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

Abstract

The processes and mechanisms underlying the diversification of host-microbe endosymbiotic associations are of evolutionary interest. Here we investigated the bacteriocyte-associated primary symbionts of weevils wherein the ancient symbiont Nardonella has experienced two independent replacement events: once by Curculioniphilus symbiont in the lineage of Curculio and allied weevils of the tribe Curculionini, and once by Sodalis-allied symbiont in the lineage of grain weevils of the genus Sitophilus. The Curculioniphilus symbiont was detected from 27 of 36 Curculionini species examined, the symbiont phylogeny was congruent with the host weevil phylogeny, and the symbiont gene sequences exhibited AT-biased nucleotide compositions and accelerated molecular evolution. These results suggest that the Curculioniphilus symbiont was acquired by an ancestor of the tribe Curculionini, replaced the original symbiont Nardonella, and has co-speciated with the host weevils over evolutionary time, but has been occasionally lost in several host lineages. By contrast, the Sodalis-allied symbiont of Sitophilus weevils exhibited no host-symbiont co-speciation, no AT-biased nucleotide compositions and only moderately accelerated molecular evolution. These results suggest that the Sodalis-allied symbiont was certainly acquired by an ancestor of the Sitophilus weevils and replaced the original Nardonella symbiont, but the symbiotic association must have experienced occasional re-associations such as new acquisitions, horizontal transfers, replacements and/or losses. We detected Sodalis-allied facultative symbionts in populations of the Curculionini weevils, which might represent potential evolutionary sources of the Sodalis-allied primary symbionts. Comparison of these newcomer bacteriocyte-associated symbiont lineages highlights potential evolutionary trajectories and consequences of novel symbionts after independent replacements of the same ancient symbiont.

Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

“…Parallel cases of symbiont-driven ecological expansion have been documented in other insects, including cockroaches (15,16), ants (17), lice (18), and beetles (19)(20)(21). Examples extend into other animal hosts although, in some, transmission may be partly or wholly horizontal rather than strictly vertical.…”

Small genome symbiont underlies cuticle hardness in beetles

“…While the Nardonella symbionts have been conserved among diverse weevils and cospeciated with the weevil hosts for over 100 My (23)(24)(25)(26)(27)(28)(29)(30)(31), previous studies have identified a number of weevil lineages in which the Nardonella symbiont had been either lost or replaced by novel bacterial symbionts (23,24,(32)(33)(34)(35). The extremely reduced Nardonella genome down to 0.2 Mb (Fig.…”

“…Despite the longlasting host-symbiont coevolution, Nardonella's biological role has been poorly understood (26). Previous studies have identified a number of weevil lineages in which Nardonella infections have been lost or replaced by different bacterial lineages, uncovering a strikingly dynamic aspect of the endosymbiotic evolution in the insect group (23,24,(32)(33)(34)(35).…”

Symbiosis as a General Principle in Eukaryotic Evolution

“…In certain instances, evolutionary change may be facilitated by among-microbe transfer of symbiosis-related gene clusters via "symbiosis islands" (Finan 2002), equivalent to pathogenicity islands in pathogenic bacteria, or by the displacement of one microbial partner by another taxon with different traits (Koga et al 2013;Toju et al 2013). With the dramatically improving genomic technologies, it is becoming increasingly feasible to answer these fundamental questions.…”