Inheritance patterns of secondary symbionts during sexual reproduction of pea aphid biotypes

Herbivorous insects frequently harbor bacterial symbionts that affect their ecology and evolution. Aphids host the obligatory endosymbiont Buchnera, which is required for reproduction, together with facultative symbionts whose frequencies vary across aphid populations. These maternally transmitted secondary symbionts have been particularly studied in the pea aphid, Acyrthosiphon pisum, which harbors at least 8 distinct bacterial species (not counting Buchnera) having environmentally dependent effects on host fitness. In particular, these symbiont species are associated with pea aphid populations feeding on specific plants. Although they are maternally inherited, these bacteria are occasionally transferred across insect lineages. One mechanism of such nonmaternal transfer is paternal transmission to the progeny during sexual reproduction. To date, transmission of secondary symbionts during sexual reproduction of aphids has been investigated in only a handful of aphid lineages and 3 symbiont species. To better characterize this process, we investigated inheritance patterns of 7 symbiont species during sexual reproduction of pea aphids through a crossing experiment involving 49 clones belonging to 9 host-specialized biotypes, and 117 crosses. Symbiont species in the progeny were detected with diagnostic qualitative PCR at the fundatrix stage hatching from eggs and in later parthenogenetic generations. We found no confirmed case of paternal transmission of symbionts to the progeny, and we observed that maternal transmission of a particular symbiont species (Serratia symbiotica) was quite inefficient. We discuss these observations in respect to the ecology of the pea aphid.