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,
- NSF-PAR ID:
- 10337234
- Date Published:
- Journal Name:
- Insects
- Volume:
- 12
- Issue:
- 9
- ISSN:
- 2075-4450
- Page Range / eLocation ID:
- 805
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract 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 betweenSerratia symbiotica andRickettsiella viridis were more common than expected, whileRickettsia and X‐type symbionts colonized aphids withHamiltonella 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: whileSerratia andRickettsiella 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. -
ABSTRACT Animal-associated microbes are highly variable, contributing to a diverse set of symbiont-mediated phenotypes. Given that host and symbiont genotypes, and their interactions, can impact symbiont-based phenotypes across environments, there is potential for extensive variation in fitness outcomes. Pea aphids, Acyrthosiphon pisum , host a diverse assemblage of heritable facultative symbionts (HFS) with characterized roles in host defense. Protective phenotypes have been largely studied as single infections, but pea aphids often carry multiple HFS species, and particular combinations may be enriched or depleted compared to expectations based on chance. Here, we examined the consequences of single infection versus coinfection with two common HFS exhibiting variable enrichment, the antiparasitoid Hamiltonella defensa and the antipathogen Regiella insecticola , across three host genotypes and environments. As expected, single infections with either H. defensa or R. insecticola raised defenses against their respective targets. Single infections with protective H. defensa lowered aphid fitness in the absence of enemy challenge, while R. insecticola was comparatively benign. However, as a coinfection, R. insecticola ameliorated H. defensa infection costs. Coinfected aphids continued to receive antiparasitoid protection from H. defensa , but protection was weakened by R. insecticola in two clones. Notably, H. defensa eliminated survival benefits conferred after pathogen exposure by coinfecting R. insecticola . Since pathogen sporulation was suppressed by R. insecticola in coinfected aphids, the poor performance likely stemmed from H. defensa -imposed costs rather than weakened defenses. Our results reveal a complex set of coinfection outcomes which may partially explain natural infection patterns and suggest that symbiont-based phenotypes may not be easily predicted based solely on infection status. IMPORTANCE The hyperdiverse arthropods often harbor maternally transmitted bacteria that protect against natural enemies. In many species, low-diversity communities of heritable symbionts are common, providing opportunities for cooperation and conflict among symbionts, which can impact the defensive services rendered. Using the pea aphid, a model for defensive symbiosis, we show that coinfections with two common defensive symbionts, the antipathogen Regiella and the antiparasite Hamiltonella , produce outcomes that are highly variable compared to single infections, which consistently protect against designated enemies. Compared to single infections, coinfections often reduced defensive services during enemy challenge yet improved aphid fitness in the absence of enemies. Thus, infection with multiple symbionts does not necessarily create generalist aphids with “Swiss army knife” defenses against numerous enemies. Instead, particular combinations of symbionts may be favored for a variety of reasons, including their abilities to lessen the costs of other defensive symbionts when enemies are not present.more » « less
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Abstract Facultative, heritable endosymbionts are found at intermediate prevalence within most insect species, playing frequent roles in their hosts’ defence against environmental pressures. Focusing on
Hamiltonella defensa , a common bacterial endosymbiont of aphids, we tested the hypothesis that such pressures impose seasonal balancing selection, shaping a widespread infection polymorphism. In our studied pea aphid (Acyrthosiphon pisum ) population,Hamiltonella frequencies ranged from 23.2% to 68.1% across a six‐month longitudinal survey. Rapid spikes and declines were often consistent across fields, and we estimated that selection coefficients forHamiltonella ‐infected aphids changed sign within this field season. Prior laboratory research suggested antiparasitoid defence as the majorHamiltonella benefit, and costs under parasitoid absence. While a prior field study suggested these forces can sometimes act as counter‐weights in a regime of seasonal balancing selection, our present survey showed no significant relationship between parasitoid wasps andHamiltonella prevalence. Field cage experiments provided some explanation: parasitoids drove modest ~10% boosts toHamiltonella frequencies that would be hard to detect under less controlled conditions. They also showed thatHamiltonella was not always costly under parasitoid exclusion, contradicting another prediction. Instead, our longitudinal survey – and two overwintering studies – showed temperature to be the strongest predictor ofHamiltonella prevalence. Matching some prior lab discoveries, this suggested that thermally sensitive costs and benefits, unrelated to parasitism, can shapeHamiltonella dynamics. These results add to a growing body of evidence for rapid, seasonal adaptation in multivoltine organisms, suggesting that such adaptation can be mediated through the diverse impacts of heritable bacterial endosymbionts. -
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Abstract Most insects harbour influential, yet non‐essential heritable microbes in their hemocoel. Communities of these symbionts exhibit low diversity. But their frequent multi‐species nature raises intriguing questions on roles for symbiont–symbiont synergies in host adaptation, and on the stability of the symbiont communities, themselves. In this study, we build on knowledge of species‐defined symbiont community structure across US populations of the pea aphid,
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Abstract Insects often harbour heritable symbionts that provide defence against specialized natural enemies, yet little is known about symbiont protection when hosts face simultaneous threats. In pea aphids (
Acyrthosiphon pisum ), the facultative endosymbiontHamiltonella defensa confers protection against the parasitoid,Aphidius ervi , andRegiella insecticola protects against aphid‐specific fungal pathogens, includingPandora neoaphidis . Here, we investigated whether these two common aphid symbionts protect against a specialized virusA .pisum virus (APV), and whether their antifungal and antiparasitoid services are impacted by APV infection. We found that APV imposed large fitness costs on symbiont‐free aphids and these costs were elevated in aphids also housingH .defensa . In contrast, APV titres were significantly reduced and costs to APV infection were largely eliminated in aphids withR .insecticola . To our knowledge,R .insecticola is the first aphid symbiont shown to protect against a viral pathogen, and only the second arthropod symbiont reported to do so. In contrast, APV infection did not impact the protective services of eitherR .insecticola orH .defensa . To better understand APV biology, we produced five genomes and examined transmission routes. We found that moderate rates of vertical transmission, combined with horizontal transfer through food plants, were the major route of APV spread, although lateral transfer by parasitoids also occurred. Transmission was unaffected by facultative symbionts. In summary, the presence and species identity of facultative symbionts resulted in highly divergent outcomes for aphids infected with APV, while not impacting defensive services that target other enemies. These findings add to the diverse phenotypes conferred by aphid symbionts, and to the growing body of work highlighting extensive variation in symbiont‐mediated interactions.
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/insects12090805
