Codivergence of the primary bacterial endosymbiont of psyllids versus host switches and replacement of their secondary bacterial endosymbionts

Abstract

Coevolution between insects and bacterial endosymbionts contributes to the success of many insect lineages. For the first time, we tested for phylogenetic codivergence across multiple taxonomic scales, from within genera to superfamily between 36 psyllid species of seven recognised families (Hemiptera: Psylloidea), their exclusive primary endosymbiont Carsonella and more diverse secondary endosymbionts (S-endosymbionts). Within Aphalaridae, we found that Carsonella and S-endosymbionts were fixed in one Glycaspis and 12 Cardiaspina populations. The dominant S-endosymbiont was Arsenophonus, while Sodalis was detected in one Cardiaspina species. We demonstrated vertical transmission for Carsonella and Arsenophonus in three Cardiaspina species. We found strong support for strict cospeciation and validated the informative content of Carsonella as extended host genome for inference of psyllid relationships. However, S-endosymbiont and host phylogenies were incongruent, and displayed signs of host switching and endosymbiont replacement. The high incidence of Arsenophonus in psyllids and other plant sap-feeding Hemiptera may be due to repeated host switching within this group. In two psyllid lineages, Arsenophonus and Sodalis genes exhibited accelerated evolutionary rates and AT-biases characteristic of long-term host associations. Together with strict vertical transmission and 100% prevalence within host populations, our results suggest an obligate, and not facultative, symbiosis between psyllids and some S-endosymbionts.

Unravelling mummies: cryptic diversity, host specificity, trophic and coevolutionary interactions in psyllid – parasitoid food webs

“…that has not been assigned to any known species due to its new host tree association [35]. However, DNA characterisation suggested that GB Cardiaspina sp., C. densitexta and C. tenuitela are either a single species or a complex of closely related sibling species [43]. The four major parasitoid morphospecies, consisting of three Psyllaephagus morphospecies and Co. psyllae , were present and abundant in most psyllid populations, including one Psyllaephagus morphospecies (P1) that was present in all psyllid populations.…”

“…According to adult and lerp (protective covers excreted by nymphs) morphology, host tree association and DNA characterisation, Cardiaspina populations were assigned to six species ( C. albitextura Taylor, C. densitexta Taylor, C. fiscella Taylor, C. maniformis Taylor, C. tenuitela Taylor and C. vittaformis Froggatt) that represent a phylogenetically broad diversity [43] of 24 known species of the genus Cardiaspina [23]. Cardiaspina from Eucalyptus moluccana Roxb.…”

“…and uncertain species status [35]. First morphological identification placed it near C. densitexta [34] but molecular evidence did not unequivocally support this and clustered this species with both C. densitexta and C. tenuitela , two species feeding on other box eucalypts [43]. For the Spondyliaspis sp.…”

“…Both host and parasitoid phylogenies were rooted with the most distantly related species according to p-distances. As different approaches exist for cophylogenetic analyses [56], we employed three current methods that have recently also been successfully applied to test codivergence and host switching of bacterial endosymbionts and their psyllid hosts [43]: phylogenetic topology-based TreeMap 3 [57], and the two phylogenetic distance-based methods, ParaFit [58] and Hommola’s cospeciation test (hereafter HCT) [59]. Briefly, TreeMap 3 was used to reconstruct tanglegrams and to assess congruence between host and parasitoid phylogenies.…”

Symbionts in waiting: the dynamics of incipient endosymbiont complementation and replacement in minimal bacterial communities of psyllids

“…Endosymbiosis can result in genome size reduction of bacterial symbionts and their loss of function [1], requiring complementation or replacement by other endosymbionts [2, 3]. Prior to this, host switches and acquisition of endosymbionts must occur, but these processes have not been studied for entire bacterial communities across many host species.…”