Environmental stress, adaptation and evolution: an overview

Environmental stress can be characterized as a force shaping adaptation and evolution in changing environments, and it is a property of both the stressor and the stressed. Here we aim to give an overview of the state of the art of evolutionarily orientated stress research and the progress it has made during the last decade. We do this by introducing the contributions to this issue of the Journal of Evolutionary Biology that resulted from a workshop held in August 2004 in Sandbjerg (Denmark), sponsored by the European Society of Evolutionary Biology (ESEB). Naturalists continually refer to external conditions, such as climate, food but is it preposterous to attribute to mere external conditions, the structure, for instance, of the woodpecker, with its feet, tail, beak, and tongue, so admirably adapted to catch insects under the bark of trees. (Darwin, 1875) The statement above by Darwin can already be found on the second page of the introductory chapter of his On the Origin of Species by Means of Natural Selection and expresses his view that, even though adaptation of individuals to their natural physical and biotic environment is central in his theory of evolution, he thought that this was mainly governed through intra and interspecific competition. To Darwin, competition between ‘organic beings’ was far more significant than adaptation to environmental conditions. This preponderance of competition in his theory is expressed even more clearly in Chapter III of the book. Based on the observation that many organisms produce far more offspring than necessary to sustain their numbers, he describes his basic idea concerning the ‘struggle for existence’ that forms the foundation of his theory of evolution and states that numbers are not so much limited by lack of adaptation to particular climates but much more by the competition with other ‘organic beings’: On the confines of its geographical range, a change of constitution with respect to climate would clearly be an advantage to our plant; but we have reason to believe that only few plants or animals range so far, that they are destroyed exclusively by the rigour of the climate. Not until we reach the extreme confines of life, in the Artic regions or on the borders of an utter desert, will competition cease. (Darwin, 1875, p. 60) In environments that are generally rather stable and have a continuous high energy and biomass production, such as some tropical or marine environments, the above-cited view of Darwin may be a proper description of the forces that shape the distributional range and abundance of species. However, in temperate climates, where the environment is more variable and unpredictable, this may not be an appropriate description any more. There environmental stress may have a significant impact on the evolutionary and ecological processes that affect and shape the genetic structure and evolution of populations, as indicated by data obtained from natural populations during the 1940s and 1950s by Drosophila researchers like Timofeeff-Ressovsky and Dobzhansky. Their investigations have led to increased interest in studying the role of environmental stress in relation to natural selection for stress resistance and adaptation. After a brief period during the 1970s and 1980s when most interest was directed to neutral evolution (Kimura, 1983), evolutionary adaptation has been receiving increasingly more attention as is evinced by the publication of a number of monographs on these issues during the last decades (e.g. Calow Hoffmann Bijlsma Sørensen et al., 2005). In addition, biotic stresses, such as competition, predation, and parasitism, can also cause stress (Relyea, 2005). Although abiotic and biotic stress can act independently, these two types of stress often act synergistically, as organisms that have suboptimal fitness because of abiotic stress often suffer more from predators and parasites. However, as pointed out before, environmental stress can only be valued in relation to the organism experiencing the stress, and therefore stress also has an intrinsic component. Genetic changes in organisms and populations brought about, for instance, by inbreeding or other changes in the genetic architecture of organisms or populations, can drastically change the perception of an otherwise unchanged (stress) environment, resulting in what is sometimes called ‘genetic stress’ (Bijlsma et al., 1997, 2000). Consequently, inbred populations may suffer greatly from changes in the environment that by noninbred populations would be perceived as nonstressful. This indicates that intrinsic and extrinsic stress may often strongly interact, and there is increasing evidence that this leads to a strong synergism between the two stresses causing normally nonsevere stresses to become harmful when combined (Jiménez et al., 1994; Bijlsma et al., 2000; Keller et al., 2002). As the extrinsic and intrinsic causes of stress generally occur together in a nonadditive manner, they should preferably be investigated jointly. This is particularly important as the growing human population causes major changes in the biotic and abiotic environment at an unprecedented scale and a fast rate. Global warming causing thermal stress and pollution exerting chemical stress go hand in hand with destruction and fragmentation of natural habitats. As the latter will inevitably go together with smaller and more isolated populations that become subject to genetic erosion, many populations and organisms will simultaneously experience deteriorating environmental conditions and genetic stress (Frankham, 2005). Therefore, understanding the nature, interactions and consequences of these stresses at a global scale from an ecological and evolutionary perspective is of the utmost importance, not only to understand the processes involved, but also to develop and evaluate possible countermeasures. Like stress, adaptation is also a concept that often causes confusion as it is used in many different ways and contexts, and many definitions are simply physiologically oriented and less suitable in an evolutionary context. In a general sense, adaptation can be defined as the process of change in an organism to conform better with (new) environmental conditions, whereby the organism (or group of organisms) acquires characteristics, involving changes in morphology, physiology or behaviour, that improve their survival and reproductive success in the particular environment. Such changes can occur phenotypically, within a set genotype, and then phenotypic adaptation is the result of what is called ‘phenotypic plasticity’, the capability of a genotype to change its phenotype according to prevailing environmental conditions. Morphological changes and other inducible defences as modelled or described for tadpoles and Daphnia in response to the presence of predators fall within this category (Gabriel, 2005; Pauwels et al., 2005; Relyea, 2005), but also maternal effects in a parthenogenetic strain of Drosophila mercatorum (Andersen et al., 2005). Adaptation can also occur through changes in allele frequencies as a result of the selection pressure exerted by the environment (e.g. David et al., 2005; Lindgren Sørensen et al., 2005). This process is known as genotypic adaptation or evolutionary adaptation. As the occurrence of plasticity and possibly also the degree of plasticity are genetically based, both these phenomena are important from an evolutionary perspective. Adaptive traits may also be the result of correlated responses, in that selection is not directly acting on the trait of study (Bubliy Hoffmann et al., 2005; Malherbe et al., 2005). A better understanding of genetic correlations and trade-offs in a stress scenario can be achieved by artificial selection experiments. However, it is important to note that at least some if not most of the correlated responses and/or trade-offs may be genotype (population) and/or environment specific. Although the occurrence of the adaptive process in evolution is well documented and also clearly shown by the fact that many organisms have adapted quite rapidly to man-made changes in the environment (e.g. pollution, pesticides, thermal stress; Bradshaw, 1952; Woods, 1981; Macnair, 1997; Hoffmann et al., 2003), we still know little about the dynamics of the adaptive process, and several models are still to be explored and tested. Already in the 1930s, during the foundation of population genetics theory, controversy arose about the mode of genetic and adaptive changes underlying evolution. According to Fisher, evolution proceeded at the genetic level mainly by largely independent allele substitutions at many loci, each having little effect on fitness (Fisher, 1930). Wright, on the other hand, argued, that populations often are characterized by ‘co-adapted’ combinations of alleles at interacting loci (Wright, 1931). The question is clearly of great fundamental importance, since in Wright's view the genetic structure of populations may constrain evolutionary changes because natural selection will often be unable to carry a population through an adaptive valley, and the valley can only be crossed ‘by chance’, i.e. through genetic drift. The importance of Wright's view is that it would explain the occurrence of phenomena like (negative) epistatic interactions, the cost of resistance and compensatory evolution, and possibly partly inbreeding depression. In Fisher's view, natural selection will essentially always be able to improve the adaptedness of populations, provided sufficient genetic variation is present. This controversy has never been fully resolved, and today population geneticists are still divided in their opinions on this matter (e.g. Coyne et al., 1997; Wade Pedersen et al., 2005). In our opinion, the contributions on environmental stress appearing in this issue of the Journal of Evolutionary Biology represent a broad cross-section of the current state of the art in evolutionary research in environmental stress, with particular focus on a few specific topics. Several papers are concerned with the role of inbreeding and the rate of inbreeding for fitness and evolutionary potential with clear-cut implications for conservation biology (Frankham, 2005; Kristensen et al., 2005; Pedersen et al., 2005). Experimental evolution with rapidly growing and reproducing organisms has recently been used successfully to test some basic issues of evolutionary adaptation, such as on the rate of compensatory evolution and adaptation (de Visser Schoustra et al., 2005). Artificial selection experiments for stress resistance are used to test for correlated responses and trade-offs (Bubliy Hoffmann et al., 2005) and to address functional relationships among traits (Malherbe et al., 2005). Thermal adaptation along climatic gradients is the topic of another set of papers studying variation in life history traits along latitudinal and altitudinal gradients (David et al., 2005; Lindgren Sørensen et al., 2005). phenotypic plasticity and maternal effects are the focus of another set of papers (Andersen et al., 2005; 2005; Pauwels et al., 2005; Relyea, 2005). the role for selection on Schoustra et al., 2005), the importance of genotype environment interactions (Bubliy Relyea, 2005). 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