Context‐dependent vertical transmission shapes strong endosymbiont community structure in the pea aphid, Acyrthosiphon pisum

Abstract

Animal-associated microbiomes are often comprised of structured, multispecies communities, with particular microbes showing trends of co-occurrence or exclusion. Such structure suggests variable community stability, or variable costs and benefits-possibilities with implications for symbiont-driven host adaptation. In this study, we performed systematic screening for maternally transmitted, facultative endosymbionts of the pea aphid, Acyrthosiphon pisum. Sampling across six locales, with up to 5 years of collection in each, netted significant and consistent trends of community structure. Co-infections between Serratia symbiotica and Rickettsiella viridis were more common than expected, while Rickettsia and X-type symbionts colonized aphids with Hamiltonella defensa more often than expected. Spiroplasma co-infected with other endosymbionts quite rarely, showing tendencies to colonize as a single species monoculture. Field estimates of maternal transmission rates help to explain our findings: while Serratia and Rickettsiella improved each other's transmission, Spiroplasma reduced transmission rates of co-infecting endosymbionts. In summary, our findings show that North American pea aphids harbour recurring combinations of facultative endosymbionts. Common symbiont partners play distinct roles in pea aphid biology, suggesting the creation of "generalist" aphids receiving symbiont-based defence against multiple ecological stressors. Multimodal selection, at the host level, may thus partially explain our results. But more conclusively, our findings show that within-host microbe interactions, and their resulting impacts on transmission rates, are an important determinant of community structure. Widespread distributions of heritable symbionts across plants and invertebrates hint at the far-reaching implications for these findings, and our work further shows the benefits of symbiosis research within a natural context.

Metacommunity theory for transmission of heritable symbionts within insect communities

“…McLean et al () found stable coinfections to be possible between multiple combinations of different aphid symbionts and even between multiple strains of the same symbiont, H. defensa . Similarly, in a long‐term study of aphid symbiont communities, Rock et al () found that the bacteria Serratia symbiotica and Rickettsiella viridis co‐occurred more often than expected, a phenomenon that was explained by their ability to promote each other's transmission to the next host generation. Wolbachia is also positively associated with Spiroplasma within Drosophila neotestacea (Fromont, Adair, & Douglas, ).…”

Nonrandom associations of maternally transmitted symbionts in insects: The roles of drift versus biased cotransmission and selection

“…Ne F , effective female population size; M T , maternal transmission rate; H T , horizontal transmission rate. The blue square highlights the range of parameters values that is likely to include the symbionts of D. neotestacea while the dotted purple one is likely to include those of the pea aphid (Chen & Purcell, ; Moran & Dunbar, ; Peccoud et al, ; Rock et al, ). (c) Example of simulation where drift created a strong positive association.…”

Editorial 2019

“…The second section featured a number of manuscripts that investigated the structure of the microbiome in an attempt to understand the drivers of microbiota community assembly and turnover. Some contributions weighed in on the role of host phylogeny vs. ecology (Erlandson, Savage, Wei, Cavender‐Bares, & Peay, ; Ivens, Gadau, Kiers, & Kronauer, 2018; Hernandez‐Gomez, Briggler, & Williams, ; Kohl, Dearing, & Bordenstein, ; Nishida & Ochman, ; Roth‐Schulze et al., ; Schuelke, Pereira, Hardy, & Bik, ), others probed how the presence of hosts themselves alters the microbiota around them (Chen & Parfrey, ; Shukla, Vogel, Heckel, Vilcinskas, & Kaltenpoth, ), one investigated patterns of co‐infection (Rock et al, ) and one documented changes in microbiota during development (Prest, Kimball, Kueneman, & McKenzie, ). A few studies in this section studied the structure of the microbiome with manipulative experiments (e.g., Chen & Parfrey, ; Erlandson et al, ; Morella, Gomez, Wang, Leung, & Koskella, ; Raymann, Bobay, & Moran, ).…”