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Major problems in evolutionary transitions: how a metabolic perspective can enrich our understanding of macroevolution

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Abstract

The model of major transitions in evolution (MTE) devised by Maynard Smith and Szathmáry has exerted tremendous influence over evolutionary theorists. Although MTE has been criticized for inconsistently combining different types of event, its ongoing appeal lies in depicting hierarchical increases in complexity by means of evolutionary transitions in individuality (ETIs). In this paper, we consider the implications of major evolutionary events overlooked by MTE and its ETI-oriented successors, specifically the biological oxygenation of Earth, and the acquisitions of mitochondria and plastids. By reflecting on these missed events, we reveal a central philosophical disagreement over the explanatory goals of major transitions theory that has yet to be made explicit in the literature. We go on to argue that this philosophical disagreement is only reinforced by Szathmáry’s recent revisions of MTE in the form of MTE 2.0. This finding motivates us to propose an alternative explanatory strategy: specifically, an interactionist metabolic perspective on major transitions. A metabolic framework not only avoids many of the criticisms that beset classic and revised MTE models, but also accommodates missing events and provides crucial explanatory components for standard major transitions. Although we do not provide a full-blown alternative theory and do not claim to achieve unity, we explain why foregrounding metabolism is crucial for any attempt to capture the major turning points in evolution, and why it does not lead to unmanageable pluralism.

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Notes

  1. We agree with one of our referees that much evolution, especially but not only at the molecular and biochemical level, is non-adaptive. However, given the selectionist cast of MTE, our current paper will address only selection-driven aspects of major turning points.

  2. In addition, although MTE treated its core concepts—such as genetic information, individuality and hierarchy—as unproblematic, subsequent philosophical analyses have raised significant complications with them.

  3. However, see Sigmund and Szathmáry (1998: 439) for what appears to be an endorsement of ‘“progress”…as a series of major transitions in evolution’; note also that MTE 2.0 still culminates in human language and society.

  4. When Maynard Smith and Szathmáry visualize the differences between prokaryotes and eukaryotes, they deliberately omit the mitochondria (and other acquired organelles) because ‘on the scenario that seems to us most plausible, these intracellular structures originated later in time than the [other distinctively eukaryotic] structures’ (1997: 122). See our discussion below of Szathmáry’s (2015) recent thoughts on this topic.

  5. For details of these competing hypotheses of eukaryote origins, see O’Malley (2010).

  6. Secondary and tertiary endosymbioses are events in which green and red algae acquire a second or even a third photosynthesizing organism (another alga) in addition to the one they already had, or after losing their original plastid (Fig. 3).

  7. Plastid endosymbioses are still occurring, with a new primary plastid acquisition well underway in Paulinella chromatophora (Fig. 3).

  8. Knoll and Bambach (2000) also propose an ‘expanding ecospace’ model that articulates a greater role for ecological transformations in major transitions, but their model mostly maps onto the classic MTE, culminating in ‘technological intelligence’ and thus similarly encouraging ascent interpretations.

  9. In bacterial biofilms and other collectives, the fruits of metabolic innovation can be exploited by surrounding cells (Benomar et al. 2015). These interactions, often of benefit to multiple species, provide the impetus for cooperative strategies designed to ensure that metabolic benefits are confined to biochemical co-operators. In cases where cooperation is intraclonal (Drescher et al. 2014), kin selection and metabolism offer complementary aspects of a unified ultimate explanation of cooperation. Metabolism is especially good for explaining how free-riding can be overcome in biological collectives (a focus of MTE), including multilineage consortia (Hillesland and Stahl 2010).

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Acknowledgments

The authors would like to thank Robert Brandon, Adrian Currie, Catherine Driscoll, Marc Ereshefsky, Doug Erwin, Peter Godfrey-Smith, Dan McShea, Kepa Ruiz-Mirazo, Nicholas Shea, members of the Duke University Philosophy of Biology reading group and Dalhousie’s Evolution Studies Group, audiences at the American Philosophical Association, Australasian Association of Philosophy, AAPNZ, and SANU Philosophy of Biology meetings, and two anonymous referees for comments on earlier versions of this manuscript. Maureen O’Malley acknowledges funding from the University of Sydney’s Bridging Support scheme; Russell Powell is grateful to Templeton Foundation Grant # 43160 for support of this research.

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    1. Department of Philosophy, University of Sydney, Sydney, Australia

      Maureen A. O’Malley

    2. Department of Philosophy, Boston University, Boston, MA, USA

      Russell Powell

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    1. Maureen A. O’Malley
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    Correspondence to Maureen A. O’Malley or Russell Powell.

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    O’Malley, M.A., Powell, R. Major problems in evolutionary transitions: how a metabolic perspective can enrich our understanding of macroevolution. Biol Philos 31, 159–189 (2016). https://doi.org/10.1007/s10539-015-9513-z

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