On the Comparative Ecology of Microorganisms and Macroorganisms

To conclude, we return to the contention (see Preface) that the ecology of macroorganisms is essentially phenomena in search of mechanistic explanation, whereas microbial ecology is experimentation in search of theory. Slobodkin (1988, p. 338) has commented that “ecology may be the most intractable legitimate science ever developed”. Despite the rich theoretical base of plant and animal ecology, few clear generalizations or specific predictions applicable to reality emerge that are other than trivial, and many of the precepts are contentious. Macroorganism ecology remains a field constrained by correlation. This is not surprising, given the complexity of higher organisms and their habitats, the interactions among traits, and the consequent difficulty of explaining phenomena mechanistically.

The consequence is that controlled experiments frequently are difficult, if not impossible, and conclusions are often not robust (for criticism of ecological experimentation see Hairston 1990; however, for a good example of how critical field experimentation in macroecology is possible, see Daan et al. 1990 on optimal clutch size in birds; for a good discussion of the utility and limits of different types of experiment, see Diamond 1986). Long-running debates on such topics as niche theory; resource generalists versus specialists; adaptive radiation; and the role of contingency in evolution over either contemporary or geological time, are but a few conspicuous examples.

Microbial ecologists, meanwhile, have focused historically on autecological studies of selected species generally under laboratory conditions. Increasingly, such entities are known only by their nucleotide sequences, from which a phenotype is inferred. Broadly speaking, while microbial systems exist that could be used to answer rigorously many ecological questions that cannot be addressed mechanistically by plant and animal studies, they still remain comparatively unexploited. Conversely, the principles and concepts of macroecology, which could serve to guide and underpin microbial ecology, remain generally unintegrated as a body of work. There have been some rare, shining exceptions, such as the insightful approach of Alexander (1971) about 50 years ago in his classic text on microbial ecology whose foundation was ecological theory. Nevertheless, the still common academic practice of sequestering microbiologists in departments unto themselves (and of placing plant and animal ecologists in botany and zoology departments, respectively), and of structuring curricula accordingly, have promoted isolationism. The upshot is that the artificial distinction between microorganism and macroorganism is amplified, different concepts of what ecology supposedly is have emerged, and different vocabularies exist to describe fundamentally the same phenomena.

This is but one manifestation of the march to specialization in science, a broader point addressed eloquently by Greene (1997). Finally, the gulf between microbial and plant and animal ecology has been widened by the historical difference in methodological approach, alluded to in the Preface and Chap. 1. The new, ever-expanding world of genomics (and numerous related .. omics”) and molecular systematics offer powerful, potentially revolutionary insights into the evolution of organism function and design. Examples include ‘soil metagenomics’, now some decades old and, of much more recent origin, the so-called ‘phy- tobiome’ and the ‘gut microbiome’. Despite some sanguine progress reports (Stearns and Magwene 2003), whether these novel subdisciplines serve to really bridge the gulf or merely extend reductionist thinking further into the macroorganism world, remains to be seen.

What does experimentation with microorganisms hold of conceptual value for the ecology of macroorganisms? How might such studies inform the discipline of ecology as a whole? One answer is that by virtue of being more amenable as research subjects, microbes provide excellent models to test ecological theory. There is a direct parallel here between such ecological exploration with the use by geneticists since the 1960s of microbial research models such as E. coli, Saccharomyces cerevisiae, Neurospora, and Caenorhabditis to answer fundamental questions in physiology and genetics applicable to macroorganisms. Though hardly free from their own limitations and artifacts, the numerous attributes of microbes and their potential utility as research models were alluded to in Chap. 1: easy clonal propagation of effectively a single genotype; fast generation times; capability for prolonged storage under conditions of suspended animation; high degree of control over environmental conditions.

Several examples of the insightful application of microbes to test ecological theory are noteworthy: Microbes have been used to address optimality concepts (e.g., the metabolic burden or maintenance costs associated with ‘excess’ gene functions can be tested with prototrophic and auxotrophic forms—see Chap. 3 and Zamenhof and Eichhorn 1967). Also as recounted in Chap. 3, Dykhuizen and colleagues have used bacterial systems to effectively address major ecological topics such as metabolic constraints, competition, and the evolution of specialism versus generalism in resource use (e.g., Dykhuizen 2016). In research extending over several decades, Graham Bell and colleagues at McGill University have focused on relatively simple model organisms in controlled culture, principally the unicellular alga Chlamydomonas, bacteria, and domestic and wild species of the yeast Saccharomyces (e.g., Replansky et al. 2008) to address fundamental ecological issues such as adaptive diversification, ‘evolutionary rescue’, historical contingency, the fitness of long-term sexual and asexual populations, and trade-offs.

Paul Rainey and colleagues in New Zealand have used bacteria to examine numerous aspects of evolutionary processes, among them the role of environmental heterogeneity in adaptive radiation (Rainey and Travisano 1998), niche theory, and the origins of individuality and multicellularity. Interestingly, the same forces (environmental heterogeneity) driving Rainey’s static bacterial culture to diverge genetically and ultimately morphologically are driving morphological divergence in sticklebacks that inhabit different environments (limnetic vs. benthic) in the same lake (Rundle et al. 2000). Richard Lenski and collaborators at Michigan State University, in a mammoth experiment begun in 1988 and ongoing, are studying fitness and evolutionary processes as revealed under controlled conditions in E. coli. Samples are taken every 500 generations from 12 clonal populations originating from a common ancestor, frozen, and compared through time. As of 2013 the subpopulations had been evolving for >50,000 generations.

Among the Lenski group’s many fascinating insights over the long course of this work is that average fitness continues to increase (and is projected to continue to do so by their model), although apparently at a decelerating rate (e.g., Wiser et al. 2013). Most of the 12 cultures behaved similarly in this regard, suggesting that evolution, at least among clonal populations in standard conditions, is broadly reproducible. Nevertheless, with respect to some key traits, historical contingency may be critical, a conclusion made elegantly by virtue of the power of their sequential sampling regimen that allows retrospective examination of population change through time in each line; e.g., Blount et al. 2008). Lenski’s former student, Brendan Bohannan, currently at the University of Oregon, has been at the forefront of applying ecological theory to microbial ecology in many contexts (e.g., see Costello et al. 2012 and Horner-Devine et al. 2004), below. Aspects of our own work in ecological theory and microbes began in the early 1980s and have been noted in various chapters in this book (see example below on island biogeography).

Two areas of major convergence between microbial and plant and animal ecology are biogeography, and community ecology and community assembly, which have received significantly increased attention in the past two decades (Horner-Devine et al. 2004; Martiny et al. 2006; Vellend 2010; Costello et al. 2012; Nemergut et al. 2013).

The stages, forces, and processes involved appear to be closely analogous for both microorganisms and macroorganisms despite some obvious differences in attributes such as dispersal, dormancy, and plasticity discussed in earlier chapters. Indeed, even within the microbial world, there are likely differences in the specific colonization dynamics between bacteria and fungi (Schmidt et al. 2014). Notwithstanding such idiosyncrasies, the simplicity and experimental tractability of microbial systems have and will continue to provide an instructive model for the experimental complexities of the macroorganism counterpart. Aspects of the colonization (invasion) process, particularly when a new habitat patch occurs, appear to be especially analogous (e.g., Gjerde et al. 2012; Tan et al. 2015). Notwithstanding close theoretical as well as practical similarities between the subdisciplines of invasion biology in ecology and biological control in plant pathology, there has been to date minimal crossover of literature or cross-fertilization of researchers and research ideas. This is ironic and regrettable.

As early as 1967, Ruth Patrick at the Academy of Natural Sciences in Philadelphia used the conceptual framework established in various indices of diversity, Preston’s models of commonality, and MacArthur and Wilson’s theory of island biogeography (1967), all developed for macroorganisms, to rigorously test area relationships and colonization dynamics of diatoms on glass slides immersed in flowing water from a spring or streams of different characteristics (e.g., species source pool size). Some of her experiments varied the invasion rate by controlling the flow rate of the water, and the size of the ‘island’ (slide). Her work not only established the importance of all three factors in the number of species and diversity of a community but highlighted the role of invasion rate in maintaining relatively rare species in a community and the implications of crowding to local extinction of those species represented by very small populations. Tom Brock and his students at Madison, Wisconsin, extended Patrick’s work with studies on the population biology of aquatic bacteria (reviewed in Brock 1971).

They ingeniously differentiated immigration from growth processes by pulsing the evolving population at short intervals by UV irradiation. Some years later, we implemented a conceptually similar disinfestation approach to test island biogeography and community assembly precepts with respect to microbial colonization of leaf surfaces. The microbes were filamentous fungi and wild yeasts, and the leaf islands were those of apple trees under manipulated (leaves initially effectively sterile; Kinkel et al. 1987; 1989a, b) or unmanipulated, orchard conditions, where species and population dynamics were followed from the incipient stage of bud break in the spring (surfaces relatively uncolonized) to leaf senescence and abscission in the fall (surfaces extensively colonized) (Andrews et al. 1987).

Another advantage of microbes in evolutionary ecology is they are unique in offering a relatively close, direct linkage between genotype and phenotype. Their developmental and structural simplicity means that the problems of pleiotropy and epigenetic effects (the so- called ‘gene net’ of Bonner 1988, pp. 144 and 174-175; or ‘informational relay’ of Stebbins 1968), though real, are comparatively small relative to those of macroorganisms. For instance, imagine that we are interested in whether a particular phenotypic trait is responsible for the competitive dominance of species A over species B in a community. To take a practical example from plant pathology, suppose further that organism A is seen to inhibit B in an agar plate assay, ostensibly by production of an antibiotic. We might notice also that under field conditions, application of populations of A also controls a disease incited by B. At this observational level there is merely a correlation between antibiotic production and competitive suppression, just as among macro organisms there may be a correlation between, say, body size and spatial location of species along a resource gradient. In the latter case, interspecific competition has often (and occasionally erroneously) been inferred as the responsible mechanism (see examples cited by Roth 1981; Connell 1983; Price 1984; Eadie et al. 1987).

The cause for such an observed pattern typically can be determined directly and often at the level of the gene in microorganisms, however, in a way that it cannot for the macro organism analog. First, the antibiotic from A could be purified, tested for an effect on B, and demonstrated to be present at inhibitory levels at the field microsites where antagonist A and pathogen B interact. Second, two complementary mutational analyses could be performed to implicate antibiosis as the mechanism. Mutants of A lacking inhibitory activity to B should not produce the antibiotic and should fail to prevent disease development. Complementation of the mutants to restore antibiotic production should also restore competitive dominance and disease suppressing ability. Second, mutants of the pathogen B could be made and tested in the same manner as those of antagonist A. B mutants insensitive to the antibiotic should cause disease in the presence of A; restoration of sensitivity should coincide with failure to cause disease. Finally, any remaining remote possibility of a correlative rather than a causal relationship between antibiotic production and biocontrol activity can be effectively eliminated by examining many mutants (for examples, see Hirano et al. 1997; Raaijmakers and Mazzola 2012).

The degree to which studies in microbial ecology will prove to be of heuristic value in macroecology, and vice versa, remains to be seen. But, clearly there are precedents and the prospects are encouraging. The fundamental commonalities as well as the practical examples reviewed in this book mark the progress of multiple research groups and provide many intriguing points of departure for further research. Nevertheless, it is evident that there will always be examples (and always a level) of comparison that just ‘don’t fit’. Nature displays an astounding richness of expression, but is surprisingly conservative in underlying pattern. Adopting a broad conceptual perspective in our individual studies is enlightening and intellectually gratifying.