Frequent Drivers, Occasional Passengers: Signals of Symbiont-Driven Seasonal Adaptation and Hitchhiking in the Pea Aphid, Acyrthosiphon pisum

Abstract

Insects harbor a variety of maternally inherited bacterial symbionts. As such, variation in symbiont presence/absence, in the combinations of harbored symbionts, and in the genotypes of harbored symbiont species provide heritable genetic variation of potential use in the insects’ adaptive repertoires. Understanding the natural importance of symbionts is challenging but studying their dynamics over time can help to elucidate the potential for such symbiont-driven insect adaptation. Toward this end, we studied the seasonal dynamics of six maternally transferred bacterial symbiont species in the multivoltine pea aphid (Acyrthosiphon pisum). Our sampling focused on six alfalfa fields in southeastern Pennsylvania, and spanned 14 timepoints within the 2012 growing season, in addition to two overwintering periods. To test and generate hypotheses on the natural relevance of these non-essential symbionts, we examined whether symbiont dynamics correlated with any of ten measured environmental variables from the 2012 growing season, including some of known importance in the lab. We found that five symbionts changed prevalence across one or both overwintering periods, and that the same five species underwent such frequency shifts across the 2012 growing season. Intriguingly, the frequencies of these dynamic symbionts showed robust correlations with a subset of our measured environmental variables. Several of these trends supported the natural relevance of lab-discovered symbiont roles, including anti-pathogen defense. For a seventh symbiont—Hamiltonella defensa—studied previously across the same study periods, we tested whether a reported correlation between prevalence and temperature stemmed not from thermally varying host-level fitness effects, but from selection on co-infecting symbionts or on aphid-encoded alleles associated with this bacterium. In general, such “hitchhiking” effects were not evident during times with strongly correlated Hamiltonella and temperature shifts. However, we did identify at least one time period in which Hamiltonella spread was likely driven by selection on a co-infecting symbiont—Rickettsiella viridis. Recognizing the broader potential for such hitchhiking, we explored selection on co-infecting symbionts as a possible driver behind the dynamics of the remaining six species. Out of twelve examined instances of symbiont dynamics unfolding across 2-week periods or overwintering spans, we found eight in which the focal symbiont underwent parallel frequency shifts under single infection and one or more co-infection contexts. This supported the idea that phenotypic variation created by the presence/absence of individual symbionts is a direct target for selection, and that symbiont effects can be robust under co-habitation with other symbionts. Contrastingly, in two cases, we found that selection may target phenotypes emerging from symbiont co-infections, with specific species combinations driving overall trends for the focal dynamic symbionts, without correlated change under single infection. Finally, in three cases—including the one described above for Hamiltonella—our data suggested that incidental co-infection with a (dis)favored symbiont could lead to large frequency shifts for “passenger” symbionts, conferring no apparent cost or benefit. Such hitchhiking has rarely been studied in heritable symbiont systems. We propose that it is more common than appreciated, given the widespread nature of maternally inherited bacteria, and the frequency of multi-species symbiotic communities across insects.

WhyWolbachia-induced cytoplasmic incompatibility is so common

“…Comparable spatial and temporal frequency variation is observed for non-CI-causing, non- Wolbachia endosymbionts that are condition-dependent mutualists (e.g., see refs. 94 and 95 ). As discussed below, data from non-CI-causing facultative endosymbionts, whether Wolbachia or not, serve as controls for our predictions concerning clade-selection advantages of CI.…”

Floral presence and flower identity alter cereal aphid endosymbiont communities on adjacent crops

“…The impact of protective bacterial symbionts on plant-insect food webs, the regulation of aphid populations, and predator-prey dynamics is only beginning to be considered (McLean et al 2016;Simon, Biere & Sugio 2017;Preedy et al 2020;Carpenter et al 2021;Leclair et al 2021). It was previously shown that as plant species richness increased along a gradient (1-4 species, created as mixed plant communities from a pool of 20), so did the number and diversity of aphid symbionts identified in three aphid species (each exclusively feeding on a different host plant) in a long-term grassland experiment .…”

“…Co-hosting symbionts can alter associated fitness costs (Zytynska, Tighiouart & Frago 2021), which can reduce aphid population growth rates or transmission of symbionts to the next generation (Rock et al 2018). Additionally, the presence of multiple different symbiont combinations in the aphid population could alter competition among natural enemies (McLean & Godfray 2017), and as these selection pressures alter symbiont infection frequencies over time (Carpenter et al 2021;Smith et al 2021) this can further affect outcomes of hosting different symbiont combinations. Some symbionts may also be present due to non-natural enemy factors (host-plant or temperature mediated selection), leading to a strong contextdependency effect on interaction outcomes (Lemoine, Engl & Kaltenpoth 2020).…”

Dynamic changes in species richness and community diversity of symbiotic bacteria in five reproductive morphs of cotton aphid Aphis gossypii Glover (Hemiptera: Aphididae)

“…It is precisely because PI Wolbachia symbiosis caused their parthenogenesis (Stouthamer et al, 1990;Russell and Stouthamer, 2011). The presence or absence of environmental stressors and bacteria may affect phenotypes (reproductive 10.3389/fmicb.2022.1086728 Frontiers in Microbiology 03 frontiersin.org strategies and morphological characteristics; Reyes et al, 2019;Carpenter et al, 2021). When Acyrthosiphon pisum was exposed to the aphid alarm pheromone (E) -β-farnesene (EBF), aphids with defense against Hamilton or Serratia symbiotic infection increased reproduction (Barribeau et al, 2010).…”