Dataset Information

Match and mismatch between dietary switches and microbial partners in plant sap-feeding insects.

ABSTRACT: Some animal groups associate with the same vertically transmitted microbial symbionts over extended periods of evolutionary time, punctuated by occasional symbiont switches to different microbial taxa. Here we test the oft-repeated suggestion that symbiont switches are linked with host diet changes, focusing on hemipteran insects of the suborder Auchenorrhyncha. These insects include the only animals that feed on plant xylem sap through the life cycle, as well as taxa that feed on phloem sap and plant parenchyma cells. Ancestral state reconstruction provides strong statistical support for a xylem feeding auchenorrhynchan ancestor bearing the dual symbiosis with the primary symbiont Sulcia (Bacteroidetes) and companion symbiont '?-Sym' (?-proteobacteria). We identified seven dietary transitions from xylem feeding (six to phloem feeding, one to parenchyma feeding), but no reversions to xylem feeding; five evolutionary losses of Sulcia, including replacements by yeast symbionts, exclusively in phloem/parenchyma-feeding lineages; and 14-15 losses of ?-Sym, including nine transitions to a different bacterial companion symbiont. Our analysis indicates that, although companion symbiont switching is not associated with shifts in host diet, Sulcia is probably required for xylem-feeding. Furthermore, the ancestral auchenorrhynchan bearing Sulcia and ?-Sym probably represents the sole evolutionary origin of xylem feeding in the animal kingdom.

SUBMITTER: Bell-Roberts L

PROVIDER: S-EPMC6532509 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Match and mismatch between dietary switches and microbial partners in plant sap-feeding insects.

Bell-Roberts Louis L Douglas Angela E AE Werner Gijsbert D A GDA

Proceedings. Biological sciences 20190501 1902

Some animal groups associate with the same vertically transmitted microbial symbionts over extended periods of evolutionary time, punctuated by occasional symbiont switches to different microbial taxa. Here we test the oft-repeated suggestion that symbiont switches are linked with host diet changes, focusing on hemipteran insects of the suborder Auchenorrhyncha. These insects include the only animals that feed on plant xylem sap through the life cycle, as well as taxa that feed on phloem sap and ...[more]

PMID: 31088273

Similar Datasets

Project description:Bacterial endosymbiosis has a recurring significance in the evolution of insects. An estimated 10-20% of insect species depend on bacterial associates for their nutrition and reproductive viability. Members of the ant tribe Camponotini, the focus of this study, possess a stable, intracellular bacterial mutualist. The bacterium, Blochmannia, was first discovered in Camponotus and has since been documented in a distinct subgenus of Camponotus, Colobopsis, and in the related genus Polyrhachis. However, the distribution of Blochmannia throughout the Camponotini remains in question. Documenting the true host range of this bacterial mutualist is an important first step toward understanding the various ecological contexts in which it has evolved, and toward identifying its closest bacterial relatives. In this study, we performed a molecular screen, based on PCR amplification of 16S rDNA, to identify bacterial associates of diverse Camponotini species.Phylogenetic analyses of 16S rDNA gave four important insights: (i) Blochmannia occurs in a broad range of Camponotini genera including Calomyrmex, Echinopla, and Opisthopsis, and did not occur in outgroups related to this tribe (e.g., Notostigma). This suggests that the mutualism originated in the ancestor of the tribe Camponotini. (ii) The known bacteriocyte-associated symbionts of ants, in Formica, Plagiolepis, and the Camponotini, arose independently. (iii) Blochmannia is nestled within a diverse clade of endosymbionts of sap-feeding hemipteran insects, such as mealybugs, aphids, and psyllids. In our analyses, a group of secondary symbionts of mealybugs are the closest relatives of Blochmannia. (iv) Blochmannia has cospeciated with its known hosts, although deep divergences at the genus level remain uncertain.The Blochmannia mutualism occurs in Calomyrmex, Echinopla, and Opisthopsis, in addition to Camponotus, and probably originated in the ancestral lineage leading to the Camponotini. This significant expansion of its known host range implies that the mutualism is more ancient and ecologically diverse than previously documented. Blochmannia is most closely related to endosymbionts of sap-feeding hemipterans, which ants tend for their carbohydrate-rich honeydew. Based on phylogenetic results, we propose Camponotini might have originally acquired this bacterial mutualist through a nutritional symbiosis with other insects.

Project description:BACKGROUND:Ecological speciation is a process in which a transiently resource-polymorphic species divides into two specialized sister lineages as a result of divergent selection pressures caused by the use of multiple niches or environments. Ecology-based speciation has been studied intensively in plant-feeding insects, in which both sympatric and allopatric shifts onto novel host plants could speed up diversification. However, while numerous examples of species pairs likely to have originated by resource shifts have been found, the overall importance of ecological speciation in relation to other, non-ecological speciation modes remains unknown. Here, we apply phylogenetic information on sawflies belonging to the 'Higher' Nematinae (Hymenoptera: Tenthredinidae) to infer the frequency of niche shifts in relation to speciation events. RESULTS:Phylogenetic trees reconstructed on the basis of DNA sequence data show that the diversification of higher nematines has involved frequent shifts in larval feeding habits and in the use of plant taxa. However, the inferred number of resource shifts is considerably lower than the number of past speciation events, indicating that the majority of divergences have occurred by non-ecological allopatric speciation; based on a time-corrected analysis of sister species, we estimate that a maximum of c. 20% of lineage splits have been triggered by a change in resource use. In addition, we find that postspeciational changes in geographic distributions have led to broad sympatry in many species having identical host-plant ranges. CONCLUSION:Our analysis indicates that the importance of niche shifts for the diversification of herbivorous insects is at present implicitly and explicitly overestimated. In the case of the Higher Nematinae, employing a time correction for sister-species comparisons lowered the proportion of apparent ecology-based speciation events from c. 50-60% to around 20%, but such corrections are still lacking in other herbivore groups. The observed convergent but asynchronous shifting among dominant northern plant taxa in many higher-nematine clades, in combination with the broad overlaps in the geographic distributions of numerous nematine species occupying near-identical niches, indicates that host-plant shifts and herbivore community assembly are largely unconstrained by direct or indirect competition among species. More phylogeny-based studies on connections between niche diversification and speciation are needed across many insect taxa, especially in groups that exhibit few host shifts in relation to speciation.

Dataset Information

Match and mismatch between dietary switches and microbial partners in plant sap-feeding insects.

Publications

Match and mismatch between dietary switches and microbial partners in plant sap-feeding insects.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets