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Plant manipulation through gall formation constrains amino acid transporter evolution in sap-feeding insects.

ABSTRACT: The herbivore lifestyle leads to encounters with plant toxins and requires mechanisms to overcome suboptimal nutrient availability in plant tissues. Although the evolution of bacterial endosymbiosis alleviated many of these challenges, the ability to manipulate plant nutrient status has evolved in lineages with and without nutritional symbionts. Whether and how these alternative nutrient acquisition strategies interact or constrain insect evolution is unknown. We studied the transcriptomes of galling and free-living aphidomorphs to characterize how amino acid transporter evolution is influenced by the ability to manipulate plant resource availability.Using a comparative approach we found phylloxerids retain nearly all amino acid transporters as other aphidomorphs, despite loss of nutritional endosymbiosis. Free living species show more transporters than galling species within the same genus, family, or infraorder, indicating plant hosts influence the maintenance and evolution of nutrient transport within herbivores. Transcript profiles also show lineage specificity and suggest some genes may facilitate life without endosymbionts or the galling lifestyle.The transcript abundance profiles we document across fluid feeding herbivores support plant host constraint on insect amino acid transporter evolution. Given amino acid uptake, transport, and catabolism underlie the success of herbivory as a life history strategy, this suggests that plant host nutrient quality, whether constitutive or induced, alters the selective environment surrounding the evolution and maintenance of endosymbiosis.

SUBMITTER: Zhao C

PROVIDER: S-EPMC5488444 | biostudies-literature | 2017 Jun

REPOSITORIES: biostudies-literature

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Plant manipulation through gall formation constrains amino acid transporter evolution in sap-feeding insects.

Zhao Chaoyang C Nabity Paul D PD

BMC evolutionary biology 20170627 1

<h4>Background</h4>The herbivore lifestyle leads to encounters with plant toxins and requires mechanisms to overcome suboptimal nutrient availability in plant tissues. Although the evolution of bacterial endosymbiosis alleviated many of these challenges, the ability to manipulate plant nutrient status has evolved in lineages with and without nutritional symbionts. Whether and how these alternative nutrient acquisition strategies interact or constrain insect evolution is unknown. We studied the t ...[more]

PMID: 28655293

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Project description:The dynamics of occurrence of target organs in plant populations produces windows of opportunity that directly and indirectly affect the structure of herbivore communities. However, mechanisms that drive herbivore specialization between resource patches are still poorly known. In this study, we tested three hypotheses related to variation in host plant phenology and community structure (i.e., composition, richness, and abundance) of gall-forming species: (a) plants with early leaf-flushing in the season will have greater vegetative growth and high contents of secondary chemical compounds; (b) gall-inducing insect community structure changes among temporary resource patches of the host; and (c) interspecific competition is a probable mechanism that drives gall-inducing insect community structure on Copaifera langsdorffii. We monitored daily a total of 102 individuals of the super-host C. langsdorffii from August 2012 to May 2013, to characterize the leaf flushing time of each host plant. The leaf flushing time had a positive relationship with the number of folioles per branch and a negative relationship with branch growth. We sampled a total of 4,906 galls belonging to 24 gall-inducing insect species from 102 individuals of C. langsdorffii. In spite of some gall-inducing species presented high abundance on early leaf-flushing plants, direct and indirect effects of plant phenology on galling insect abundance was species dependent. At the community level, our study revealed that the quality and quantity of plant resources did not affect the richness and abundance of gall-inducing insects associated with C. langsdorffii. However, the richness and composition of gall-inducing species varied according to the variation in leaf flushing time of the host plant. The results of null model analysis showed that galls co-occurrence on C. langsdorffii trees differ more than expected by chance and that interspecific competition can be one potential mechanism structuring this gall-inducing insect community.

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.

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Plant manipulation through gall formation constrains amino acid transporter evolution in sap-feeding insects.

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Plant manipulation through gall formation constrains amino acid transporter evolution in sap-feeding insects.

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