Ecological Facilitation May Drive Major Evolutionary Transitions
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University of Montana ScholarWorks at University of Montana Biological Sciences Faculty Publications Biological Sciences 5-2009 Ecological Facilitation May Drive Major Evolutionary Transitions Zaal Kikvidze Ragan M. Callaway University of Montana - Missoula, [email protected] Follow this and additional works at: https://scholarworks.umt.edu/biosci_pubs Part of the Biology Commons Let us know how access to this document benefits ou.y Recommended Citation Kikvidze, Zaal and Callaway, Ragan M., "Ecological Facilitation May Drive Major Evolutionary Transitions" (2009). Biological Sciences Faculty Publications. 93. https://scholarworks.umt.edu/biosci_pubs/93 This Article is brought to you for free and open access by the Biological Sciences at ScholarWorks at University of Montana. It has been accepted for inclusion in Biological Sciences Faculty Publications by an authorized administrator of ScholarWorks at University of Montana. For more information, please contact [email protected]. Articles Ecological Facilitation May Drive Major Evolutionary Transitions ZAAL KIKVIDZE AND RAGAN M. CALLAWAY There is a growing consensus among ecologists that ecological facilitation comprises a historically overlooked but crucial suite of biotic interactions. Awareness of such positive interactions has recently led to substantial modifications in ecological theory. In this article we suggest how facilitation may be included in evolutionary theory. Natural selection based on competition provides a conceptually complete paradigm for speciation, but not for major evolutionary transitions—the emergence of new and more complex biological structures such as cells, organisms, and eusocial populations. We find that the successful theories developed to solve these specific problematic transitions show a consistent pattern: they focus on positive interactions. We argue that facilitation between individuals at different levels of biological organization can act as a cohesive force that generates a new level of organization with higher complexity and thus allows for major evolutionary transitions at all levels of biological hierarchy. Keywords: positive biotic interactions, biological hierarchy, biological complexity, speciation, evolutionary theory cology and evolutionary biology are two closely models that include direct and indirect species interactions Erelated disciplines, yet their theoretical directions do in ecological communities predict that positive interactions not always overlap. Therefore, an effort to synthesize the are as probable and as important as negative interactions theoretical directions developing within these disciplines (Callaway 2007). has the potential to provide crucial insight into biology’s Evolutionary theory has also explicitly based the origins of challenging issues. Because biotic interactions are the foun- new lineages on negative biotic interactions, since the elim- dation for many important ecological and evolutionary ination of less fit individuals is very often the negative effect concepts, including speciation, extinction, niche theory, and of one organism on another. But as in ecology, this focus has geographical distributions, they provide important inter - been criticized for the neglect of positive interactions as im- disciplinary common ground. While ecologists studied the portant drivers of evolution (Kutschera and Niklas 2004). The mechanisms of biotic interactions, evolutionists explored core of this criticism has been that novel biological structures their genetic consequences. Here we suggest that recent eco- cannot emerge unless functional links and cooperation, logical advances on understanding how species interact have essentially positive interactions, occur among the compo- important implications for evolutionary theory. nents of a system. For example, the theory of natural selec- Ecological studies of biotic interactions have a long history, tion on phenotypes resulting exclusively from mutations yet until recently, theories on coexistence, diversity-ecosystem does not satisfactorily explain the rapid and important evo- function, meta-population dynamics, the niche, and the fun- lutionary transitions necessary to produce eukaryotic cells damental nature of communities have focused on negative in- (Ryan 2002). Thus, most biologists now accept the en- teractions such as competition and predation, whereas positive dosymbiotic hypothesis, which explicitly bases the origins of interactions were considered to be interesting but idiosyncratic eukaryotic cells on positive interactions (Margulis et al. 2000, (Callaway 1997, Stachowicz 2001). Only since the 1990s has Kooijman et al. 2003). compelling evidence accrued for facilitation—that is, species In fact, ecology’s relatively recent shift in focus regarding interactions that are mutually beneficial—as a ubiquitous biotic interactions in ecology has a parallel in evolutionary bi- and important component of the suite of biotic interactions ol ogy. In their book The Major Transitions in Evolution, John that determine fundamental ecological theory (Callaway Maynard Smith and Eörs Szathmáry (1997) demonstrate 1998, 2007, Bruno et al. 2003, Brooker et al. 2008). Current how the problems that have proved difficult for mainstream BioScience 59: 399–404. ISSN 0006-3568, electronic ISSN 1525-3244. © 2009 by American Institute of Biological Sciences. All rights reserved. Request permission to photocopy or reproduce article content at the University of California Press’s Rights and Permissions Web site at www.ucpressjournals.com/ reprintinfo.asp. doi:10.1525/bio.2009.59.5.7 www.biosciencemag.org May 2009 / Vol. 59 No. 5 • BioScience 399 Articles evolutionary theory have been tackled by invoking new hy- hierarchy of life. Here we assess the potential of positive in- potheses that shift the focus from negative to positive inter- ter actions to provide conceptual generality for major evolu- actions (also see Queller 1997). Maynard Smith and Szathmáry tionary transitions by discussing the importance of facilitation analyzed the strengths and weaknesses of evolutionary the- in the context of specific theories. ory and argued that when evolution is presented as a series of major evolutionary transitions from less complex to more Overview of specific theories on major complex biological forms (eukaryotic cells are more complex evolutionary transitions than prokaryotic cells, animals and plants are more com- The sequence of major evolutionary transitions, the most suc- plex than protists, and so on), the theory of natural selection cessful specific theories explaining these transitions, and the needs substantial modifications to predict or explain the ecological interactions hypothesized to drive them are sum- emergence of new and more complex biological structures. marized in figure 1. Below we comment briefly on each of This problem becomes more evident if we superimpose these transitions, from subcellular structures to socially or- evolutionary theory onto another general biological ganized populations. As this overview includes a broad range concept—the hierarchy of biological organization (figure 1, of biological hypotheses, we have presented them in a basic left panel). The hierarchical presentation of biological orga- format that emphasizes fundamental underlying biotic inter - nization is heuristically useful because it portrays the com- actions and, for brevity’s sake, leaves out other important plexity of all biological forms precisely and succinctly (McShea details. 2001).The general hierarchical pattern is “nestedness”: higher levels of biological organization include lower levels (organ- Precellular evolution to simple cells. Precellular evolution includes isms include cells, cells include organelles, and so on). The at least two major evolutionary transitions: (1) from bio- major transitions refer precisely to these passages from one molecules to supermolecular aggregations such as chromo- level of biological organization to another (figure 1, yellow somes and ribosomes, and (2) from supermolecular arrows). A competition-based view of natural selection suc- aggregations to prokaryotic cells. No fossils were left by pre- cessfully explains emergence of biological diversity within cellular transitions, and research relies mainly on the physics levels, especially at the levels of cells and organisms, but a com- and chemistry of biomolecules, reconstructions of metabolic petition-based approach fails to satisfactorily explain the pathways for different evolutionary lineages, and theoretical major transitions from lower to upper levels—and this modeling. The many hypotheses these studies produced are pattern of nestedness, which portrays some of the most reviewed and discussed elsewhere (e.g., Knoll 2004, Martin and fundamental evolutionary changes in life. Russell 2007), but to date the leading theory is the “RNA- The problem, as Maynard Smith and Szathmáry (1997) ex- world” (Alberts et al. 2002). This hypothesis is based on the plained, is that natural selection based on negative interactions ability of RNA molecules (ribozymes) not only to self-repli- predicts competition between entities at the lower level (repli- cate but also to catalyze necessary chemical reactions. Al- cating molecules, free-living prokaryotes, single cells, individual though a complete chemical reconstruction of self-replicating organisms), which disrupts their ability to integrate into ribozymes is still to be achieved, the current hypothesis is con- higher levels (chromosomes,