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The Evolution of Ecosystem Phenotypes

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Abstract

Evolution by natural selection (ENS) has been extended to several supraorganismic levels, but whether it can apply to ecosystems remains controversial on two main counts. First, local ecosystems are loosely individuated, so that it is unclear how they manifest heredity and fitness. Second, even if they did, the meta-ecosystem formed by this population of local ecosystems will also suffer from a very low degree of cohesion, which will jeopardize any ENS. We suggest a way to overcome both issues, focusing on ecosystem properties (or phenotypes) rather than on ecosystemic individuals. First, we follow recent theoretical developments which deny the centrality of reproduction in ENS. This leads us to merge heredity and fitness in a single process, in which a local ecosystem (the unit of selection) causally influences its neighbors, in a way responsible for their phenotypic similarity. Second, we suggest that the resulting meta-ecosystem (the unit of evolution) need not meet the criteria of individuality (sensu Ghiselin–Hull). Instead, the evolving meta-ecosystem is best understood as a homeostatic property cluster, i.e., a set of phenotypes that together evolve by ENS at the ecosystem level. We illustrate this conceptual framework with a hypothetical example of local ecosystems that vary in terms of stability, productivity, diversity, and complementarity between species. Finally, we stress that our property-based account of ecosystemic ENS can help understand evolution at other biological levels, such as early life evolution and holobionts.

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Notes

  1. Ecosystems are communities (a biotic compartment) embedded in an abiotic compartment. Depending on the literature cited, either communities or ecosystems are considered as putative levels of selection. We will prefer the use of “ecosystems,” because it is more inclusive.

  2. Defined as “a set of ecosystems connected by spatial flows of energy, materials, and organisms” (Loreau et al. 2005).

  3. Following Okasha (2006, p. 18), I will consider that a “level of selection is simply the hierarchical level occupied by the entities that are units of selection.”

  4. In the species-as-individuals literature, the term “individuals” is used without any adjective, but a more specific term was necessary here, in order to establish a distinction with “evolutionary individuals,” hence the term “cohesive individuals.” “Cohesion” has been defined by Mishler and Brandon (1987) as “situations where an entity behaves as a whole with respect to some process,” the relevant process being natural selection, in contrast to “integration,” which corresponds to “active interaction among the parts of an entity” (Mishler and Brandon 1987). Here, the notion of “cohesive individuals” combines two criteria, the persistence through time of the internal organization (Hull 1978), and the response as a whole to natural selection (Mishler and Brandon 1987).

  5. See also the mathematical framework of Tikhonov (2016), which considers a scenario where two communities are brought into contact. The similarity between the resulting offspring community and the two parental communities depends on community-level rather than on species-level properties.

  6. There was a single parent in one of the two experiments presented in Swenson et al. (2000b).

  7. The replicator/interactor distinction has been introduced by Hull (1981). However, as pointed out by Okasha (2006), Brandon (1982) makes a similar move with his unit/level dichotomy.

  8. But see the case of hybrid speciation, e.g., Mallet (2007).

  9. The term “phenotype” designates both single traits of an individual organism (e.g., body mass) or an ensemble of its traits which together characterize this evolutionary individual. If trait ensembles are defined coarsely, several individuals may share the same phenotype. If they are defined finely, each phenotypic category will include a single individual (Godfrey-Smith 2009, p. 35). Unless specified, we will generally use the term “phenotype” in the case of a single discretized trait (e.g., heavy, medium, light). In that case, many individuals can share the same phenotype.

  10. The degree of cohesive individuality measures how well the internal organization of a unit of evolution persists through time, and at which point does it respond as a whole to natural selection. It should not be confused with the degree of evolutionary individuality, which measures how the units of selection conform with the classical three tenets of ENS (Godfrey-Smith 2009; Pradeu 2016).

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Acknowledgements

I thank Yves D. J. Meinard, Georges J. F. Arnoldi, and three anonymous reviewers for their thoughtful suggestions on an earlier version of this manuscript. I am also indebted to the participants of the workshop entitled “Evolution des écosystèmes” (Paris 2018, supported by the GDR Theomodive) for their discussions about ecological and evolutionary theory.

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  1. Laboratoire d’Ecologie Alpine, Université Savoie Mont Blanc, Chambéry, France

    Sébastien Ibanez

  2. Centre National de la Recherche Scientifique (CNRS), UMR 5553, Université Grenoble Alpes, Grenoble, France

    Sébastien Ibanez

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Ibanez, S. The Evolution of Ecosystem Phenotypes. Biol Theory 15, 91–106 (2020). https://doi.org/10.1007/s13752-020-00345-8

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