Decreased coevolutionary potential and increased symbiont fecundity during the biological invasion of a legume‐rhizobium mutualism

Abstract

Although most invasive species engage in mutualism, we know little about how mutualism evolves as partners colonize novel environments. Selection on cooperation and standing genetic variation for mutualism traits may differ between a mutualism's invaded and native ranges, which could alter cooperation and coevolutionary dynamics. To test for such differences, we compare mutualism traits between invaded-and native-range host-symbiont genotype combinations of the weedy legume, Medicago polymorpha, and its nitrogen-fixing rhizobium symbiont, Ensifer medicae, which have coinvaded North America. We find that mutualism benefits for plants are indistinguishable between invaded-and native-range symbioses. However, rhizobia gain greater fitness from invaded-range mutualisms than from native-range mutualisms, and this enhancement of symbiont fecundity could increase the mutualism's spread by increasing symbiont availability during plant colonization. Furthermore, mutualism traits in invaded-range symbioses show lower genetic variance and a simpler partitioning of genetic variance between host and symbiont sources, compared to native-range symbioses. This suggests that biological invasion has reduced mutualists' potential to respond to coevolutionary selection. Additionally, rhizobia bearing a locus (hrrP) that can enhance symbiotic fitness have more exploitative phenotypes in invaded-range than in native-range symbioses. These findings highlight the impacts of biological invasion on the evolution of mutualistic interactions.

Negotiating mutualism: A locus for exploitation by rhizobia has a broad effect size distribution and context‐dependent effects on legume hosts

“…The wide effect size distribution and significant context dependency we reveal for hrrP effects suggest that the evolutionary impacts of candidate mutualism loci may be complex in natural mutualist populations. In contrast to previous findings that hrrP can improve the performance of rhizobia at the expense of plant hosts (Price et al, 2015;Wendlandt et al, 2021), we show that, on average, the presence of hrrP in a rhizobium strain's genome has positive effects on both plant host and rhizobium performance. Our findings broadly align with the working balance hypothesis of peptidase-NCR peptide activity, which predicts that complete suppression of HrrP activity (corresponding to our knockout mutants) harms both plant hosts and rhizobia by allowing host-derived NCR peptides to overdifferentiate rhizobia to the point that they are incapable of nitrogen fixation .…”

“…medicae strains and are only detectable in 56% of E . medicae populations (Wendlandt et al, 2021), consistent with a lack of strong fitness benefit of hrrP for rhizobium or host fitness. The fact that naturally occurring hrrP + and hrrP − rhizobia have only slightly different mean phenotypic effects on hosts (Wendlandt et al, 2021) could reflect a situation in which hrrP ‐ strains phenotypically resemble hrrP + strains for which hrrP has a nearly neutral effect size.…”

“…In the Knockout Experiment, we used one M. polymorpha genotype (RTM; Table 1). Plant host genotypes were named for the populations from which they were isolated; thus, the RTM host was sympatric to all the E. medicae strains having 'RTM' in their name (Wendlandt et al, 2021). In the G × G Knockout Experiment, we used two M. polymorpha genotypes (RTM, MEL; Table 1).…”

“…In a previous PCR screen, 12.5% of the E. medicae strain collection was found to bear hrrP (i.e., hrrP+ strains), with the remainder lacking this locus (i.e. hrrP-strains; Wendlandt et al, 2021). We performed targeted gene disruptions in 12 hrrP+ E. medicae strains to generate hrrP-knockout mutants, and measured hrrP effect size for each strain as the relative difference in trait values of hrrP+ and hrrP-strains.…”

Global potential distribution prediction of Xanthium italicum based on Maxent model

“…With the rapid development of economic globalization, international trade exchanges and human activities are becoming more and more frequent, alien invasive species are expanding at an unprecedented rate 1 – 3 . The resulting ecological problems and increasing risks of biological invasion have caused huge eco-environmental hazards and economic losses all over the world 4 , 5 . The biological invasion has become a great challenge for human beings.…”