central regions of its distribution. However, the margins of distributions of at least some animal species are limited by physiological constraints. Genes allowing further adaptation may not arise or, if they do, the animals carrying them may not survive (Parsons, 1991; Hoffmann and Blows, 1994). Physiological constraints can therefore determine the location of species borders, for example, in many North American bird species and in some small mammals (Bozinovic and Rosenmann, 1989; Root, 1993). In any case, organisms living at the very extremes of a species range are rarely the healthiest and most vigorous members of that species. B. HABITATS PREFERRED Habitats in which minimum energy is expended should be preferentially occupied. Intermediate temperatures between limiting extremes should therefore be preferred in an environment where temperature gradients exist. In these regions, maximum energy should be available for behavior,

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growth, and reproduction (Huey, 1991), and resistance to stress should be higher than elsewhere (Klieber, 1961; Arking et al., 1988; Zotin, 1990). Of course, these are the circumstances in which high population sizes may lead to maximum competition, but in all but the most abiotically stable of habitats such abiotic effects should be transient. Insects living in habitats with steep abiotic gradients can be useful for habitat preference studies. For example, in temperate zone rain forests, adults of an Australian Drosophila species, D . inornata, tend to rest on the fronds of tree ferns in the 15-20" range, with a mean of 17.7 ?I 2.0"C, following behavioral responses to the microenvironment. Consequently, flies attempt to select microhabitats as close as possible to optimal for temperature/humidity conditions, where the energy cost from the physical environment would be minimized (Parsons, 1993a). Similarly, Jones et al. (1987) found behavioral flexibility for thermal niche preference in D . melanoguster, whereby the effects of temperature extremes were ameliorated by habitat selection. Survival is thereby enhanced, since animals in early developmental stages are intolerant of energetically costly extreme conditions. In this context, the microenvironment (soil moisture and air temperature) experienced by a larva during wandering and pupation is important for pupal survivorship (Rodriguez et al., 1992). Furthermore, larvae from populations from dry habitats in Tunisia pupate closer to food than those from wet habitats (Rodriguez et al., 1991). Adult food-searching range is dependent on temperature. In D . melanogaster, the range searched is substantially smaller at the stressful temperature of 30°C than at 25°C (Good, 1993), presumably because of the high energetic cost of surviving at 30°C. Genetic shifts in preferred temperatures occurred in a gradient, when flies were reared at 25, 27, and 30°C for 15 generations. In addition, Yamamoto (1994) found temperature preferences in natural populations of D. immigruns and D . virilis to be heritable. Ye et al. (1994) found substantial genetic differences between strains of D. melanogaster from six local populations for adult starvation resistance, presumably as adaptations to cope with specific microhabitats. The six strains ranked for search behavior in parallel with starvation resistance, such that resistant strains searched over more extended ranges than did sensitive strains. In the two-spotted spider mite, Tetranychus urticae, there is genetic variation in aerial dispersal behavior, associated with resistances to the environmental stresses of desiccation and starvation (Li and Margolies, 1994). These few examples suggest that behavioral flexibility can reduce the energy costs of physical stresses. Furthermore, genetic changes can occur, enabling adaptation to varying habitats, assessed abiotically. Hence, ecobehavioral genetic adaptation can evolve under varying stress levels in free-

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living populations, which should ameliorate the direct effects of stress in an evolutionary sense. Turning now to the physiological state of insects, in D. melanogaster, starved flies are less discriminatory in responding to alternative resources in orchards than when unstressed (Hoffmann and Turelli, 1985). Resource selection is therefore most efficient when organisms do not simultaneously need to cope with extreme stress. However, nutritional stress appears to be the norm in natural populations of Drosophifa. For example, within a French population of D. melanogaster, high reproductive potential is not normally expressed under natural conditions, because of substantial and variable fluctuations in food availability (BoulCtreau-Merle et af., 1987). Furthermore, in a widespread montane North American butterfly, Speyeria mormonia, experiments with varying feeding regimes show that survival claims resources as a priority over reproduction (Boggs, 1994). In summary, more emphasis is needed on the study of habitat preferences under a range of realistic abiotic environmental conditions. In the remainder of this chapter, some background is provided for the consideration of limits to adaptation under predominantly rigorous conditions.

11. ENERGY LIMITSTO ADAPTATION

A. NONSEXUAL BEHAVIOR

Energetically expensive behaviors are common, for example, web construction in spiders, and insect and avian flight. However, the amount of energy that can be assimilated from food is finite (Weiner, 1992). Oxygen consumption can increase to meet a higher demand for ATP production, but the maximum possible oxygen consumption (Bennett, 1991) sets a limit to total behavioral activity. Consequently, any superimposed environmental stress would be deleterious by increasing respiration and hence stress sensitivity. For example, metabolic rate and whole-body thermal conductance increased in polar bears exposed to oil pollution, which increased mortality during the stress of a hard winter (Hurst et af., 1991). In D. melanogaster, high-metabolicrate “shaker” mutants show high levels of behavioral activity, and are very sensitive to environmental stresses, including high temperature, desiccation, and exposure to an unsaturated aldehyde acrolein (Barros et af., 1991; Parsons, 1992). In fasting rats, minimum heat production occurs in the thermoneutral zone and increases at higher and especially lower temperatures in association with reduced stress resistance (Klieber, 1961; Blaxter, 1989). In the social Damara mole rat, Cryptomys damarensis, body tempera-

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ture remains stable at ambient temperatures from 7 to 30°C, so that there is a substantial metabolic cost at extremes; at 7°C the metabolic rate is more than four times higher than in the thermoneutral zone (Lovegrove, 1986). In C. damarensis, which is from arid regions in southern Africa, the rate of metabolism is much lower than for comparable species from wetter regions. This is an energy-saving device enabling adaptation to aridity stress. In addition, cooperative searching and food sharing can reduce energy demands further (Lovegrove, 1986). Such adaptations can occur seasonally, or transiently during periods of bad weather. For instance, in the house martin, Delichon urbica, energy is saved during transient problems in finding food in the breeding season, by a complex of physiological and behavioral adaptations, including low basal metabolic rate, low thermal conductance, clustering behavior, high tolerance of the young to periods of low food supply, and the ability to become torpid (Prinzinger and Siedle, 1988). In subterranean blind mole rats of the Spalax ehrenbergi superspecies complex, aggression tendency and basal metabolic rate decrease geographically across Israel as the climatic stresses of temperature, and especially aridity, increase (Nevo, 1991). These responses would minimize water and energy expenditure, and are adaptations to counter extreme stress. Furthermore, in isolates from the environmentally harsh Sahara Desert of northern Egypt, mole rats were totally pacifist, presumably as an adaptation to an environment that is even more extreme than that in Israel (Nevo et al., 1992). Consequently, a behavioral-ecophysiological response has evolved based on selection against aggression. This response has enabled the spread of S. ehrenbergi into extremely arid environments (Ganem and Nevo, 1996). In summary, energetically costly behaviors occur frequently, and can determine limits of adaptation of organisms. Under these circumstances, any additional stress would be rapidly restrictive. Adaptations to high stress levels include reductions in resting metabolic rate, social behavior patterns that conserve energy, and pacifist behavior.

B. SEXUAL BEHAVIOR AND SEXUAL SELECTION The energy used in calling can exceed resting levels by up to 20 times in frogs (Ryan, 1988), suggesting that the mating process can be energetically expensive. In some frog species, mating success of males increases with increasing chorus tenure (Pough, 1989). As the time a male spends in the breeding chorus is important in determining mating success, fitness assessed in this way is likely to be related to available metabolic energy. In damsel flies, Calopteryx maculata, territorial contests favor males with the greatest energy reserves, measured by fat content (Marden and Waage, 1990). In great tits, Parus major, and male pied flycatchers, Ficedula hypoleuca, in

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breeding condition, resting metabolic rate is positively correlated with dominance rank (Roskaft et al., 1986). In the fish Betta splendens, winners and dominant individuals in a hierarchy consume more energy per unit time than losers and submissives (Haller and Wittenberger, 1988). In pupfish, Cyprinodon pecosensis, critical swimming speed is higher in territorial than in nonterritorial males, indicating a positive correlation of vigor with social status (Kodric-Brown and Nicoletto, 1993). In summary, these and other examples imply that fitness in mating is normally correlated with energy consumption. Similarly, daily energy expenditure increased significantly with increasing display rate and time spent in the lek in the male sage grouse, Centrocercus urophasianus (Vehrencamp et al., 1989). Daily energy expenditure for the most vigorously displaying males was two times higher than for a nondisplaying male, and four times higher than the basal metabolic rate. The increased levels of lek attendance and display levels appear fueled by increased quantity or quality of food, since the more actively displaying males can forage further from the lek. Furthermore, the abiotic environment is relevant, since metabolic expenditure increases as temperature falls; this would be ultimately restrictive. The inadequate resources available for free-living organisms should be used efficiently. Accordingly, resources are normally channeled to only some of those seeking to use them, so that a dominant few survive; the remainder in a population are vulnerable. This can be achieved by territorial and social behaviors, largely restricting resources to the dominant few, as demonstrated in passerine bird species by Moller (1991). Analogously, polygyny can replace monogamy in traditional human societies, when there are substantial fitness differences among men, following pathogen stress. The minority of resistant men are dominant in mating, because they are more skilled in promoting polygyny; these skills include hunting, winning disputes, and resource acquisition (Low, 1990). Considering stress from parasites, in the lizard, Sceloporus occidentalis, Schall and Sarni (1987) found that the time males spend in social behaviors was 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 behaviors, and stressful microhabitats are avoided. In feral rock doves, Columbia liviu, 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 et ul., 1993). Finally, in the colonially nesting cliff swallow, Hirundo pyrrhonutu, mark-recapture experiments over an 8-year period showed that the annual survivorship of birds

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parasitized with cimicid bugs, fleas, and chewing lice was .38, compared with .57 for fumigated, nonparasitized birds (Brown et al., 1995). Turning to reproduction, 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 red jungle fowl, Gallus gallus, chicks infected with parasites grew more slowly than uninfected controls (Zuk et al., 1990). Since this effect was most pronounced for secondary sexual traits, there is a channeling of resources into the normal growth of nonornamental traits under parasite stress. Generally, birds and fish with high parasite loads engage in less courtship display and obtain fewer mates than those with lower loads (Hamilton and Zuk, 1982; Kennedy et al., 1987; Clayton, 1990). Therefore, the energy cost of parasites in combination with abiotic stresses can preclude the full development of ornamental traits, and reduce mating and fitness generally. Furthermore, if there are energy restrictions from nutritional stress, an ornament can rapidly regress, as found for the nuptial crest of male newts of the genus Triturus (see Halliday, 1978). In addition, sexual ornamentation in some birds is restricted to the breeding season, indicating an excessive cost in less favorable abiotic environments. Sexual selection can be constrained by costs associated with mate choice, when interacting with unfavorable abiotic circumstances. The same should apply to biotic effects, although less obviously. Especially for predation, theoretical models (e.g., Pomiankowski, 1987) predict that female preference should decrease with increasing costs of mate choice. Accordingly, individual females should modify their choice behavior to minimize this risk. In terms of energy costs, this means that females should become less discriminatory when given a choice among potential mates at times when the predation risk is increased. For example, male pipefish, Syngnathus typhle, exposed to the cod, Gadus morhua, as a predator, copulated infrequently and indiscriminately, whereas control males copulated more often with large than with small females (Berglund, 1993); and predation from the cichlid fish, Crenicichla alta, reduced female preference in the guppy, Poecilia reticulata (Godin and Briggs, 1996). Even so, Magnhagen (1991) has cautioned that only in a very few cases has it been shown that individuals actively change their mating behavior according to predation risk. Additional studies would be useful. Overall, the stressful scenario in nature should reduce the tendency for traits involved in the sexual selection process to become progressively more extreme, thereby limiting the runaway process in which the sexual ornament is continuously exaggerated (Fisher, 1930; Lande, 1980). Therefore, a tradeoff occurs, since the energy cost of the development and maintenance of

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ornaments of increasing size is countered by the cost of stress (Parsons, 1995a). The most extreme ornaments should therefore occur when the stress level is relatively low in the background environment, and the size of ornaments should fall with increasing stress. Species with morphologically complex sexual ornaments should be vulnerable during periods of environmental stress (McLain, 1993), such as extinction events. For instance, McLain et al. (1995) record that sexually dimorphic bird species are more vulnerable to extinction than are monomorphic species, following their introductions into the oceanic islands of Oahu and Tahiti. Certainly, in the initial occupation of new adaptive zones, sexually dimorphic species would appear to be at a disadvantage compared with more generalist species, because of the energy costs in developing and maintaining secondary sexual characters and in sexual display, which in total may approach the maximum limit of available energy (Moller, 1994a). In many bird species the cost of secondary sexual ornaments can be reduced by an investment in physiological and anatomical adaptations. These adaptations coevolve with the secondary sexual characters, thereby permitting levels of sexual display considerably higher than those observed in their absence (Moller, 1996). This indicates strong selection at energetic limits, implying extreme vulnerability of birds to any increase in stress. Finally, and in accord with the previous considerations, a recent theoretical analysis concludes that sexual selection in a changing environment enhances population extinction by increasing selection intensities on a male trait (Tanaka, 1996). C. SPECIES BOUNDARIES In general, the available data on species boundaries are restricted to successful species, and represent end points of adaptive change during the speciation process. Accordingly, it is appropriate to consider briefly the boundaries between closely related species, especially those that are mainly sympatric. The predominantly sympatric sibling species, D. rnelanogaster and D. sirnulans, are distinguishable physiologically, based on differing resistances to environmental extremes, especially high and low temperatures, and toxic levels of ethanol and acetic acid. Furthermore, within these extremes, ecobehavioral differences indicate very different microhabitats for the species in nature, especially for larvae. Even so, these species of subgenus Sophophora are ecobehaviorally and physiologically very similar, and contrast substantially with another widespread species, D. irnrnigrans of subgenus Drosophila (Ehrman and Parsons, 1981).

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Similarly, marine sympatric invertebrate species show distinct habitat preferences defined by depth, salinity, exposure, or preference for host substrates (Knowlton, 1993). In carnivorous stoneflies (Plecoptera), eggs are laid at similar times, but newly hatched larvae rarely occur together in the same habitat, defined by hatching temperature, incubation temperature, and time of hatching, thereby largely eliminating competition btween the species (Elliott, 1995). In two closely related hymenopteran parasitoid species of Drosophila, there is odor-mediated avoidance of competition, as Leptopilina heterotoma can recognize patches on stinkhorns where groups of L. clavipes females occur (Janssen et al., 1995). These examples indicate that in responding to abiotic stresses, physiological and ecobehavioral traits are important in adapting to habitats, and are likely to be important targets of selection in evolutionary shifts underlying the speciation process. Consequently, the resources of the environment become utilized efficiently, as the sibling species do not directly compete with each other. Divergence at the ecobehavioral and physiological levels is therefore primary to morphological divergence. Only to the extent that it has a functional role can morphology be regarded as a direct target of selection (Bonner, 1988). Thermal constraints on the time and energy budgets of lizards have been investigated extensively, and upper and lower critical thermal limits can be determined (Adolph and Porter, 1993). Canyon lizards, Sceloporus merriami, have a characteristic body temperature of 32.2”C, which is lower than that of other North American desert iguanids. Under this thermal environment, individual activities (movement rate, feeding strikes, and social displays) are restricted to a 2-hr period beginning around local sunrise and to a brief period in the late afternoon. When the average temperature was around 32.2”C, maximum activity and maximum use of microenvironments occurred. However, as the temperature deviated from 32.2”C, the use of microenvironments became more constrained (Grant and Dunham, 1988; Adolph and Porter, 1993). Presumably, energy costs would increase in parallel with divergence from 32.2”C. As thermal regimes deviate from optimal, lizard activity becomes more restrictive, which is a behavior that influences home range size, population density, fecundity, social history, and ultimately survival. From populations across a range of elevations, complex relationships have been established between biophysical constraints and fitness mediated through daily time budgets and seasonal energy-mass budgets. These relationships underlie life-history variation and the adaptation of organisms to specific environments (Dunham et al., 1989). Adolph and Porter (1993) argue for the importance of activity as a connecting link between thermal environment and lizard life histories. The

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implication is that lizard activity is a target of selection, which is reasonable because of its energy cost. When the energy available for activity becomes so restrictive that there is no discretionary energy for reproduction, growth, or storage, species boundaries are likely to be located. This is in accord with the physiological constraints that appear important at the margins of distributions of an increasing number of animal taxa (see Section 1,A). 111. VARIABILITY A N D THE SURVIVAL OF VARIANTS Under environments that are demonstrably extreme, heterozygotes tend to be favored, especially for polymorphisms in natural populations. Even under less extreme conditions characteristic of the laboratory, the level of heterozygosity of individual organisms in populations tends in some cases to correlate with measures of performance or fitness, in particular growth rate and developmental stability. Enzyme loci influencing metabolism and contributing to the amount of energy available for development and growth show the most significant positive associations with heterozygosity (Mitton, 1993). Consequently, heterozygotes should be differentially favored in growth and reproduction as stress increases, and when resources become limited (Parsons, 1996b). In the white-tailed deer, Odocoileus virginianus, antler size, body mass, fat levels, and other dimensions were found to be correlated with heterozygosity, dominance status, and reproductive success by Scribner et al. (1989), who emphasized the importance of metabolic efficiency of the heterozygotes. In bighorn sheep, Ovis canadensis, horn size largely determines breeding superiority, as large horns give access to estrous ewes. In addition, such rams have superior foraging ability, energy efficiency, and disease resistance (Hogg, 1987). In the seventh year of life, which is around the time of onset of breeding, 21% of variation in horn volume can be explained by an association with heterozygosity. In contrast, the horns of young rams show little variation in size that is attributable to genetic factors (Fitzsimmons et al., 1995). Therefore, when energy demands from the development and maintenance of horns and from the mating process itself are high, heterozygote advantage is maximal. In any case, mating is an expensive process energetically, and fitness assessed by mating success can often be related to available metabolic energy (see Section 11,B). Consequently, heterozygotes should be favored during mating, as documented in a number of species, especially insects and fish (Thornhill and Gangestad, 1993). Furthermore, Rolan-Alvarez et al. (1995) found a positive association between heterozygosity and sexual fitness for males in populations of the marine snail, Littorina mariae.

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In the context of this discussion, competition can be used as an example of stress under laboratory conditions. In offspring from a diallel cross involving three inbred strains of mice, several traits were studied in a normal cage, and a smaller cage with enhanced crowding. In the normal cages, 14% of inseminated females did not produce offspring; 29.4% did not in the smaller cages, suggesting that crowding reduced reproductive fitness. Additive genetic variability increased under crowding stress, especially for preimplantation mortality, litter size, and relative adrenal weight. For preimplantation mortality and litter size, nonadditive effects and heterozygote advantage increased under stress (Belyaev and Borodin, 1982). Genetic variability for behavioral traits can therefore be high under stress (Parsons, 1988). These and many other examples show that under highly stressed situations, especially in free-living populations, genetic variability is not normally expected to be restrictive. In addition to heterozygote advantage under stress, there is a substantial body of data indicating increased mutation, recombination, developmental variability, and phenotypic variability as stresses approach levels where extinctions become a real possibility (Parsons, 1987; Hoffmann and Parsons, 1991). For novel variants, the issue then turns to the conditions under which their survival and reproduction is likely. Following Fisher (1930), the chances of survival of a novel variant should be inversely related to the magnitude of its phenotypic change, or in the context of this discussion, the energy cost of the change. In addition, survival should be inversely related to the magnitude of energy cost of existing in a variable environment, so that the more extreme the environment, the smaller the change that can be accommodated by organisms for their survival (Parsons, 1996b). In summary, the level of genetic variability is unlikely to be restrictive for adaptation, but the ecological conditions determining the survival of the variants may be. It is in this light that the issue of extending the limits of adaptation in populations will now be considered, for a continuum of environments, from extreme at species borders to benign, where learning is possible. The survival of variants should increase as conditions become less severe, even though variants can apparently appear under all conditions.

I v . EXTENDING THE LIMITS OF ADAPTATION A. ABIOTIC STRESSES A N D RESOURCES Speciation necessarily involves a shift in the limits of adaptation of established species. Therefore, the process of speciation, approached ecologi-

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cally, implies energy costs (Van Valen, 1976a,b). Shifts in limits can in principle involve changes in resistance to abiotic stresses, changes in resource availability and usage, or a combination of these variables. Commencing with abiotic stress, thermophilia occurs in some desert ant genera, enabling successful foraging for arthropods that have succumbed to extreme heat. For instance, the Saharan silver ant, Cataglyphis bombycina, scavenges for the corpses of insects and other arthropods that have SUCcumbed to the heat stress of their desert environment in a small thermal window with a maximum width of 7°C (46.5-53.6"C). The boundaries of the window are underlain by predatory pressure exerted by a desert lizard at the lower limit and heat stress at the upper limit (Wehner et al., 1992). Parallel situations occur in the Australian ant, Melophorus bagoti (Christian and Morton, 1992), and in the burrowing spiders Seothyra in Namib desert dunes (Lubin and Henschel, 1990). Finally, the diamond above, Geopelia cuneara, an inhabitant of the arid savannahs and semideserts of Australia, is extremely heat tolerant, and consequently activity occurs throughout the day under dry and hot conditions when potential predators and food competitors are reduced (Schleucher, 1993). These are examples of extreme abiotic stress, where predators and competitors are likely to be absent, enabling the occupation of extreme habitats. Ultimately, as found in the lizard, Scleroporus merriami, at extreme temperatures, the energy for activity becomes so restricted that there is no discretionary energy for reproduction, growth, or storage, and species boundaries occur (Adolph and Porter, 1993). Heat shock protein synthesis may occur in association with thermotolerance, as found in the ant Cataglyphis (Gehring and Wehner, 1995). However, the formation of heat shock proteins is likely to have a metabolic cost, thereby reducing fitness (Krebs and Loeschke, 1994). Consequently, assuming that species boundaries are regions of energy restriction, it seems difficult to envisage much widening of windows of opportunity for direct abiotic extremes of climatic origin, especially as the survival of novel variants would be unlikely. Turning to resources, innovation can involve ecobehavioral traits in shifting to alternatives at stressful times (Parsons, 1993b). Examples include: (1) the evolution of specialization of D. sechellia onto a single resource, Morinda citrifolia, from a stressful window of opportunity from D. simulans, which finds the resource toxic (R'Kha et al., 1991); (2) the evolution of host races of a stem-galling tephritid, Eurosta solidaginis, on two goldenrod host species assisted by a 10- to 14-day difference in emergence times on the two hosts (Craig et al., 1993); and (3) the evolution of races of the tephritid fly, Rhagoletis pomonella, from its native host hawthorn to introduced fruits maturing at different times (Feder et al., 1988).

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Therefore, resource heterogeneity can underlie divergence, especially if associated with the simultaneous need to adapt to some abiotic stress. The summed environmental change must be intense enough to cause disruptive selection for sufficiently long that any incipient divergence can become established, and consequently to have the potential to lead to isolation. A possible example comes from the intertidal snail, Littorina saxatilis, where there is assortative mating leading to incipient reproductive isolation associated with habitat selection by two morphs; one of these occurs in the uppershore barnacle belt and the other in the lower-shore mussel belt, indicating physiological and behavioral adaptations by the morphs to the two differing environments (Johannesson etal., 1995). In contrast, in the Galapagos finch, Geospiza conirostris, partial isolation of a population based on resource heterogeneity occurred following a drought, but prolonged divergence was prevented by extreme fluctuations in the abiotic environment (Grant and Grant, 1989).

B. RESOURCE POLYMORPHISMS Genetically based resource and habitat polymorphisms permit the occupation of more than one niche within a species, and can underlie divergence ( West-Eberhard, 1986; Stanhope et al., 1992). For instance, sympatric populations of the tropical sponge-dwelling coral-reef shrimp, Synalpheus brooksi, occupy two alternative host species of sponge, and in laboratory situations tend to choose native sponge species. This promotes assortative mating and hence divergence, as shown by significant host-associated genetic divergence of shrimp in two of three reefs based on proteinelectrophoretic variation (Duffy, 1996). In the Arctic charr, Salvelinus alpinus, there are benthivorous, planktivorous, and/or piscivorous forms in lakes in Iceland, which show substantial morphological, developmental, and behavioral specialization for discrete resource categories. The behavioral differences break down when food is artificially superabundant, occurring only in the nutritionally restricted environments of free-living populations (Skulason et al., 1993). Under these latter conditions, energy returns to charr appear to be maximized by genetic divergence among morphs, enabling the efficient exploitation of differing resource categories. Novel variants promoting such divergence would be favored on grounds of energetic efficiency. Schluter and McPhail (1993) record multiple examples of fish in lowdiversity postglacial lakes, where there are sympatric species involving limnetic and benthic forms. The limnetic forms, which exploit plankton in open water, are typically smaller, with a narrower mouth and longer, more numerous gill rakers than the benthic forms, which consume larger prey;

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the morphological differences are adaptations to differing food requirements. The benthic-limrtetic split could therefore be a predictable first step in the diversification of many fish taxa (Schluter and McPhail, 1993), and this split would be favored by energy efficiency in resource utilization. While Skulason and Smith (1995) argue that resource polymorphism has been underestimated as an evolutionary force leading to divergence, this could be precluded by abiotic instability, as noted in the finch G. conirosfris. More generally, during a 2-year California drought in 1976-1977, pressures on development time intensified in colonies of the specialist insect herbivore, the butterfly Euphdryas editha, because host plants senesced rapidly (Ehrlich et al., 1980). Conversely, continuous rainfall can retard postdiapause larval development so that adult flight is delayed beyond plant senescence (Dobkin et al., 1987). Such climatic perturbations would appear sufficient to swamp the selection for energy-use efficiency based on resource polymorphisms that can occur under more stable and less stressful abiotic conditions. The utilization of heterogeneous resources therefore is likely to be the most efficient when organisms d o not simultaneously need to cope with the energy costs of extreme stresses (see also Section 1,B). C. LEARNING The finch Pinaroloxias inornata, of Cocos Island, Costa Rica, has extremely generalist feeding habits, spanning those of several families of birds on the mainland, encompassing insects, Crustacea, seeds, fruits, nectar from many flower species, and perhaps lizards. In contrast, individuals feed as specialists year-round, often using just one of the many feeding techniques and resources observed at the population level. Apparently, these specializations are transmitted at least partly culturally, from the observation of other individuals. Hence, these tropical birds have developed learning ability, permitting the exploitation of heterogeneous resources (Werner and Sherry, 1987), which implies high energy-use efficiency. The ecological situation on Cocos Island appears permissive of this situation, as it is an aseasonal environment with very few competing species, and with high availability, variety, and predictability of food resources. Under these circumstances of relatively low energy constraints from the environment, specialization has apparently occurred. Ultimately, such behavioral specialization could be assimilated genetically, perhaps following varying biochemical demands made on finches from differing food categories. For instance, differences in feeding behavior in the crustacean Gammarus palustris are associated with genetic variation in the properties of a digestive enzyme (Guarna and Borowsky, 1993).

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Another example of learning comes from bluegill sunfish, Lepomis macrochirus, in North American freshwater lakes, where learning assisted the behavioral modification needed to search efficiently in vegetated and open-water habitats (Ehlinger, 1990). Habitat-specific foraging efficiency occurred, thereby increasing the energetic effectiveness of resource exploitation. Therefore, behaviors governing resource use may be influenced by the previous experience of individuals. In insects, prior exposure to a particular resource can enhance a female’s tendency to oviposit on that type of resource. For instance, in the true fruit fly, Rhagoletis pomonella, the propensity to accept a particular fruit prior to the deposition of an egg can be modified by previous ovipositional experience (Prokopy and Papaj, 1988). Learning should assist in exploiting windows of opportunity presented by introduced fruit species, which would be enhanced if mating occurred at the resource. Learning may therefore assist in adaptation to new hosts from the original host. Hence, following Baldwin (1896) learning may be a factor in switches into novel habitats, thereby assisting in the integration of genetic components of behavior into the gene pool. As learning eases the process of genetic change (Anderson, 1995), the energy costs in the occupation of novel habitats would be reduced. For instance, fifteen-spined sticklebacks, Spinachia spinachia, attack Gamrnarus and Artemia more efficiently as a result of experience. By decreasing handling time, learning increased the profitability of specific prey, expressed in terms of energy expended per given time period (Croy and Hughes, 1991).

V. FROM STRESS-RESISTANCE GENOTYPES TO A CONNECTED METABOLISM

A. STRESS-RESISTANCE GENOTYPES Koehn and Bayne (1989) argue that high stress resistance is associated with the efficient use of metabolic resources for growth and reproduction, especially when resources are limited. Since stress-resistance phenotypes tend to have a low metabolic rate (Hoffmann and Parsons, 1991), a low maintenance requirement is implied. Consequently, growth should be supportable over a wide range of conditions. In particular, the association between metabolic efficiency and stress resistance suggests that genes for stress resistance should be favored during the metabolically costly process of the development and maintenance of sexual ornaments and mating itself (Parsons, 1995a). During mating, the preferred male trait may reflect the underlying genetic quality of the male, so that females mating with these males gain additional

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advantages for themselves or their offspring outside of mating (Thornhill and Alcock, 1983). Such advantages are conventionally regarded as being under the control of “good genes,” which enhance fitness both during the mating process, conferring direct benefits to females, or by producing offspring with superior fitness (Moore, 1994). Wedekind (1994) argued that sexual selection for stress-resistance genes is important in improving the survival chances of offspring. In other words, mate preferences would be most efficient if coupled with resistance genes in parents and offspring. Following Hamilton and Zuk (1982), this conclusion comes from an assessment of parasite-driven sexual selection. In the pheasant, Phasianus colchicus, male spur length correlates with male viability, female mate choice, and offspring survival (von Schantz et al., 1996). Genetic analyses show that the major histocompatibility complex genotype is associated with variation in male spur length and male viability. Von Schantz et al. (1996) conclude that these data directly support the “good genes” hypothesis (Hamilton and Zuk, 1982) that females discriminate among males based on secondary sexual characters, and so pass on genes for disease resistance that improve offspring fitness. In any case, a premium on stress resistance and hence metabolic efficiency conferring overall fitness is expected, assuming that populations are normally exposed to high levels of stress (Parsons, 1996b, 1997a). Furthermore, because “good genes” reflect fitness under these environmental conditions, it should be possible to incorporate other fitness traits into this scheme. For instance, in an African cockroach, Nauphoeta cinerea, females have offspring that develop relatively quickly following mating with the most attractive males (Moore, 1994). This suggests that the choosing female prefers individuals carrying “good genes,” which also underlie rapid development. Additional examples cited by Moore (1994) include heritable variation in plumage as an indicator of viability in male great tits, Parus major (Norris, 1993), and improved growth and survival of offspring of peacocks, Pavo cristatus, with more elaborate trains (Petrie, 1994). In the damselfly, Zschnura graellsii, Corder0 (1995) found that the best predictor of male lifetime mating success was mature life-span. In barn swallows, Hirundo rustica, Mdler (1994b) found that offspring longevity is positively related to that of their fathers, and to the ornament size of the male parent. Considering aging, assuming that a long life-span and rapid development depend on metabolically efficient stress-resistance genes, individuals having high inherited stress resistance should develop fastest and live longest (Parsons, 1996b,c). Accordingly, ornament size, mating success, longevity, and development time can perhaps be viewed as a coordinated suite of characters assuming the stressful environments of free-living populations. If a major target of selection of stress is at the level of energy carriers, “good

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genes” therefore should be stress-resistance genes, and these should be increasingly important for ensuring fitness as limits to adaptation are approached. O n a cautionary note, the paucity of empirical observations for this predicted relationship presumably relates to the point that studies carried out under relatively benign laboratory conditions are unlikely to be efficient in revealing such associations, because selection for stress resistance is necessarily less intense than in free-living populations. On the other hand, irrespective of the background environment, associations of development time and life-span with mating success and the size of sexual ornaments should be the most readily detectable, because mating and the development and maintenance of sexual ornaments are normally energetically expensive processes. Lifetime reproductive success has not been considered to any extent in this article, and in any case it is usually strongly correlated with longevity. However, direct extrapolations from laboratory to natural populations cannot be assumed. For instance, in D. melanogaster, substantial and variable deficiencies in food availability under natural conditions preclude the expression of reproductive potential (BoulCtreau-Merle et af., 1987). In any case, adults of English Drosophila populations had a mean life expectancy of 1.3 to 6.2 days, which is at least an order of magnitude less than survival under equable laboratory conditions (Rosewell and Shorrocks, 1987). In a recent review of genetic variation and aging, Curtsinger et al. (1995) argued for a model where old and young fitness components are correlated, which is in accord with a prediction from the stress theory of aging (Parsons, 1993b). Accordingly, survival at any age should be a predictor of lifetime reproductive success in free-living populations (see Parsons, 1997b, where this conclusion is considered in the light of various evolutionary theories of aging).

B. FITNESS A N D METABOLIC EFFICIENCY In Section 111, it was noted that heterozygosity levels tend to be correlated with fitness during the mating process, especially for enzyme loci controlling metabolism and hence energy availability. For instance, in bighorn sheep, Hogg (1987) argued that this association reflects a “good genes” strategy favoring heterozygotes at an energetically demanding time. Extending to other fitness traits, in particular development rate but also life-span, substantial evidence suggests that heterozygosity tends to be associated with high fitness in a wide range of taxa, especially under stressful circumstances (Mitton, 1993; Parsons, 1996b,c, 1997a).

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Consequently, two approaches imply parallel associations for a range of fitness traits. The first approach commences at the whole organism level and leads to genes for stress resistance for promoting fitness, while the second approach commences at the gene level using electrophoretic variants, and leads to generalized heterozygous advantage for promoting fitness under stress. Although these approaches have developed largely independently, they can be linked by a requirement for metabolic efficiency in the face of the stress to which free-living populations are normally exposed. Detailed gene location studies based on natural populations appear necessary for additional elaborations. The generalized advantage of heterozygotes under stress does, however, suggest that many interacting loci may be involved in promoting metabolic efficiency, so that it appears more appropriate to talk of “good genotypes” than good genes. This does not, of course, preclude the involvement of some major genes, such as the more anodal allozymehozyme at the phosphoglucose isomerase locus, which is favored in a range of stressful situations, including high temperature, high salinity, anoxia, and desiccation in natural populations of a wide range of taxa (Riddoch, 1993). In summary, a wide-ranging literature suggests that stress resistance and metabolic efficiency are associated for a range of fitness measures (Table I). The ranking 1 to 10 in Table I represents a continuum of organizational levels ranging from the essentially molecular (1) to the organismic. The items of main concern in this paper are categories 7 and 8, and correlations with other life-history characteristics, especially 6 and 9, are noted under 10.

TABLE 1 ASSOCIATIONS PREDICTED I N STRESSED FREE-LIVING POPULATIONS“ ~~~~~~~

1. Stress-resistance genes

2. High (electrophoretic) heterozygosity

3. High vitality, vigor. and resilience 4. High homeostasis in response to external stresses 5. Low fluctuating asymmetry 6. Rapid development 7. High male mating success 8. Extremes of sexual ornaments 9. Long life span 10. Positive correlations among fitness traits a See Parsons (199%. 1966b.c. 1997a) for detailed discussions from which this table was derived.

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Items 3-5 are various measures of homeostasis, from the morphological to physiological levels. For instance, survival to an old age is associated with high vitality, vigor, and resilience (3), and high homeostasis in response to external stresses (4). Fluctuating asymmetry (FA) measures the degree to which an individual can control development under given environmental and genetic conditions ( 5 ) , and is a measure of individual phenotypic quality or fitness (Zakharov, 1989; Parsons, 1990; Markow, 1994; Polak, 1997; Moller, this volume). One manifestation of energy dissipation is increased FA (Mitton, 1993), for instance the FA of antlers of reindeer is positively correlated with parasite intensity (Folstad ef al., 1996). Accordingly, low F A should occur in organisms in which metabolic efficiency or fitness is highest (5). Similarly, low FA should be associated with genes for stress resistance, which implies that FA should be heritable to some extent, as noted from associations between development rate and life-span (Parsons, 1996d), but more generally from a meta-analysis of 29 studies of 13 species, which revealed a mean heritability of FA of 0.27 (Moller and Thornhill, 1997). Furthermore, because the level of heterozygosity of organisms tends to correlate with performance or fitness, correlations with high FA should be maximal in heterozygotes. There are now sufficient data sets to infer that rapid development, a long life-span, success in mating, and extremes of sexual ornaments tend to be associated with low FA, and this tends to be clearest in heterozygotes. However, there is a need to devise laboratorybased experiments to model the environments of free-living populations to obtain additional empirical data to explore these apparent and rather tentative generalizations more directly. Finally, the extreme stress scenario, which is the basic assumption underlying this paper, gains support from Kauffman (1993) who argues that the normal situation faced by organisms is an extremely perturbed world. Under these circumstances, he argues that a connected metabolism is important for the facilitation of adaptive change in response to environmental challenges. There is a convergence with the model in this paper, as the associations in Table I are underlain by selection by environmental stress, which targets energy carriers in free-living populations. In any case, an energetic approach to fitness has appeared previously. For instance, Van Valen (1976b) argued that energy underlies fitness, which can then be viewed as the rate at which resources, exceeding those needed for growth and maintenance, are available for reproduction in the broadest sense (Brown et al., 1993). In the context of this paper, mating, the development and maintenance of sexual ornaments, and various nonsexual behaviors can extract substantial energy from resources, and so may be critical in determining limits to adaptation in extreme environments.

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V1. SUMMARY Energy expenditure is a prerequisite for organisms to exist in any habitat, as exposure to biotic and especially abiotic stress is the norm in free-living populations. Therefore, the distribution and abundance of organisms can be related to energy balances, derived from the costs of various stresses interacting with gains from resources. Consequently, the behavioral selection of preferred habitats imposing low energy costs is adaptive. On the other hand, limits to adaptation occur when available energy becomes totally restrictive. Therefore, energetically costly behaviors, especially those involving sexual selection, are important in determining limits. Assuming that species borders are regions of energy restriction, it is difficult to envisage much widening of windows of opportunity for direct stresses of climatic origin. However, when combined with resource heterogeneity, evolutionary divergence led by behavioral shifts appears more likely, provided that abiotic perturbations are not extreme. In abiotically benign environments, implying minimal energy constraints, resource use specialization by learning appears possible. Heterozygotes tend to be favored in extreme environments because of their energy and metabolic efficiency. Therefore, genetic variability is unlikely to be restrictive in stressed free-living outlier populations; however, ecological circumstances can preclude the survival of novel variants. Consequently, the primary key to understanding limits to adaptation for behavioral traits is likely to be ecological. Under stressed free-living conditions, favored “good genotypes” are likely to be stress resistant and heterozygous. An association between success in mating, the development of extreme sexual ornaments, rapid development, and a long life can be postulated based on the metabolic efficiency of stress-resistance genotypes. While these postulated associations among fitness traits are supported by only limited empirical evidence, they may be important in any habitat where organisms are close to their limits of survival. If many organisms are born but few survive to reproduce because of climatic stress interacting with and causing nutritional stress, this situation may be quite normal. Although I contend that this model of the environment is generally valid, a reference point for comparisons with more benign environments is certainly provided.

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