The evolution of mutualistic symbiosis is a puzzle that has fascinated evolutionary ecologist for quite a while. Data on transitions between symbiotic bacterial ways of life has evidenced shifts from mutualism towards parasitism and vice versa (Sachs et al., 2011), so there does not seem to be a strong determinism on those transitions. From the host’s perspective, mutualistic symbiosis implies at the very least some form of immune tolerance, which can be costly (e.g. Sorci, 2013). Empirical approaches thus raise very important questions: How can symbiosis turn from parasitism into mutualism when it seemingly needs such a strong alignment of selective pressures on both the host and the symbiont? And yet why is mutualistic symbiosis so widespread and so important to the evolution of macro-organisms (Margulis, 1998)?

While much of the theoretical literature on the evolution of symbiosis and mutualism has focused on either the stability of such relationships when non-mutualists can invade the host-symbiont system (e.g. Ferrière et al., 2007) or the effect of the mode of symbiont transmission on the evolutionary dynamics of mutualism (e.g. Genkai-Kato and Yamamura, 1999), the question remains whether and under which conditions parasitic symbiosis can turn into mutualism in the first place. Earlier results suggested that spatial demographic heterogeneity between host populations could be the leading determinant of evolution towards mutualism or parasitism (Hochberg et al., 2000). Here, Ledru et al. (2022) investigate this question in an innovative way by simulating host-symbiont evolutionary dynamics in a spatially explicit context. Their hypothesis is intuitive but its plausibility is difficult to gauge without a model: Does the evolution towards mutualism depend on the ability of the host and symbiont to evolve towards close-range dispersal in order to maintain clusters of efficient host-symbiont associations, thus outcompeting non-mutualists?

I strongly recommend reading this paper as the results obtained by the authors are very clear: competition strength and the cost of dispersal both affect the likelihood of the transition from parasitism to mutualism, and once mutualism has set in, symbiont trait values clearly segregate between highly dispersive parasites and philopatric mutualists. The demonstration of the plausibility of their hypothesis is accomplished with brio and thoroughness as the authors also examine the conditions under which the transition can be reversed, the impact of the spatial range of competition and the effect of mortality. Since high dispersal cost and strong, long-range competition appear to be the main factors driving the evolutionary transition towards mutualistic symbiosis, now is the time for empiricists to start investigating this question with spatial structure in mind.

References

Ferrière, R., Gauduchon, M. and Bronstein, J. L. (2007) Evolution and persistence of obligate mutualists and exploiters: competition for partners and evolutionary immunization. Ecology Letters, 10, 115-126. https://doi.org/10.1111/j.1461-0248.2006.01008.x

Genkai-Kato, M. and Yamamura, N. (1999) Evolution of mutualistic symbiosis without vertical transmission. Theoretical Population Biology, 55, 309-323. https://doi.org/10.1006/tpbi.1998.1407

Hochberg, M. E., Gomulkiewicz, R., Holt, R. D. and Thompson, J. N. (2000) Weak sinks could cradle mutualistic symbioses - strong sources should harbour parasitic symbioses. Journal of Evolutionary Biology, 13, 213-222. https://doi.org/10.1046/j.1420-9101.2000.00157.x

Ledru L, Garnier J, Rohr M, Noûs C and Ibanez S (2022) Mutualists construct the ecological conditions that trigger the transition from parasitism. bioRxiv, 2021.08.18.456759, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.08.18.456759

Margulis, L. (1998) Symbiotic planet: a new look at evolution, Basic Books, Amherst.

Sachs, J. L., Skophammer, R. G. and Regus, J. U. (2011) Evolutionary transitions in bacterial symbiosis. Proceedings of the National Academy of Sciences, 108, 10800-10807. https://doi.org/10.1073/pnas.1100304108

Sorci, G. (2013) Immunity, resistance and tolerance in bird–parasite interactions. Parasite Immunology, 35, 350-361. https://doi.org/10.1111/pim.12047