Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress

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.

Population dynamics of defensive symbionts in aphids

“…This result is perhaps not surprising, because this isolate of S. symbiotica was found to confer only moderate resistance to wasps, and parasitism interfered with reproduction such that infected, parasitized aphids received no direct fitness benefit to infection (Oliver et al 2003(Oliver et al , 2006. Other reports indicate that S. symbiotica provides thermal protection in A. pisum (Chen et al 2000;Montllor et al 2002;Russell & Moran 2006), and this effect may explain the persistence of this inherited symbiont in aphid populations in nature.…”

“…Experimental laboratory assays have identified diverse beneficial roles conferred by inherited symbionts of invertebrates (e.g. Montllor et al 2002;Oliver et al 2003;Tsuchida et al 2004). These studies identify potential mechanisms by which symbionts may invade and persist in host populations, but do not explicitly test the population dynamics of the mutualist symbiont infections within host populations.…”

“…In addition to Buchnera, aphids may also be infected with one or more facultatively associated, inherited bacteria, called secondary symbionts (SS). Recent laboratory studies have implicated A. pisum SS in mediating several phenotypes important to aphid survival and reproduction, including resistance to parasitic wasps (Oliver et al 2003(Oliver et al , 2005, resistance to fungal pathogens (Scarborough et al 2005), performance on particular host plants (Tsuchida et al 2004) and thermal tolerance (Chen et al 2000;Montllor et al 2002;Russell & Moran 2006). Two A. pisum SS have been shown to confer some level of resistance to parasitism by the wasp Aphidius ervi in laboratory assays.…”

Evidence for specificity in symbiont-conferred protection against parasitoids

“…Symbiotic bacteria play important roles in protecting their insect hosts from various threats, including viruses [61,62], fungal pathogens [13,15,63], parasites [64] and predators [65,66], as well as abiotic hazards such as heat shock [67,68]. However, these protective effects can differ markedly within a single symbiont 'species' [5,11,15].…”

Symbiosis as a source of selectable epigenetic variation: taking the heat for the big guy

“…Because of this interdependence, aphids are highly constrained to the ecological tolerances of Buchnera (Dunbar et al 2007). In the field, temperatures ranging from 25 to 308C result in pea aphids with lower densities of Buchnera (Montllor et al 2002). A recent study (Dunbar et al 2007) showed that heat tolerance of pea aphids and Buchnera could be destroyed with a single nucleotide deletion in a heat shock gene promoter.…”