Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress

Abstract

Abstract 1. Natural populations of pea aphids in California contain at least two facultative bacterial secondary symbionts (pea aphid secondary symbiont, PASS, or pea aphid rickettsia, PAR) in a range of frequencies throughout the state. 2. Two pea aphid clones without either of these facultative associates failed to reproduce in the first 8 days after the final moult if they had been heat‐stressed for a period of about 4 h at 39 °C as 1‐day‐old larvae in the laboratory. 3. Aphids infected artificially with PASS, however, were able to produce up to 48% of the normal complement of offspring produced by PASS‐positive aphids that had not been heat‐stressed. Clones infected artificially with PAR did not have the same advantage as those with PASS after heat stress. 4. In aphids without PASS or PAR, heat stress reduced the number of bacteriocytes (in which the obligate primary symbiont, Buchnera , resides) to 7% of non‐heat‐stressed aphids, while aphids with only PASS retained 70% of their bacteriocytes. Bacteriocytes in aphids with PAR but not PASS were reduced to 42% of controls. 5. When larvae were heat‐stressed as older instars (5 days old), a similar pattern emerged, though the effect of heat stress was less extreme. Clones containing PASS produced the most offspring, three to 14 times as many as aphids without PASS or PAR. Aphids with PAR only, or PASS and PAR together, had reduced or no advantage over aphids without facultative symbionts. 6. Aphids of all clones that had been heat‐stressed as later instars gave birth to a variable number of stillborn offspring. Aphids without facultative symbionts produced the most stillborn larvae. 7. Field studies showed a higher incidence of PASS in aphids collected in California in summer compared with aphids from the same sites collected 2–4 months earlier. The difference was significant in two of three widely dispersed locations.