Microbiome composition within a sympatric species complex of intertidal isopods (Jaera albifrons)

Abstract

The increasingly recognised effects of microbiomes on the eco-evolutionary dynamics of their hosts are promoting a view of the “hologenome” as an integral host-symbiont evolutionary entity. For example, sex-ratio distorting reproductive parasites such as Wolbachia are well-studied pivotal drivers of invertebrate reproductive processes, and more recent work is highlighting novel effects of microbiome assemblages on host mating behaviour and developmental incompatibilities that underpin or reinforce reproductive isolation processes. However, examining the hologenome and its eco-evolutionary effects in natural populations is challenging because microbiome composition is considerably influenced by environmental factors. Here we illustrate these challenges in a sympatric species complex of intertidal isopods (Jaera albifrons spp.) with pervasive sex-ratio distortion and ecological and behavioural reproductive isolation mechanisms. We deep-sequence the bacterial 16S rRNA gene among males and females collected in spring and summer from two coasts in north-east Scotland, and examine microbiome composition with a particular focus on reproductive parasites. Microbiomes of all species were diverse (overall 3,317 unique sequences among 3.8 million reads) and comprised mainly Proteobacteria and Bacteroidetes taxa typical of the marine intertidal zone, in particular Vibrio spp. However, we found little evidence of the reproductive parasites Wolbachia, Rickettsia, Spiroplasma and Cardinium, suggesting alternative causes of sex-ratio distortion. Notwithstanding, a significant proportion of the variance in microbiome composition among samples was explained by sex (14.1 %), nested within geographic (26.9 %) and seasonal (39.6 %) variance components. The functional relevance of this sex signal was difficult to ascertain given the absence of reproductive parasites, the ephemeral nature of the species assemblages and substantial environmental variability. These results establish the Jaera albifrons species complex as an intriguing system for examining the effects of microbiomes on reproductive processes and speciation, and highlight the difficulties associated with snapshot assays of microbiome composition in dynamic and complex environments.

Female-biased sex ratios unrelated to Wolbachia infection in European species of the Jaera albifrons complex (marine isopods)

“…We conclude that Wolbachia bacteria are present in at least two species of the Jaera albifrons complex in French regions Brittany and Normandy, but most likely with a very small prevalence (both in terms of the number of individuals infected and the concentration of bacteria within infected individuals). This finding consolidates the simultaneous result obtained by Wenzel et al (2018), where bacterial 16s rDNA sequencing did not reveal any trace of Wolbachia in Scottish populations from the four European species of the Jaera albifrons complex.…”

“…Other endosymbiotic manipulators of sex (such as bacteria from groups Cardinium, Rickettsia, and Spiroplasma, or microsporidia) could be involved. In their microbiome study, (Wenzel et al, 2018) found evidence for the presence of Rickettsiacea in J. ischiosetosa females (and not in males), but in minute quantities (1.16% of the 16s sequences obtained for a sample of J. ischiosetosa females, M. Wenzel pers. comm.).…”

“…Bouchon et al (1998) found no Wolbachia in J. albifrons, but it could have been due to sampling insufficiency (three individuals were tested). Recently, Wenzel et al (2018) performed an analysis of the microbiome of the four European species of the Jaera albifrons complex using bacterial 16S rDNA sequencing in populations from Scotland. None of the bacterial 16S sequences that they identified belonged to the Wolbachia group.…”

First insights into the gut microbiomes and the diet of the Littorina snail ecotypes, a recently emerged marine evolutionary model

“…We found high bacterial diversity both in the environmental and host microbiomes, 12,566 OTUs in total. Diverse bacterial communities are associated with other marine invertebrates (Moisander et al, 2015 ; Weigel & Erwin, 2017 ; Wenzel et al, 2018 ), and this may reflect the vast diversity of marine bacteria in general (Glöckner et al, 2012 ). In the environmental samples the dominant phyla were Proteobacteria and Bacteroidetes, which is typical for marine environment (Bolhuis & Cretoiu, 2016 ; Gilbert et al, 2009 ; Wenzel et al, 2018 ).…”

Effects of Dysbiosis and Dietary Manipulation on the Digestive Microbiota of a Detritivorous Arthropod

“…For example, the increase in temperature leads to the loss of bacteria belonging to Actinobacteria in the common rough woodlouse Porcellio scaber [ 26 ]. In sympatric populations of the marine isopod Jaera albifrons the variance in the microbiota composition over a year was mainly explained by the season and to a lesser extent by sex and geographical origin [ 27 ]. The composition of the digestive microbiota of P. scaber is significantly affected by the host diet in particular by the amount of biofilms it ingests [ 28 ].…”