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Evolutionary Challenges of Extreme Environments (Part 2) TALBOT H

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Evolutionary Challenges of Extreme Environments (Part 2) TALBOT H 130JOURNAL OF EXPERIMENTAL T.H. WATERMAN ZOOLOGY (MOL DEV EVOL) 291:130–168 (2001) Evolutionary Challenges of Extreme Environments (Part 2) TALBOT H. WATERMAN* Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut, 06520-8193 Despite a plethora of theories, basic laws of na- deals with relative growth and quantitatively pre- ture seem elusive in biology even though they have dicts the relation between metabolic rate and size usually been considered the ultimate goal of phys- in major groups from microbes to elephants (Smil, ics and chemistry (Waterman, ’68). Perhaps their 2000). Despite much data and thought, a widely evasiveness in biology stems from the quite spe- acceptable explanation of this impressive gener- cial entities with which it deals. Living beings alization remains to be agreed upon (Dodds, et have many complex components, dynamically in- al., 2001). Quite often, such biological rules are terconnected in multiple ways. These are clearly soon forgotten, or frequently rejected, sometimes rather different from those of a falling apple, ra- with jeers, by second thoughts of others. Yet some diation propagating through space, or the com- of them have considerable staying power. bustion of glucose in a flask filled with oxygen For instance, life’s vigorous persistence in an gas. Some scientists suggest that biology is more unstable and often highly stressful world may de- like engineering, because it often uses the laws of pend quite typically on two pairs of remarkable, physics and chemistry to explain living material seemingly contradictory, traits: and its information systems (Hengeveld and • diversity and unity Walter, ’99). Whether this is true or not, biology • flexibility and stability and engineering often have mutually rewarding roles as in cybernetics and robotics (Ritzmann et On the one hand, the exuberant diversity of the al., 2000). millions of different species and kinds of living Even so, quite a few broad rules or laws about things, plus their innumerable component organs, life have been proposed. Arguably, the broadest cells, genes and special protein molecules, would and most persistent of such laws (Kleiber’s Law) seem to contradict any notion of underlying uni- formity. On the other hand, all living organisms are This essay is a more technical and detailed version of the last chapter of the author’s book about extremophile animals, Animal built of the same chemical elements and do func- Frontiers, to be published by the Yale University Press. Some addi- tion basically in the same way, subject to the clas- tional material has been drawn from earlier chapters to make this part of the book stand on its own. Part one of three (Waterman, 1999) sic laws of thermodynamics. In other words, they focused on currently productive ways to study the evolution of ani- all share a remarkable unity, particularly in the mals living on the environmental frontiers. This second part concen- trates on relevant long-term evolutionary trends and their relation nature of cytoplasm, the anaerobic core of energy to natural selection in extremophiles. The last part will discuss evo- metabolism, the basic genetic code, and the drives lution and the environment, including the frontiers, as well as sources of phenotypic variation, evolutionary rates, and extinction as poten- to survival and self-replication. This oneness of tial components of extremophile evolution. life imposes limits and constraints on evolution Part 1 of this discussion already showed that the challenges of the essay’s title are twofold. Biologically, potential animal extremophiles that often seem to be overlooked by biologists. have been frequently challenged for at least 500 million to 600 mil- In addition, flexibility and stability also appear lion years to maintain their fitness in environments that demanded greater hardiness and more stress avoidance than they had previ- quite opposite. Yet they are complementary and ously experienced. Failure to meet such environmental challenges necessary aspects of life in a world with many obviously would block a species or its group from becoming more extremophilic despite the currently steep deterioration of global habi- kinds of habitats, constantly changing on shorter tats. Professionally motivated biologists are also challenged to ex- tend and integrate the rather scattered and sparse existent data on extremophile evolution, as well as to analyze the mechanisms re- sponsible and their ultimate relevance to the rapidly changing bio- *Correspondence to: Talbot H. Waterman, Department of Molecu- sphere and its future. lar, Cellular, and Developmental Biology, 902KBT, Yale University, Part 3 will discuss sources of phenotypic variation, rates of evolu- P.O. Box 208203, New Haven, CT 06520-8193. tion extinction as a component of evolution, and extremophiles’ future. Received 22 August 2000; Accepted 12 December 2000. © 2001 WILEY-LISS, INC. EVOLUTIONARY CHALLENGES IN EXTREME ENVIRONMENTS 131 or longer scales of time and space. Diversity and through natural selection, should not to be con- flexibility (plasticity, evolvability) are obviously sidered adaptive (Rose, ’96). But more general central to our preoccupation with evolution. Yet definitions are commonly used by scientists and they are critically interrelated with the unity and engineers referring to the adaptation, Darwin- stability that have been responsible for life’s per- ian or not, of many complex systems, both biotic sistence for billions of years. and nonbiotic: for instance, sophisticated robots Another more controversial aspect of life relates (Ritzmann et al., 2000; Frank, ’96; Givnish and to its adaptedness. Observers of nature have for Sytsma, ’97; Auyang, ’98). millennia noticed that animals and their environ- As is evident from this essay, the author, as an ments seem to match each other, often to an ex- emeritus comparative physiologist who worked traordinary degree. Such correlations are often mainly on underwater vision and orientation particularly dramatic in extremophiles. Desert (Waterman, ’81; Waterman, ’82; Waterman, ’97), animals, polar animals, deepsea animals, and high was used to a far broader definition of adaptation mountain animals, for instance, are usually no- (Slobodkin and Rapoport, ’74) than one based table for a variety of structural, functional, and strictly on its evolutionary dependence on natu- behavioral features closely correlated with the ral selection. Adaptation and accommodation in stressful aspects of their extreme habitats. These eyes, as well as many other kinds of physiological correlations with the environment have long been regulation, acclimatization, behavior, learning, re- called adaptations and have often been considered productive and developmental patterns, pheno- as basic characteristics of life. typic plasticity, symbiosis, human culture and so In the 1960s and 1970s, the Darwinian belief on, are surely parts of the usual match between that this pervasive match between organisms and organisms and their environments (Frank, ’96), their environment arose mainly if not exclusively, not to mention the fitness of the environment it- by natural selection, was widely accepted by bi- self (Henderson, ’13). Clearly, adaptation as Dar- ologists (Amundson, ’96). Even so, the interdisci- win conceived it is not the only factor in the whole plinary research necessary to prove such a causal evolutionary process. link was scarce, difficult to carry out, and, in fact, Another broad biological rule of some interest not widely pursued despite considerable specula- here is Malthus’s Law. It was suggested in part l tion that fine-tuned adaptation was indeed the of this essay to be an emergent universal prop- rule. This state of affairs was vigorously de- erty of life arising from its complex system prop- nounced by Gould and Lewontin in 1979 (see erties and providing a critical internal driving also Pigliucci and Kaplan, 2000) amid archi- force relevant to animal evolution (Koslowski, ’99). tectural and literary flourishes, and for some If so, this “law” might explain how animals are readers, potential links with the “sociobiology impelled into becoming extremophiles. Malthus’s wars” (Brown, ’99; Sterelny and Griffiths, ’99; Law states that living things tend to reproduce Segerstråle, 2000). themselves indefinitely until their numbers reach This outspoken indictment criticized weakly or exceed the limits of the ecological resources they documented evolutionary “adaptationism” and the require, including living space. irresponsible “adaptationists” who practiced or The resulting Malthusian population pressure accepted it. Whether from guilt as charged, or to expand any given animal’s range was suggested sheer vulnerability, a topic of central interest to as a likely mechanism bringing animals to the biology, seemingly at one blow became a pejora- frontiers of extreme environments and constantly tive term not to be mentioned in respectable com- challenging their capacity to survive greater pany. Some 20 years later adaptation and its stresses. In addition to this increase in biological degree of precision are still matters of controversy numbers that creates crowding pressure for ex- (Weibel et al., ’98). Yet there are sustained signs pansion, several other possible evolutionary trends that the subject may be making a substantial were mentioned briefly in part 1. Despite some comeback (Rose and Lauder, ’96; Bijlsma and risk of resurrecting old controversies, these de- Loeschcke,
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