Experimental evolution at high temperature in a Lepidopteran host of an entomopathogenic nematode and its associated microbiota

Entomopathogenic Nematodes (EPNs) have a great potential to control various insect crop pests, but their ability to perform their entire life-cycle in insects depends on environmental conditions. The insect killing ability of the endosymbiotic bacterial species (i.e., Xenorhabdus) located in the EPNs' gut (Steinernema) has been described for years. More recently, experimental data have suggested that other bacteria species of the nematode microbiota may also contribute to the parasitic success of the EPNs. EPNs and their associated bacteria should therefore be considered as holobionts. Global change, among its many predicted consequences, is expected to increase temperatures which may impair the parasitic success of these EPNs in the insect. Furthermore, higher environmental temperatures could modify the composition of the EPN-associated microbiota and could therefore also contribute to parasitic impairement. Using a S. carpocapsae strain originating from a French orchard, we investigated these hypotheses by experimentally evolving independent EPNs lineages in vivo in the lepidopteran species Galleria mellonella, at elevated and control temperatures. Several life-history traits of the evolved lineages were measured (insect killing ability, EPN emergence rate, EPN reproduction rate), and the bacterial microbiota of the evolved lineages was characterized by a metabarcoding approach. The EPNs' lineages evolved at higher temperature showed impaired emergence rate and their reproduction rate was lower, when compared to lineages evolved at control temperature. The bacterial microbiota composition of these lineages was modified, with particular enrichment in bacteria of the genera Alcaligenes and Pseudomonas. Our results provide new evidence that modification of the environment (here, the abiotic parameter temperature) during several successive generations can modify the parasitic success of EPNs, concomitantly to a change in the microbiota composition. A better understanding of the life-history traits of these EPNs should help improve the biocontrol efficiency in a context of global warming.