Endosymbiont Phylogenesis in the Dryophthoridae Weevils: Evidence for Bacterial Replacement

Abstract

Intracellular symbiosis is widespread in the insect world where it plays an important role in evolution and adaptation. The weevil family Dryophthoridae (Curculionoidea) is of particular interest in intracellular symbiosis evolution with regard to the great economical and ecological features of these invasive insects, and the potential for comparative studies across a wide range of host plants and environments. Here, we have analyzed the intracellular symbiotic bacteria of 19 Dryophthoridae species collected worldwide, representing a wide range of plant species and tissues. All except one (Sitophilus linearis) harbor symbiotic bacteria within specialized cells (the bacteriocytes) assembled as an organ, the bacteriome. Phylogenetic analysis of the 16S rDNA gene sequence of the Dryophthoridae endosymbionts revealed three endosymbiotic clades belonging to gamma3-Proteobacteria and characterized by different GC contents and evolutionary rate. The genus name Candidatus Nardonella was proposed for the ancestral clade infesting Dryophthoridae 100 MYA and represented by five of nine bacterial genera studied. For this clade showing low GC content (40.5% GC) and high evolutionary rate (0.128 substitutions/site per 100 Myr), a single infection and subsequent cospeciation of the host and the endosymbionts was observed. In the two other insect lineage endosymbionts, with relatively high GC content (53.4% and 53.8% GC), competition with ancestral pathogenic bacteria might have occurred, leading to endosymbiont replacement in present-day last insects.

Diversification of endosymbiosis: replacements, co-speciation and promiscuity of bacteriocyte symbionts in weevils

“…Based on these results, we conclude that Curculioniphilus comprises the primary symbiont clade associated with the Curculionini weevils. As Nardonella is the ancestral primary symbiont of weevils (Lefèvre et al, 2004;Conord et al, 2008), it is conjectured that Curculioniphilus was acquired by the common ancestor of the Curculionini weevils and took over the original symbiont. 1.00…”

“…The bacteriocyte-associated Nardonella symbionts are found from diverse weevil subfamilies including the Dryophthorinae and the Molytinae, have strictly co-speciated with their hosts for over 125 million years, and exhibit highly AT-biased nucleotide compositions and accelerated molecular evolution that are typical of ancient insect symbionts of obligate nature (Lefèvre et al, 2004;Conord et al, 2008;Hosokawa and Fukatsu, 2010). On the other hand, the bacteriocyte-associated Sodalis-allied symbionts are restricted to a few grain weevil species of the genus Sitophilus (Heddi and Nardon, 2005), and the bacteriocyte-associated Curculioniphilus symbionts were recently described from several seed-infesting weevils of the genus Curculio (Toju et al, 2010).…”

Swapping symbionts in spittlebugs: evolutionary replacement of a reduced genome symbiont

“…But, as a result of host-symbiont coadaptation, symbiont cells are intimately involved in host development (for example, Braendle et al, 2003;Koga et al, 2012) such that their sudden removal causes lethal developmental disruption. Nonetheless, several cases are known in which an insect host lineage has acquired a new symbiont, which has entirely replaced an ancestral one (for example, Lefèvre et al, 2004;Conord et al, 2008;Toenshoff et al, 2012;Toju et al, 2013) or has persisted along with the ancestral symbiont while assuming a subset of its functions (for example, Lamelas et al, 2011).…”

Antimicrobial peptides and cell processes tracking endosymbiont dynamics

“…Candidatus Nardonella would be the ancestral symbiont (125 million years (Myr) of this superfamily and occurs in at least eight studied genera [24]. Candidatus Sodalis pierantonius symbiosis with the cereal weevils of the genus Sitophilus spp.…”

“…Candidatus Sodalis pierantonius symbiosis with the cereal weevils of the genus Sitophilus spp. is hypothesized to have been established recently (less than 1 Myr) [26], probably following Candidatus Nardonella's displacement [24,26,27]. Owing to its recent association as a symbiont, S. pierantonius is a valuable model for studying the early steps of insect endosymbiogenesis, in that its genome has not suffered any drastic size reduction [28 -30].…”