Standing genetic variation in host preference for mutualist microbial symbionts

Abstract

Many models of mutualisms show that mutualisms are unstable if hosts lack mechanisms enabling preferential associations with mutualistic symbiotic partners over exploitative partners. Despite the theoretical importance of mutualism-stabilizing mechanisms, we have little empirical evidence to infer their evolutionary dynamics in response to exploitation by non-beneficial partners. Using a model mutualism-the interaction between legumes and nitrogen-fixing soil symbionts-we tested for quantitative genetic variation in plant responses to mutualistic and exploitative symbiotic rhizobia in controlled greenhouse conditions. We found significant broad-sense heritability in a legume host's preferential association with mutualistic over exploitative symbionts and selection to reduce frequency of associations with exploitative partners. We failed to detect evidence that selection will favour the loss of mutualism-stabilizing mechanisms in the absence of exploitation, as we found no evidence for a fitness cost to the host trait or indirect selection on genetically correlated traits. Our results show that genetic variation in the ability to preferentially reduce associations with an exploitative partner exists within mutualisms and is under selection, indicating that micro-evolutionary responses in mutualism-stabilizing traits in the face of rapidly evolving mutualistic and exploitative symbiotic bacteria can occur in natural host populations.

Host investment into symbiosis varies among genotypes of the legume Acmispon strigosus, but host sanctions are uniform

“…Host sanctions against ineffective symbionts were robust in hosts from all populations, but we found variation in host ability to preferentially invest in nodule size according to symbiont effectiveness, even when plants were also enacting sanctions (i.e., in the co‐inoculation experiment). This study contributes to reports of variation in host control from two other legume species (soybean, Kiers et al ., ; Medicago lupulina , Simonsen & Stinchcombe, ), suggesting that this could be a consistent feature of legume species that engage in symbiosis. Differences in symbiont fitness produced by the combined action of invariant sanctions and variable investment could help maintain variation in the effectiveness of symbiont populations.…”

Geographically structured genetic variation in theMedicago lupulina–Ensifermutualism

“…Variation in performance among partner genotypes is important for driving the evolution of partner choice, host sanctions, and cheating in mutualisms, an area that has been explored extensively in the legume–rhizobia symbiosis (Sachs and Simms ; Frederickson ; Simonsen and Stinchcombe ; Jones et al. ).…”

Environmental variation impacts trait expression and selection in the legume–rhizobium symbiosis

“…In a previous study, Simonsen and Stinchcombe (2014b) collected M. lupulina seeds from 11 subpopulations spanning 1.2 km 2 of the University of Toronto's Koffler Scientific Reserve (KSR, http://www.ksr.utoronto.ca), located in King, Ontario, Canada. Toward reducing maternal effects, seeds from each subpopulation were selfed for one generation in the greenhouse, and 10 lines from each subpopulation were randomly selected for a total of 110 lines.…”

“…We planted 30 lines of the legume Medicago lupulina in four plots in old fields in southern Ontario. The same 30 lines were also used in a previous greenhouse experiment (Simonsen and Stinchcombe, 2014b), allowing us to test how the environment impacts the expression of genetic variance (G × E interactions) in and selection (S × E interactions) on a key mutualism‐related trait, nodulation. The greenhouse environment differed from the field in several important ways: the only source of nitrogen available to plants was that fixed by rhizobia, only two strains of rhizobia were present in the soil, and the spatial and temporal heterogeneity of key resources (e.g., light, water, nutrients other than N) were minimized.…”