Abstract
The parasitoid wasp genus Nasonia (Hymenoptera: Chalcidoidea) is a well-established model organism for insect development, evolutionary genetics, speciation, and symbiosis. The host-microbiota assemblage which constitutes the Nasonia holobiont (a host together with all of its associated microbes) consists of viruses, two heritable bacterial symbionts and a bacterial community dominated in abundance by a few taxa in the gut. In the wild, all four Nasonia species are systematically infected with the obligate intracellular bacterium Wolbachia and can additionally be co-infected with Arsenophonus nasoniae. These two reproductive parasites have different transmission modes and host manipulations (cytoplasmic incompatibility vs. male-killing, respectively). Pioneering studies on Wolbachia in Nasonia demonstrated that closely related Nasonia species harbor multiple and mutually incompatible Wolbachia strains, resulting in strong symbiont-mediated reproductive barriers that evolved early in the speciation process. Moreover, research on host-symbiont interactions and speciation has recently broadened from its historical focus on heritable symbionts to the entire microbial community. In this context, each Nasonia species hosts a distinguishable community of gut bacteria that experiences a temporal succession during host development and members of this bacterial community cause strong hybrid lethality during larval development. In this review, we present the Nasonia species complex as a model system to experimentally investigate questions regarding: (i) the impact of different microbes, including (but not limited to) heritable endosymbionts, on the extended phenotype of the holobiont, (ii) the establishment and regulation of a species-specific microbiota, (iii) the role of the microbiota in speciation, and (iv) the resilience and adaptability of the microbiota in wild populations subjected to different environmental pressures. We discuss the potential for easy microbiota manipulations in Nasonia as a promising experimental approach to address these fundamental aspects.
Highlights
Bacterial symbionts are widely recognized as important drivers of insect physiology, development, behavior, reproduction, nutrition, and evolution (Buchner, 1965; Moran, 2007; Douglas, 2010, 2015)
This review highlights the important contribution Nasonia has made regarding our understanding of the manifold roles of both heritable symbionts and the general microbiota on host fitness and evolution
This, among many other advantages highlighted in this review, reinforces the Nasonia holobiont as a highly versatile and tractable model, allowing for a controlled approach to host−microbe analyses
Summary
Bacterial symbionts are widely recognized as important drivers of insect physiology, development, behavior, reproduction, nutrition, and evolution (Buchner, 1965; Moran, 2007; Douglas, 2010, 2015). Biologists recognize that symbioses are shaped by complex multipartite interactions, between the host and its associated microbes, and between different members of the microbial community and the environment. This understanding has led to the view of hosts as complex ecosystems (McFall-Ngai et al, 2013; Sicard et al, 2014), and to the recognition that a more holistic approach is needed to understand the role of the microbiota in major facets of host biology (Gilbert et al, 2012). The microbiota can mediate reproductive isolation and the mechanisms that drive speciation (Brucker and Bordenstein, 2012c, 2013; Shropshire and Bordenstein, 2016), underscoring the need to understand host−microbiota dynamics over evolutionary timescales
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