The Evolution of Mutualistic Dependence

Chomicki, Guillaume; Kiers, E. Toby; Renner, Susanne S.

doi:10.1146/annurev-ecolsys-110218-024629

Cited by 83 publications

(80 citation statements)

References 166 publications

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“…called cheaters if they benefit from nonreciprocating and are evolutionarily derived from mutualists; see refs. [13][14] potentially share in the collective benefits the host provides, while paying lower costs. A major question in symbiosis research is how such conflicts are avoided.…”

Section: Introductionmentioning

confidence: 99%

Compartmentalization drives the evolution of symbiotic cooperation

Chomicki

Werner

West

et al. 2020

Phil. Trans. R. Soc. B

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Across the tree of life, hosts have evolved mechanisms to control and mediate interactions with symbiotic partners. We suggest that the evolution of physical structures that allow hosts to spatially separate symbionts, termed compartmentalization, is a common mechanism used by hosts. Such compartmentalization allows hosts to: (i) isolate symbionts and control their reproduction; (ii) reward cooperative symbionts and punish or stop interactions with non-cooperative symbionts; and (iii) reduce direct conflict among different symbionts strains in a single host. Compartmentalization has allowed hosts to increase the benefits that they obtain from symbiotic partners across a diversity of interactions, including legumes and rhizobia, plants and fungi, squid and Vibrio , insects and nutrient provisioning bacteria, plants and insects, and the human microbiome. In cases where compartmentalization has not evolved, we ask why not. We argue that when partners interact in a competitive hierarchy, or when hosts engage in partnerships which are less costly, compartmentalization is less likely to evolve. We conclude that compartmentalization is key to understanding the evolution of symbiotic cooperation. This article is part of the theme issue ‘The role of the microbiome in host evolution’.

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Section: Introductionmentioning

confidence: 99%

Compartmentalization drives the evolution of symbiotic cooperation

Chomicki

Werner

West

et al. 2020

Phil. Trans. R. Soc. B

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“…Numerous experimental and observational studies have shown that symbiotic interactions, both parasitic and mutualistic, have dramatic effects on the host organism (Chomicki et al, 2020; Firth et al, 2017). Such interactions can alter the host's experience of environmental stress by altering the host phenotype (Feldhaar, 2011), with consequences for host fitness (i.e.…”

Section: Introductionmentioning

confidence: 99%

Foul‐weather friends: Modelling thermal stress mitigation by symbiotic endolithic microbes in a changing environment

Zardi

Monsinjon

McQuaid

et al. 2021

Global Change Biology

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Temperature extremes are predicted to intensify with climate change. These extremes are rapidly emerging as a powerful driver of species distributional changes with the capacity to disrupt the functioning and provision of services of entire ecosystems, particularly when they challenge ecosystem engineers. The subsequent search for a robust framework to forecast the consequences of these changes mostly ignores within‐species variation in thermal sensitivity. Such variation can be intrinsic, but can also reflect species interactions. Intertidal mussels are important ecosystem engineers that host symbiotic endoliths in their shells. These endoliths unexpectedly act as conditionally beneficial parasites that enhance the host's resistance to intense heat stress. To understand how this relationship may be altered under environmental change, we examined the conditions under which it becomes advantageous by reducing body temperature. We deployed biomimetic sensors (robomussels), built using shells of mussels (Mytilus galloprovincialis) that were or were not infested by endoliths, at nine European locations spanning a temperature gradient across 22°of latitude (Orkney, Scotland to the Algarve, Portugal). Daily wind speed and solar radiation explained the maximum variation in the difference in temperature between infested and non‐infested robomussels; the largest difference occurred under low wind speed and high solar radiation. From the robomussel data, we inferred body temperature differences between infested and non‐infested mussels during known heatwaves that induced mass mortality of the mussel Mytilus edulis along the coast of the English Channel in summer 2018 to quantify the thermal advantage of endolith infestation during temperature extremes. Under these conditions, endoliths provided thermal buffering of between 1.7°C and 4.8°C. Our results strongly suggest that sustainability of intertidal mussel beds will increasingly depend on the thermal buffering provided by endoliths. More generally, this work shows that biomimetic models indicate that within‐species thermal sensitivity to global warming can be modulated by species interactions, using an intertidal host–symbiont relationship as an example.

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“…Evolutionary interactions between hosts and their symbionts can shape patterns of genetic diversity and adaptation in natural communities ( Kaltz and Shykoff, 1998 ; Howells et al, 2013 ; Caldera et al, 2019 ). For this diversification to occur there must be heritable variation in the traits determining the “compatibility” between a host and a symbiont, from resistance and infectivity to more complex life-history or developmental traits ( Law and Dieckmann, 1998 ; Dale and Moran, 2006 ; Chomicki et al, 2020 ). In many systems, this variation can be assessed in controlled infection experiments, using different combinations of host and symbiont genotypes ( Carius et al, 2001 ; Kaltz and Shykoff, 2002 ; Cayetano and Vorburger, 2013 ).…”

Section: Introductionmentioning

confidence: 99%

Among-Strain Variation in Resistance of Paramecium caudatum to the Endonuclear Parasite Holospora undulata: Geographic and Lineage-Specific Patterns

et al. 2020

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Resistance is a key determinant in interactions between hosts and their parasites. Understanding the amount and distribution of variation in this trait between strains can provide insights into (co)evolutionary processes and their potential to shape patterns of diversity in natural populations. Using controlled inoculation in experimental mass cultures, we investigated the quantitative variation in resistance to the bacterial parasite Holospora undulata across a worldwide collection of strains of its ciliate host Paramecium caudatum. We combined the observed variation with available information on the phylogeny and biogeography of the strains. We found substantial variation in resistance among strains, with upper-bound values of broad-sense heritability >0.5 (intraclass correlation coefficients). Strain estimates of resistance were repeatable between laboratories and ranged from total resistance to near-complete susceptibility. Early (1 week post inoculation) measurements provided higher estimates of resistance heritability than did later measurements (2–3 weeks), possibly due to diverging epidemiological dynamics in replicate cultures of the same strains. Genetic distance (based on a neutral marker) was positively correlated with the difference in resistance phenotype between strains (r = 0.45), essentially reflecting differences between highly divergent clades (haplogroups) within the host species. Haplogroup A strains, mostly European, were less resistant to the parasite (49% infection prevalence) than non-European haplogroup B strains (28%). At a smaller geographical scale (within Europe), strains that are geographically closer to the parasite origin (Southern Germany) were more susceptible to infection than those from further away. These patterns are consistent with a picture of local parasite adaptation. Our study demonstrates ample natural variation in resistance on which selection can act and hints at symbiont adaptation producing signatures in geographic and lineage-specific patterns of resistance in this model system.

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The Evolution of Mutualistic Dependence

Cited by 83 publications

References 166 publications

Compartmentalization drives the evolution of symbiotic cooperation

Compartmentalization drives the evolution of symbiotic cooperation

Foul‐weather friends: Modelling thermal stress mitigation by symbiotic endolithic microbes in a changing environment

Among-Strain Variation in Resistance of Paramecium caudatum to the Endonuclear Parasite Holospora undulata: Geographic and Lineage-Specific Patterns

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