Social behaviour in bees influences the abundance of Sodalis (Enterobacteriaceae) symbionts

Abstract

Social interactions can facilitate transmission of microbes between individuals, reducing variation in gut communities within social groups. Thus, the evolution of social behaviours and symbiont community composition have the potential to be tightly linked. We explored this connection by characterizing the diversity of bacteria associated with both eusocial and solitary bee species within the behaviourally variable family Halictidae using 16S amplicon sequencing. Contrary to expectations, we found few differences in bacterial abundance or variation between social forms; most halictid species appear to share similar gut bacterial communities. However, several strains of Sodalis, a genus described as a symbiont in a variety of insects but yet to be characterized in bees, differ in abundance between eusocial and solitary bees. Phylogenetic reconstructions based on whole-genome alignments indicate that Sodalis has independently colonized halictids at least three times. These strains appear to be mutually exclusive within individual bees, although they are not host-species-specific and no signatures of vertical transmission were observed, suggesting that Sodalis strains compete for access to hosts. The symbiosis between halictids and Sodalis therefore appears to be in its early stages.

Keywords: Halictidae; Sodalis; eusociality; microbiome; sweat bees; symbiosis.

Figure 1.

(a). Collecting sites for all specimens used for 16S rRNA gene sequencing, number of total specimens from each site, and proportions of those samples classified as each behavioural type. (b) Phylogeny of halictid species sampled in this study based on the time-calibrated phylogeny from [33]. Social behaviour is indicated by colours.

Figure 2.

Principal coordinates analysis plots of all halictid samples examined in the current study. MidiP, Midi-Pyrénées; PACA, Provence-Alpes-Côte d'Azur. The most frequently represented geographical regions and species are indicated and others are grouped together. Individual plots represent the use of different beta diversity metrics (weighted and unweighted Jaccard).

Figure 3.

(a) Topology showing evolutionary relationships of the three Sodalis lineages identified in this study (SAL1, SAL2, SLEU), three previously sequenced Sodalis genomes (So. praecaptivus, So. glossinidius, So. pierantonius), and several free-living (host: ‘none’) taxa as out-groups. Bolded taxa are symbionts of insects. Boxplots show genome-wide distributions of dN/dS values. dN/dS ratios of Sodalis symbionts were compared to So. praecaptivus using Wilcoxon rank-sum tests and significant differences are shown with asterisks. (b) Proportions of reads originating from the two Sodalis lineages SAL1 and SAL2 in shotgun sequencing data for 36 L. albipes specimens. Samples are separated by populations of origin shown by maps.