The Potential for Genotype-by-Environment Interactions to Maintain Genetic Variation in a Model Legume–Rhizobia Mutualism

Abstract

The maintenance of genetic variation in mutualism-related traits is key for understanding mutualism evolution, yet the mechanisms maintaining variation remain unclear. We asked whether genotype-by-environment (G×E) interaction is a potential mechanism maintaining variation in the model legume–rhizobia system, Medicago truncatula–Ensifer meliloti . We planted 50 legume genotypes in a greenhouse under ambient light and shade to reflect reduced carbon availability for plants. We found an expected reduction under shaded conditions for plant performance traits, such as leaf number, aboveground and belowground biomass, and a mutualism-related trait, nodule number. We also found G×E for nodule number, with ∼83% of this interaction due to shifts in genotype fitness rank order across light environments, coupled with strong positive directional selection on nodule number regardless of light environment. Our results suggest that G×E can maintain genetic variation in a mutualism-related trait that is under consistent positive directional selection across light environments.

Genome-wide association studies across environmental and genetic contexts reveal complex genetic architecture of symbiotic extended phenotypes

“…Next we discuss the coevolutionary implications of genotypedependence (G x G interactions), then wrap up with a call for further synthesis with metabolic network models towards systems genetics of symbiosis. (106,88,107,108). Nevertheless we note that these sorts of G × E variants were rare in our study, despite strong rank-order effects among strain means at the organismal level (Table 2); moreover, because our "environments" were simply different greenhouse experiments, relating such antagonistic effects to adaptation in the wild will require the type of in situ studies that are common in plants (e.g., 100, 97, 109) but more difficult in soil microbes.…”

“…Evolutionary change in response to environments implies that the loci underlying selected traits have differential effects on fitness across environments. Here we identify the loci that generate important trait variation both within and among environments, the (90,108,109,110). Nevertheless we note that these sorts of G × E variants were rare in our study, despite strong rank-order effects among strain means at the organismal level (Table 2); moreover, because our "environments" were simply different greenhouse experiments, relating such antagonistic effects to adaptation in the wild will require the type of in situ studies that are common in plants (e.g., 99,102,111) but more difficult in soil microbes.…”

“…Despite widespread conditional neutrality, a handful of interesting variants had strong effects on host growth, but in opposing directions across experiments within a single host genetic background. These sorts of antagonistic effects can favour different variants in different environments, and thus, potentially help explain the maintenance of mutualism variation in nature (95,113,114,115). Nevertheless we note that these sorts of G × E variants were rare in our study, despite strong s://doi.org/10.1101/2021.08.03.454976 bioRχiv: https://doi.org/10.1101/2021.08.03.454976 bioRχiv: https://doi.org/10.1101/2021.08.03.454976 bioRχiv: https://doi.org/10.1101/2021.08 rank-order effects among strain means at the organismal level (Table 2); moreover, because our "environments" were simply different greenhouse experiments, relating such antagonistic effects to adaptation in the wild will require the type of in situ studies that are common in plants (e.g., 104,107,116) but more difficult in soil microbes.…”

A New Year's spotlight on two years of publication

“…(2020) assessed the impact of demographic processes on genomic diversity and positive selection in Arabidopsis lyrata by analyzing re-sequencing data from 52 populations collected worldwide. Vaidya and Stinchcombe (2020) used the Medicago truncatula - Ensifer meliloti system to demonstrate that genotype-by-environment interactions make a significant contribution to maintaining genetic variation in mutualisms, and Hodgins et al. (2020) found that invasive populations of Canada thistle show rapid adaptation with no trade-off between stress tolerance and performance.…”

Plant Evolutionary Adaptation

“…Under this assumption, genotypes that perform well in one environment do poorly in another, ensuring that variation is maintained. Vaidya and Stinchcombe (2020) tested this hypothesis by examining the performance of 50 legume genotypes in different light environments. Changes in genotype fitness rank were observed across light environments, confirming that, as predicted, G × E is responsible for the maintenance of variation in mutualism-enhancing traits in this system.…”