Abstract
Research on mutualism seeks to explain how cooperation can be maintained when uncooperative mutants co-occur with cooperative kin. Gains and losses of the gene modules required for cooperation punctuate symbiont phylogenies and drive lifestyle transitions between cooperative symbionts and uncooperative free-living lineages over evolutionary time. Yet whether uncooperative symbionts commonly evolve from within cooperative symbiont populations or from within distantly related lineages with antagonistic or free-living lifestyles (i.e., third-party mutualism exploiters or parasites), remains controversial. We use genomic data to show that genotypes that differ in the presence or absence of large islands of symbiosis genes are common within a single wild recombining population of Mesorhizobium symbionts isolated from host tissues and are an important source of standing heritable variation in cooperation in this population. In a focal population of Mesorhizobium, uncooperative variants that lack a symbiosis island segregate at 16% frequency in nodules, and genome size and symbiosis gene number are positively correlated with cooperation. This finding contrasts with the genomic architecture of variation in cooperation in other symbiont populations isolated from host tissues in which the islands of genes underlying cooperation are ubiquitous and variation in cooperation is primarily driven by allelic substitution and individual gene gain and loss events. Our study demonstrates that uncooperative mutants within mutualist populations can comprise a significant component of genetic variation in nature, providing biological rationale for models and experiments that seek to explain the maintenance of mutualism in the face of non-cooperators.
Highlights
Mutualism theory seeks to explain the maintenance of cooperation between species despite the omnipresent threat of selfish, uncooperative mutants [1,2,3,4,5,6]
This finding contrasts with the genomic architecture of variation in mutualistic cooperation in other symbiont populations isolated from host tissues in which the islands of genes underlying cooperation are ubiquitous and variation in cooperation is primarily driven by allelic substitution and individual gene gain and loss events [31, 71,72,73,74]
In the recombining Mesorhizobium population we study, strains that differ in the presence or absence of the entire symbiosis island are common in host nodules, and this stands in stark contrast to the population genomics of symbiosis plasmids in other rhizobial populations
Summary
Mutualism theory seeks to explain the maintenance of cooperation between species despite the omnipresent threat of selfish, uncooperative mutants [1,2,3,4,5,6]. Empirical model systems often consider binary shifts in mutualistic cooperation, artificially generating uncooperative mutants that fail to provide host benefit [10,11,12,13]. Gains and losses of the genetic modules harboring symbiosis genes punctuate symbiont evolutionary histories and cause transitions between cooperative symbionts and uncooperative free-living lineages, though these are not necessarily antagonistic to their host [14,15,16,17]. A central challenge for understanding the evolution of mutualistic cooperation in natural populations is to understand how frequently such variation in the presence and absence of symbiosis genetic modules impact closely related symbionts competing for host resources
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