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

Abstract

Virtually all higher organisms form holobionts with associated microbiota. To understand the biology of holobionts we need to know how species assemble and interact. Controlled experiments are suited to study interactions between particular symbionts, but they only accommodate a tiny portion of the diversity within each species. Alternatively, interactions can be inferred by testing if associations among symbionts in the field are more or less frequent than expected under random assortment. However, random assortment may not be a valid null hypothesis for maternally transmitted symbionts since drift alone can result in associations. Here, we analyse a European field survey of endosymbionts in pea aphids (Acyrthosiphon pisum), confirming that symbiont associations are pervasive. To interpret them, we develop a model simulating the effect of drift on symbiont associations. We show that drift induces apparently nonrandom assortment, even though horizontal transmissions and maternal transmission failures tend to randomise symbiont associations. We also use this model in the approximate Bayesian computation framework to revisit the association between Spiroplasma and Wolbachia in Drosophila neotestacea. New field data reported here reveal that this association has disappeared in the investigated location, yet a significant interaction between Spiroplasma and Wolbachia can still be inferred. Our study confirms that negative and positive associations are pervasive and often induced by symbiont‐symbiont interactions. Nevertheless, some associations are also likely to be driven by drift. This possibility needs to be considered when performing such analyses, and our model is helpful for this purpose.

Cohabitation and roommate bias of symbiotic bacteria in insect hosts

“…than alfalfa ( M. sativa ). Consistent associations across the data set included a negative association between H. defensa and R. insecticola and a positive one between H. defensa and X‐type (previously identified, reviewed in Mathé‐Hubert et al, ; Zytynska & Weisser, ). The majority of negative associations occurred among the more abundant symbionts, leading to a negative correlation between the prevalence of a particular symbiont and the number of coinfecting symbionts to be greater than expected under random assortment.…”

“…For example, Spiroplasma from clade 2 was more frequent in aphids that cohosted other symbionts, and clade 3 Spiroplasma was less frequent if the aphid cohosted H. defensa . This highlights the necessity to consider the co‐occurrence of aphid and symbiont genotypes as well as variation across host species, and can also inform on rates of horizontal transmission as suggested by Mathé‐Hubert et al (). While this is not a new idea (Ferrari & Vavre, ), we now have the knowledge and ability to design field experiments to transfer theoretical and controlled experimental work to realistic systems.…”

“…The building evidence that host‐symbiont dynamics are strongly influenced by maternal and horizontal transmission rates, host and symbiont genetic variation, and the wider interacting community, highlights the need to focus efforts on combining laboratory experimental work with field studies. One step forward is provided by Mathé‐Hubert et al () in this issue of Molecular Ecology . These authors explore the role of drift and symbiont‐symbiont interactions to explain associations between various symbiont species in field populations.…”

“…Mathé‐Hubert et al () analysed a European data set on symbiont occurrence from 498 pea aphids ( Acyrthosiphon pisum ), identifying seven symbiont species: Hamiltonella defensa , Regiella insecticola , Serratia symbiotica , Rickettsia , Rickettsiella , Spiroplasma and X‐type (now Fukatsuia symbiotica ). They found similar average numbers of symbionts within aphids collected from two different host plant species (0.97 symbionts per aphid on Trifolium spp.…”

“…The second part of the study by Mathé‐Hubert et al () focused on the within‐species variation of the Spiroplasma symbiont. They identified three main genetic clades (clusters) to show that while there was no variation in strain frequency across host plant species, the frequency of these clades varied strongly due to the presence of other symbionts.…”