Rapid compensatory evolution can rescue low fitness symbioses following partner-switching

Abstract

Partner-switching plays an important role in the evolution of symbiosis, enabling local adaptation and recovery from the breakdown of symbiosis. Because of intergenomic epistasis, partner-switched symbioses may possess novel combinations of phenotypes but may also exhibit low fitness due to their lack of recent coevolutionary history. Here, we examine the structure and mechanisms of intergenomic epistasis in the Paramecium-Chlorella symbiosis and test if compensatory evolution can rescue initially low fitness partner-switched symbioses. Using partner-switch experiments coupled with metabolomics we show evidence for intergenomic epistasis wherein low fitness arose from mismatched photoprotection traits and the resulting light stress experienced by non-native symbionts when in high light environments. Experimental evolution under high light conditions revealed that an initially low fitness partner-switched non-native host-symbiont pairing rapidly adapted, gaining fitness equivalent to the native host symbiont pairing in less than 50 host generations. Compensatory evolution took two alternative routes: Either, hosts evolved higher symbiont loads to mitigate for their new algal symbiont's poor performance, or the algal symbionts themselves evolved higher investment in photosynthesis and photoprotective traits to better mitigate light stress. These findings suggest that partner-switching combined with rapid compensatory evolution will enable the recovery and local adaptation of symbioses in response to changing environments.

Emergent RNA–RNA interactions can promote stability in a facultative phototrophic endosymbiosis

“…The interaction is facultative (11,(14)(15)(16)(17) and based on two-way metabolic exchange (18)(19)(20)(21)(22)(23)(24)(25)(26). Endosymbiotic algae are housed within modified host phagosomes called perialgal vacuoles, which may be fused with host lysosomes to trigger digestion (14,27), allowing P. bursaria to maintain a high degree of control over the interaction in the event of conflict (28)(29)(30). However, it is unclear how this endosymbiotic system is protected from overexploitation by the host, which would ultimately lead the interaction to collapse (31)(32)(33)(34)(35)(36).…”

Emergent RNA-RNA interactions can promote stability in a nascent phototrophic endosymbiosis

“…Identification of undirected 'RNAi collisions' in the P. bursaria -Chlorella system represents one such intermediary state, emergent in nature and untargeted, upon which sustained cellular interaction coupled with the potential for host-symbiont conflict could drive the selection of targeted RNA-RNA interactions. The reduced pattern of co-evolution between endosymbiont and host in the P. bursaria -Chlorella system, resulting from the potential for repeated partner switching by the host 11,34 , offers a possible explanation for why this mechanism has remained emergent.…”

“…The interaction is facultative 11,14–17 and based on two-way metabolic exchange 18–25 . Endosymbiotic algae are housed within modified host phagosomes called perialgal vacuoles, which may be fused with host lysosomes to trigger digestion 26 allowing P. bursaria to maintain control over the interaction in the event of conflict 27–29 . However, it is unclear how this endosymbiotic system is protected from over-exploitation by the host which would ultimately lead the interaction to collapse 30–35 .…”

“…Disruption of the endosymbiosis can lead to fusion of host lysosomes with the perialgal vacuoles and lysis of the algal endosymbiont within 29 . Manipulation of the endosymbiont population, including partner switching, is believed to have allowed P. bursaria to maintain control over the interaction [32][33][34] . Yet it is unclear how this endosymbiotic system is protected from over-exploitation by the host which would ultimately lead the interaction to collapse [35][36][37][38][39][40] .RNA-RNA interactions can play a role in host-pathogen symbiotic systems [41][42][43][44][45] , whereby RNA is passed between interacting partners in order to modulate the expression of genes involved in virulence or resistance 41,44,45 .…”

Epistasis and Adaptation on Fitness Landscapes

“…As a first step and proof-of-concept to address this question, features of probabilistic fitness landscapes with widespread epistasis could be incorporated into genomic simulations to quantify how the presence of epistasis changes subsequent population-genetic inference. Finally, epistasis can span all biological levels of organization: within or between genes, between host and symbiont, and possibly between species (see, e.g., Sørensen et al 2021, Buskirk et al 2020. Incorporating these levels into a theory of co-evolutionary fitness landscape is an exciting challenge.…”