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Comparative genomics reveals convergent rates of evolution in ant-plant mutualisms.

ABSTRACT: Symbiosis-the close and often long-term interaction of species-is predicted to drive genome evolution in a variety of ways. For example, parasitic interactions have been shown to increase rates of molecular evolution, a trend generally attributed to the Red Queen Hypothesis. However, it is much less clear how mutualisms impact the genome, as both increased and reduced rates of change have been predicted. Here we sequence the genomes of seven species of ants, three that have convergently evolved obligate plant-ant mutualism and four closely related species of non-mutualists. Comparing these sequences, we investigate how genome evolution is shaped by mutualistic behaviour. We find that rates of molecular evolution are higher in the mutualists genome wide, a characteristic apparently not the result of demography. Our results suggest that the intimate relationships of obligate mutualists may lead to selective pressures similar to those seen in parasites, thereby increasing rates of evolution.

SUBMITTER: Rubin BE

PROVIDER: S-EPMC5007375 | biostudies-literature | 2016 Aug

REPOSITORIES: biostudies-literature

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Comparative genomics reveals convergent rates of evolution in ant-plant mutualisms.

Rubin Benjamin E R BE Moreau Corrie S CS

Nature communications 20160825

Symbiosis-the close and often long-term interaction of species-is predicted to drive genome evolution in a variety of ways. For example, parasitic interactions have been shown to increase rates of molecular evolution, a trend generally attributed to the Red Queen Hypothesis. However, it is much less clear how mutualisms impact the genome, as both increased and reduced rates of change have been predicted. Here we sequence the genomes of seven species of ants, three that have convergently evolved ...[more]

PMID: 27557866

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Project description:Costs and benefits for partners in mutualistic interactions can vary greatly, but surprisingly little is known about the factors that drive this variation across systems. We conducted a meta-analysis of ant-plant protective mutualisms to quantify the effects of ant defenders on plant reproductive output, to evaluate if reproductive effects were predicted from reductions in herbivory and to identify characteristics of the plants, ants and environment that explained variation in ant protection. We also compared our approach with two other recent meta-analyses on ant-plant mutualisms, emphasizing differences in our methodology (using a weighted linear mixed effects model) and our focus on plant reproduction rather than herbivore damage. Based on 59 ant and plant species pairs, ant presence increased plant reproductive output by 49% and reduced herbivory by 62%. The effects on herbivory and reproduction within systems were positively correlated, but the slope of this relationship (0.75) indicated that tolerance to foliar herbivory may be a common plant response to absence of ant guards. Furthermore, the relationship between foliar damage and reproduction varied substantially among systems, suggesting that herbivore damage is not a reliable surrogate for fitness consequences of ant protection. Studies that experimentally excluded ants reported a smaller effect of ant protection on plant reproduction than studies that relied upon natural variation in ant presence, suggesting that study methods can affect results in these systems. Of the ecological variables included in our analysis, only plant life history (i.e., annual or perennial) explained variation in the protective benefit of mutualistic ants: presence of ants benefitted reproduction of perennials significantly more than that of annuals. These results contrast with other quantitative reviews of these relationships that did not include plant life history as an explanatory factor and raise several questions to guide future research on ant-plant protection mutualisms.

Dataset Information

Comparative genomics reveals convergent rates of evolution in ant-plant mutualisms.

Publications

Comparative genomics reveals convergent rates of evolution in ant-plant mutualisms.

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