Seasonal wild dance of dual endosymbionts in the pear psyllid Cacopsylla pyricola (Hemiptera: Psylloidea)

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英语. <div><p>Most sap-feeding insects maintain obligate relationships with endosymbiotic bacteria that provide their hosts with essential nutrients. However, knowledge about the dynamics of endosymbiont titers across seasons in natural host populations is scarce. Here, we used quantitative PCR to investigate the seasonal dynamics of the dual endosymbionts "Candidatus Carsonella ruddii" and "Ca. Psyllophila symbiotica" in a natural population of the pear psyllid Cacopsylla pyricola (Hemiptera: Psylloidea: Psyllidae). Psyllid individuals were collected across an entire year, covering both summer and overwintering generations. Immatures harboured the highest titers of both endosymbionts, while the lowest endosymbiont density was observed in males. The density of Carsonella remained high and relatively stable across the vegetative period of the pear trees, but significantly dropped during the non-vegetative period, overlapping with C. pyricola's reproductive diapause. In contrast, the titer of Psyllophila was consistently higher than Carsonella's and exhibited fluctuations throughout the sampling year, which might be related to host age. Despite a tightly integrated metabolic complementarity between Carsonella and Psyllophila, our findings highlight differences in their density dynamics throughout the year, that might be linked to their metabolic roles at different life stages of the host.</p><p>Symbiotic associations between Eukaryotic and Prokaryotic organisms have had a tremendous impact on the diversification of multicellular organisms, contributing to a great proportion of the planet's biodiversity 1,2 . For instance, endosymbiotic bacteria played a central role in shaping the ecological niches of phytophagous insects by enabling them to feed on a nutritionally unbalanced plant sap diet 3-5 . Bacterial endosymbionts of phytophagous insects are often housed within specialized cells (bacteriocytes) aggregated within special organs (bacteriomes) and provide their hosts with essential nutrients lacking in the plant sap 4,6 . This resulted in the establishment of obligate co-diverging host-symbiont associations, accompanied by drastic reductions in the genome size of the symbiotic bacteria until only core housekeeping genes and biosynthetic pathways for the nutrients required by the insect hosts are retained 7-9 . Many sap-feeding hemipteran lineages, such as sternorrhynchans (aphids, adelgids, psyllids, scales, mealybugs) and auchenorrhynchans (planthoppers, spittlebugs, cicadas), are associated with more than one obligate endosymbiont 9 . In most dual endosymbiotic systems studied to date, the primary endosymbiont supplies the host with the majority of essential amino acids (EAAs), whereas the co-primary endosymbiont complements the genes or pathways that are no longer present in the primary endosymbiont 10-13 .</p><p>Although endosymbionts provide important benefits, maintaining them also entails fitness costs for the host. For instance, in aphids the titer of the primary endosymbiont Buchnera is negatively correlated with the overall host reproductive rate 14 . This is likely due to metabolic costs involved in endosymbiont maintenance 15 . Hence, optimal regulation of endosymbiont titers by the host is crucial to maintain a delicate balance: endosymbiont titers should be as low as possible to reduce the associated costs for the host but as high as necessary to produce sufficient amounts of nutrients and to ensure vertical transmission to the next generation 16-18 . Furthermore, due to different investments in reproduction, the host's nutritional requirements may vary across the host's life cycle OPEN</p></div>