Comparative Evolution: Latent Potentials for Anagenetic Advance (Adaptive Shifts/Constraints/Anagenesis) G

Proc. Natl. Acad. Sci. USA Vol. 85, pp. 5141-5145, July 1988 Evolution Comparative evolution: Latent potentials for anagenetic advance (adaptive shifts/constraints/anagenesis) G. LEDYARD STEBBINS* AND DANIEL L. HARTLtt *Department of Genetics, University of California, Davis, CA 95616; and tDepartment of Genetics, Washington University School of Medicine, Box 8031, 660 South Euclid Avenue, Saint Louis, MO 63110 Contributed by G. Ledyard Stebbins, April 4, 1988 ABSTRACT One of the principles that has emerged from genetic variation available for evolutionary changes (2), a experimental evolutionary studies of microorganisms is that major concern of modem evolutionists is explaining how the polymorphic alleles or new mutations can sometimes possess a vast amount of genetic variation that actually exists can be latent potential to respond to selection in different environ- maintained. Given the fact that in complex higher organisms ments, although the alleles may be functionally equivalent or most new mutations with visible effects on phenotype are disfavored under typical conditions. We suggest that such deleterious, many biologists, particularly Kimura (3), have responses to selection in microorganisms serve as experimental sought to solve the problem by proposing that much genetic models of evolutionary advances that occur over much longer variation is selectively neutral or nearly so, at least at the periods of time in higher organisms. We propose as a general molecular level. Amidst a background of what may be largely evolutionary principle that anagenic advances often come from neutral or nearly neutral genetic variation, adaptive evolution capitalizing on preexisting latent selection potentials in the nevertheless occurs. While much of natural selection at the presence of novel ecological opportunity. molecular level must involve minor improvements in fitness, major adaptive advances in the complexity oforganisms-for One of the research strategies that has been most useful in example, the origin of aerobic respiration; of the sexual generating progress in molecular biology is based on the cycle; of multicellularity; ofjaws, teeth, and limbs of verte- notion that simple model systems illustrate mechanisms and brates, etc.-must ultimately emanate from the molecular principles that are found to be generally applicable. This level through genes that provide new functions and that strategy has been particularly successful in the study of the regulate and integrate these functions. molecular genetics of bacteria and bacterial viruses. As the The challenge ofunderstanding morphological evolution at field of evolutionary genetics becomes increasingly molecu- the molecular level cannot be met straightaway with attempts lar, a similar strategy is also becoming productive in this area to analyze major shifts that occur in complex multicellular (1). Microbial organisms may prove to be useful as model organisms, because of the presently inadequate understand- systems in studies of population and evolutionary biology. ing of the relevant molecular principles of development. An In point of fact, a good deal of evolutionary work with alternative place to start is via analysis of adaptive reactions microbial organisms has already been carried out, and the in microorganisms, in which the relationship between mo- results are only just beginning to be integrated into evolu- lecular change and adaptation to the environment is often tionary thinking. The present paper attempts to add to this relatively direct. Microorganisms have additional practical synthesis by showing that certain evolutionary principles that advantages for this purpose. Populations of 1010 or greater have emerged from microbial experiments can be applied as can be studied in chemostats or Petri dishes in experiments paradigms to higher levels ofthe evolutionary hierarchy. The lasting only a few days or weeks, and progressive genetic following sections provide the background of the principles changes can be followed for hundreds of generations. The and examples of their application to complex evolving sys- success of such experiments in analyzing the genetic and tems, including both microevolution and macroevolution. molecular basis of adaptive shifts is well documented (4-7). Current evolutionary biology continues to debate whether Given the demonstration that adaptive shifts can be ana- major adaptive shifts and anagenetic advances in evolution lyzed in microorganisms, can the results be extrapolated to result from one or two macromutations that bring about the help explain the much more complex situation in multicellular changes relatively suddenly or from the slow accumulation of highly differentiated organisms? We believe that it can, for many small differences gradually acquired during millions of the following reasons: years. We believe that the classification of evolutionary (i) Chemostat experiments with unicellular lower eukary- advance based on the number of favorable mutations is arbi- otes, such as yeast, suggest that adaptations to different trary and artificial. Rather, the arguments that follow lead us to environments involve molecular mechanisms and principles believe that evolutionary advances result from occasions in similar to those observed in prokaryotes (8-10). which populations fortuitously exposed to various selection (ii) Comparisons among unicellular lower eukaryotes that pressures are coincidentally able to respond to them-no matter differ greatly in size and in methods of nutrition reveal a whether the genetic basis ofthe response resides in one or a few wealth of intermediate situations in which the origin of such lucky mutations or a larger number gradually accumulated. major advances as ingestion of food particles, filter feeding, gametic conjugation, etc., may be analyzed at the molecular Background level (see reviews in ref. 11). (iii) Major adaptive shifts in higher organisms consist of a During the past 25 years, knowledge ofthe nature and extent complex sequence of genetic and morphological alterations, ofgenetic variation has increased dramatically. While in 1960 the individual elements of which may be analogous to many geneticists were concerned with the seeming paucity of metabolic shifts in simpler organisms. For instance, trophic shifts in a vertebrate animal, such as from filter or suspension feeding to the ingestion of larger organisms, entail several The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact. tTo whom reprint requests should be addressed. 5141 Downloaded by guest on September 26, 2021 5142 Evolution: Stebbins and HartPProc. Natl. Acad. Sci. USA 85 (1988) biochemical events of breakdown and digestion that may be enzyme kinetics (whence the term), in which many reactions comparable to metabolic shifts in bacteria, plus alterations in exhibit a hyperbolic relationship between the activity of a external morphology. Because understanding any series of particular enzyme in a metabolic pathway and metabolic flux biological processes, including evolution, requires that re- through the pathway. At low activities, the flux increases ductional analyses precede final syntheses, reductional anal- almost linearly with enzyme activity, but at higher activities ysis of adaptive shifts may be made more precise by analogy the system becomes saturated and the relationship between with results of experiments on simpler organisms. flux and activity becomes almost flat. (iv) In many instances, the evolutionary consequences of Organizational constraints result from physical structures adaptive shifts lie not in their degree of complexity, but in the or the manner in which they are organized. For example, one ecologic or phylogenetic context in which they occur. For of the cardinal discoveries of molecular evolution is that example, the evolutionary progression from a flying bird that different structural domains of the same protein molecule nests on solid ground on an island to a swimming penguin that often evolve at different rates. Domains requiring precise hatches its eggs and raises its young on glacial ice was fully physical interactions with other molecules, such as the active as profound and complex as the evolution of a primitive and binding sites of enzymes, or that associate with ligands labyrinthodont amphibian from a rhipidistian fish. Yet, the such as heme, are often constrained so that their rate of penguin has never been and probably will never be the evolution is slower than that of other domains with less ancestor of an evolutionary lineage, because the sparse stringent requirements for interaction. niches of its antarctic marine habitat are already filled, while the labyrinthodont was in the fortunate position of pioneering Types of Constraints in a terrestrial habitat that offered a wealth of vacant niches to receive its evolving descendants. Similarly, the shift in Saturational constraints resulting from diminishing-return modern genera of flowering plants from insect to bird effects have been observed at many levels of biological pollination may seem trivial to nonbotanists, because the organization. The following sections outline examples rang- effects are relatively slight with reference to most floras. Yet, ing from the molecular level to that of the whole organism. from the genetic and morphological point of view, the various As noted, many biochemical pathways

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