Evolutionary signals of symbiotic persistence in the legume-rhizobia mutualism

Abstract

Understanding the origins and evolutionary trajectories of symbiotic partnerships remains a major challenge. Why are some symbioses lost over evolutionary time whereas others become crucial for survival? Here, we use a quantitative trait reconstruction method to characterize different evolutionary stages in the ancient symbiosis between legumes (Fabaceae) and nitrogen-fixing bacteria, asking how labile is symbiosis across different host clades. We find that more than half of the 1,195 extant nodulating legumes analyzed have a high likelihood (>95%) of being in a state of high symbiotic persistence, meaning that they show a continued capacity to form the symbiosis over evolutionary time, even though the partnership has remained facultative and is not obligate. To explore patterns associated with the likelihood of loss and retention of the N2-fixing symbiosis, we tested for correlations between symbiotic persistence and legume distribution, climate, soil and trait data. We found a strong latitudinal effect and demonstrated that low mean annual temperatures are associated with high symbiotic persistence in legumes. Although no significant correlations between soil variables and symbiotic persistence were found, nitrogen and phosphorus leaf contents were positively correlated with legumes in a state of high symbiotic persistence. This pattern suggests that highly demanding nutrient lifestyles are associated with more stable partnerships, potentially because they "lock" the hosts into symbiotic dependency. Quantitative reconstruction methods are emerging as a powerful comparative tool to study broad patterns of symbiont loss and retention across diverse partnerships.

Keywords: cooperation; deep history; persistence; reconstruction; symbiosis.

Fig. 1.

Histogram of the stable fixing likelihood for all nodulating legume species in our reconstruction. To illustrate this variation, we list a range of species and their associated likelihoods of being stable fixers. Species with a stable fixing likelihood of over 50% are labeled red; the other species are labeled blue.

Fig. 2.

Pie charts indicate the likelihood of a host node being in either a nonsymbiotic state (orange), a “regular” N₂-fixing state (green), or in a stable fixing state (purple), where the symbiosis has a high persistence. Represented are the legumes from their ancestral node about 62 million years ago. After the evolution of symbiotic nitrogen fixation (transition from orange to green), repeated evolution of stable fixing (transition from green to purple) is found across the legumes. Particularly within the Papilionoideae, legume species are very likely to currently be stable fixers, meaning that they show a continued capacity to form the symbiosis over evolutionary time. (Scale bar: 10 million years.)

Fig. 3.

Occurrences of regular (A, blue) and stable fixing (B, red) legumes across the globe extracted from the Global Biodiversity Information Facility. Over 3.2 million occurrence records were plotted for the nodulating legumes analyzed in our dataset (Methods).

Fig. 4.

Positive correlation between the calculated likelihood of extant nodulating legumes being in a stable fixing state and the average leaf nitrogen content of these same species (phylogenetic regression, P = 0.03).

Fig. 5.

Positive correlation between the calculated likelihood of extant nodulating legumes being in a stable fixing state and the average leaf phosphorus content of these same species (phylogenetic regression, P = 0.03).