Abstract

BackgroundMutualistic obligate endosymbioses shape the evolution of endosymbiont genomes, but their impact on host genomes remains unclear. Insects of the sub-order Sternorrhyncha (Hemiptera) depend on bacterial endosymbionts for essential amino acids present at low abundances in their phloem-based diet. This obligate dependency has been proposed to explain why multiple amino acid transporter genes are maintained in the genomes of the insect hosts. We implemented phylogenetic comparative methods to test whether amino acid transporters have proliferated in sternorrhynchan genomes at rates grater than expected by chance.ResultsBy applying a series of methods to reconcile gene and species trees, inferring the size of gene families in ancestral lineages, and simulating the null process of birth and death in multi-gene families, we uncovered a 10-fold increase in duplication rate in the AAAP family of amino acid transporters within Sternorrhyncha. This gene family expansion was unmatched in other closely related clades lacking endosymbionts that provide essential amino acids.ConclusionsOur findings support the influence of obligate endosymbioses on host genome evolution by both inferring significant expansions of gene families involved in symbiotic interactions, and discovering increases in the rate of duplication associated with multiple emergences of obligate symbiosis in Sternorrhyncha.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0315-3) contains supplementary material, which is available to authorized users.

Highlights

  • Mutualistic obligate endosymbioses shape the evolution of endosymbiont genomes, but their impact on host genomes remains unclear

  • These results provide strong support for our hypothesis that expansions of amino acid transporters were favored in sap-feeding sternorrhynchan lineages relying on endosymbiosis for essential amino acid provisioning

  • Transcriptomic analyses show that sternorrhynchans with amino acidprovisioning symbionts have amino acid transporter paralogs expressed at their symbiotic interface, supporting a role for host paralogs in nutritional symbiosis [10]. These observations, combined with formal statistical tests for deviation from a neutral birth-death model, support the hypothesis that selection maintains amino acid transporter paralogs in sternorrhynchan insections By demonstrating that amino acid transporter gene families underwent expansions in this sub-order, our results provide further evidence for the selective maintenance of amino acid transporter paralogs of the auxin permease transporters (AAAP), and perhaps acid polyamine organocation transporters (APC), gene families in sternorrhynchan insections We propose that selection arises from evolutionary constraints for novel transporters with specialized roles in mediating symbiotic amino acid exchange

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Summary

Introduction

Mutualistic obligate endosymbioses shape the evolution of endosymbiont genomes, but their impact on host genomes remains unclear. Insects of the sub-order Sternorrhyncha (Hemiptera) depend on bacterial endosymbionts for essential amino acids present at low abundances in their phloem-based diet. This obligate dependency has been proposed to explain why multiple amino acid transporter genes are maintained in the genomes of the insect hosts. Nutritional symbioses are found in blood-feeding insects such as the kissing bug, Rhodnius prolixus, and the human body louse, Pediculus humanus. These blood-feeders obtain vitamins from their bacterial symbionts [5,6,7].

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