Post‐association barrier to host switching maintained despite strong selection in a novel mutualism

Abstract

Following a host shift, repeated co‐passaging of a mutualistic pair is expected to increase fitness over time in one or both species. Without adaptation, a novel association may be evolutionarily short‐lived as it is likely to be outcompeted by native pairings. Here, we test whether experimental evolution can rescue a low‐fitness novel pairing between two sympatric species of Steinernema nematodes and their symbiotic Xenorhabdus bacteria. Despite low mean fitness in the novel association, considerable variation in nematode reproduction was observed across replicate populations. We selected the most productive infections, co‐passaging this novel mutualism nine times to determine whether selection could improve the fitness of either or both partners. We found that neither partner showed increased fitness over time. Our results suggest that the variation in association success was not heritable and that mutational input was insufficient to allow evolution to facilitate this host shift. Thus, post‐association costs of host switching may represent a formidable barrier to novel partnerships among sympatric mutualists.

Host Association and Spatial Proximity Shape but Do Not Constrain Population Structure in the Mutualistic Symbiont Xenorhabdus bovienii

“…For a host shift to occur, lineage 1 bacteria would be carried into an insect with one species of nematode and leave with another, and to persist, this novel pairing would have to outcompete the native pairs. In noncompetitive laboratory experiments, wherein aposymbiotic nematodes are paired with novel bacteria, S. affine nematodes were not able to accept X. bovienii bacteria from S. kraussei or S. texanum , while S. kraussei nematodes could accept S. affine -associated X. bovienii bacteria, albeit at such a severe fitness cost that the pairing would be unlikely to persist in nature ( 30 , 34 ). In contrast, S. kraussei nematodes were found to accept S. texanum -associated X. bovienii with no reduction in fitness.…”

Adaptive colonization across a parasitism–mutualism gradient

“…Evolutionary rescue theory has incorporated biotic interactions in a variety of ways ( Klausmeier et al, 2020 ; Searle & Christie, 2021 ). In particular, evolutionary rescue has been applied to the colonization of a novel host by a pathogen ( Gandon et al, 2013 ), the evolution of a “naive” host in response to a novel pathogen ( Christie & Searle, 2018 ; DiRenzo et al, 2018 ; Golas, 2021 ), success in the establishment of a novel mutualism ( Dinges et al, 2022 ), the effects of a novel pathogen on evolutionary rescue of a host metapopulation ( Jiao et al, 2020 ), and the influence of positive interactions in evolutionary rescue ( Goldberg & Friedman, 2021 ; Henriques & Osmond, 2020 ). Moreover, Jones and Gomulkiewicz (2012) revealed how interactions with resident species (including predator–prey, mutualistic, and competitive relationships) shape the establishment success of an introduced species.…”