Understanding Mutualism When There is Adaptation to the Partner

de Mazancourt, C., Loreau, M., & Dieckmann, U. ORCID: https://orcid.org/0000-0001-7089-0393 (2005). Understanding Mutualism When There is Adaptation to the Partner. IIASA Interim Report. IIASA, Laxenburg, Austria: IR-05-016

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Abstract

1. A mutualism is a mutually beneficial interaction between individuals of two species. Using the ongoing debate about plant-herbivore interactions as a springboard, we show that different measures of benefit arise depending on whether adaptation within the mutualism is considered.

2. A species' proximate response measures the short-term effect of addition or removal of the partner species, without allowing for any adaptation. We define a proximate mutualism as an interaction in which removal of each partner results in a decreased performance of the other, i.e., both species show a positive proximate response to the presence of the partner.

3. Almost all empirical studies use the proximate response criterion. However, a proximate mutualism might only reflect evolved dependence (implying that, through adaptation to the partner, a species has lost its ability to perform well without the partner). Therefore, some authors discard the proximate definition of mutualism, to prefer what we define as ultimate mutualism.

4. A species' ultimate response measures the long-term effect of adding or removing the partner species, thus allowing for the focal species to adapt to the absence or presence of its partner. We define an ultimate mutualism as an interaction in which each partner could never have performed as well without the other, even if it was adapted to the absence of the partner. In other words, a mutualism is called ultimate if both species show a positive ultimate response to the presence of the partner. Despite the conceptual attractiveness of this definition, ultimate responses are difficult to measure, rendering the notion of ultimate mutualism operationally problematic.

5. Using examples from the literature, we demonstrate the counterintuitive result that even obligate mutualisms are not necessarily ultimate mutualisms.

6. Finally, we define mutualistic evolution 1 as evolution of a trait that is costly to the bearer but beneficial to its partner in a proximate mutualism and show that, paradoxically, neither proximate nor ultimate mutualisms necessarily result in mutualistic evolution.

7. We conclude that the proximate response is the only criterion for mutualism that is operational in empirical research. A possible key mechanism that can generate a benefit in such mutualisms, evolved dependence, has to be further investigated empirically and seriously taken into account in theoretical studies, if our understanding of mutualism is to evolve.

8. More than a semantic case of hair splitting, our paper reveals a naive view of mutualism that needs revision. We need to recognise that in most if not all interactions now considered as mutualisms, measured benefits to at least one partner are likely to be partly or even completely the result of adaptation to the partner, leading to evolved dependence, rather than to what we would like to consider as real or ultimate benefits.

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