3 r- and K-Selection and Microbial Ecology JOHN H. ANDREWS and ROBIN F. HARRIS 1. Introduction The essence of the concept of r- and K-selection is that organisms strive to maximize their fitness for survival in either uncrowded (r-selection) or crowded (K-selection) environments. Fitness is defined following ecolog­ ical convention as the proportion of genes left in the population gene pool (Pianka, 1983, p. 10). The terms rand K refer, respectively, to the max­ imum specific rate of increase (maximum specific growth rate minus min­ imum specific death rate) of an organism and to the density of individ­ uals that a given environment can support at the population equilibrium. Since both r and K can vary within a species and are subject to modifi­ cation, the division of natural selection into r- and K-selection is of con­ siderable basic interest in evolutionary ecology. In this chapter we review and attempt to interpret in a microbial con­ text the basis for r- and K-selection. We stress key contributions to the concept, rather than present an exhaustive historical chronology. Details regarding the terminology and mathematical derivations. are given in an Appendix (see Section 7), so that they are accessible without disrupting the text. (A list of symbols and abbreviations is also appended in Section 7.4.) A conspicuous shortcoming of ecological concepts is that mechan­ istic explanations are typically lacking. A mechanistic interpretation is JOHN H. ANDREWS • Department of Plant Pathology, University of Wisconsin, Madison, Wisconsin 53706. ROBIN F. HARRIS • Departments of Soil Science and Bacteriology, University of Wisconsin, Madison, Wisconsin 53706. 99 K. C. Marshall (ed.), Advances in Microbial Ecology © Springer Science+Business Media New York 1986 100 J. H. Andrews and R. F. Harris emphasized to clarify the idea and to provide focal points for testing hypotheses. An overview of the topic, together with our analysis and oth­ ers that have been or might be used, appears in the flowsheet in Fig. I. 2. The Concept of r- and K-Selection 2.1. The Postulate We explore the notion of r- and K-selection as a postulate (Fig. 1); i.e., a hypothesis posed as an essential premise for a chain of reasoning. r-and K-traits and their associated environments seem to be significant factors to consider in population biology; however, we do not know how valid the postulate is-our approach is not an attempt to establish pri­ macy, but rather to present the postulate and evaluate the evidence for it. The premise advanced concerns the tradeoff between fitness in crowded versus uncrowded environments. Thus, according to the pos­ tulate, organisms face a suite of "either-or" r/ K-related choices such as: high rate of acquisition of nutrients or high affinity for nutrients; high stress resistance of spores or high sensitivity of spores to stimulation; doing one thing well ("specialists") or many things indifferently ("generalists"). A critical analysis of the concept requires that something be known about what constitutes "crowding" and about the nature of the environ­ ments concerned. The major differences affecting fitness between uncrowded and crowded environments are summarized in Table I. These criteria set the stage for comparisons of life history strategies among organisms in the two environments. However, such comparisons can best be made only for species occupying the same trophic level, because whether a species is limited by resources or some other mechanism (e.g., predation) is related to its trophic position (Wilbur et al., 1974). Put briefly, uncrowded environments provide for "r-conditions": population densities are low, and density-dependent growth factors are negligible. Population regulation is typically mainly through density-independent mechanisms (e.g., sporadic storms, desiccation, or temperature extremes), which affect essentially the same proportion of individuals at all densities. Conversely, crowded environments provide for "K-condi­ tions": population densities are high and populations are limited by den­ sity-dependent controls, such as food supply, toxic metabolites, or pre­ dation, which cause proportionate (per capita) changes in birth or death as population density changes. Hence, crowding implies more than just competition for food or space. This broader interpretation is noteworthy and is often overlooked (e.g., Parry, 1981). rjK Postulate: 'i' POSTULATE Organisms compromise between ll) maximized genotypic fitness in basis of postulate c.= uncrowded versus crowded ~ environments; Section 2.1 00 ~ nII> ::t. theoretical proof empirical evidence =0 f 1 ~ Genetic/physiological Phenotypic EVIDENCE constraints on a= correlates Ef "master of all trades"; I mechanistic basis •I Micro- Macro- Section 2.2 • I organisms; organisms; S: Section 2.3.2 Section 2.3.1 e:. tr.! e. mechanistic mechanistic basis basis ~ mechanistic basis Phenotypic determinants Phenotypic determinants EXPLANATION are potentially are components of determinable components logistic equation of mechanistic intercepts; Section 3 and equations; Section 3 Appendix genetic engineering IMPLICATION Implications for '---------------1--l microbial ecology; Sections 4 and 5 Figure 1. r- and K-selection: An overview of the organization of this chapter; a synopsis of evidence for and ex pial­ .::>""" nations of the concept; and its implications for microbial ecology. """ 102 J. H. Andrews and R. F. Harris Table I. Some Key Attributes of Crowded versus Uncrowded Environments Which Affect Fitness Effect on potential growth inhibition or death Potential death acceleration acceleration due to Population Per capita Inadequate Toxic predation or Environment density food supply food metabolites parasitism Uncrowded Low High Low Low Low Crowded High Low High High High Uncrowded environments are typically unpredictable and transitory. Species colonizing such habitats will do best if they have a high r (in effect, in microbiological terms, a high P.max; Table II), which promotes discovery of habitat ~ reproduction ~ dissemination before a saturated condition (K-selection) or loss of the habitat occurs. On the other hand, organisms that compete well in terms of seizing and retaining a particular habitat and efficiently extracting energy from it will be favored under crowded conditions. Genotypes with a high r will be selectively favored in the former situation; those with a high K, in the latter. The ecological dogma is that a high r occurs at the expense of a low K, or a relatively low r is the sacrifice for a high K (e.g., Wilson and Bos­ sert, 1971, pp. 111-112; Roughgarden, 1971). Apparently, organisms can­ not thrive under both conditions; i.e., they cannot maximize both param­ eters. This does not mean that the two forms of selection are mutually exclusive. Both r and K are subject to evolutionary adjustment upward or downward; the relative degree of the corresponding selective pressure is determined largely by environmental stability (MacArthur and Wilson, 1967). Put another way, with the focus on the environment rather than the organism, environments can be characterized on an rjK basis, deter­ mined by the extent and periodicity of transient r- and K-conditions pre­ vailing over time. Any environment is thus an integrator of the instanta­ neous conditions of which it is comprised. We define an r-condition to be when the environment/population relationship (defined quantitatively later) is such that members of the population in question grow at their maximum specific rate of increase r. An r-condition may arise temporar­ ily because of an increase in the food supply andjor a catastrophic decline in the population density. A K-environmental condition exists when the environment/population relationship is such that the specific rate of increase of the population is close to or at zero and the population density is correspondingly close to or at the carrying capacity K. In oligotrophic r- and K-Selection and Microbial Ecology 103 waters, for example, this state commonly exists because the inherently low rate of food supply favors fixation of the per capita rate of food sup­ ply in the maintenance rather than the growth-supporting range. Hence, in theory, an r/K environmental continuum can be visualized, delimited at the rend by an exclusively r-environment in which r-conditions exist continuously, and at the K end by an exclusively K-environment in which extreme K-conditions exist continuously. In practice, most natural microbial environments will show characteristic oscillations between extreme r- and extreme K-conditions, the relative frequency and extent of which will dictate the location of the environment along the rjK con­ tinuum and the related pressure for microbial fitness. Although the role of environmental stability in r- and K-selection is a recurrent theme implicit in much of the literature, we explicitly emphasize its importance and focus on it in this review. In predictably extreme (harsh) environments, such as hydrothermal vents, the arctic, hot springs, deserts, or the highly saline conditions of the Salton Sea, adaptations to the physical environment could be prom­ inent. Greenslade ( 1983) proposed a habitat template partitioned into areas dominated by three selection processes: r-selection, where habitat predictability is low; K-selection, where the habitat is favorable and its predictability is high; and A-selection in unfavorable habitats, particu­ larly those that are predictably unfavorable. However, we believe and explain later that, in