Abstract

BackgroundThe 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.ResultsUsing 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.ConclusionsThe 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.

Highlights

  • The herbivore lifestyle leads to encounters with plant toxins and requires mechanisms to overcome suboptimal nutrient availability in plant tissues

  • The plant defenses interact directly with nutrient availability by decreasing uptake or impeding digestion, myriad mechanisms have been described for how herbivores adapt to or avoid defenses [1]

  • Our results indicated that galling insects, in Phylloxeridae and among aphidomorphs, experienced increased constraints on the evolution of acid transporters (AAT) likely because of their ability to manipulate plant host metabolism

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Summary

Introduction

The herbivore lifestyle leads to encounters with plant toxins and requires mechanisms to overcome suboptimal nutrient availability in plant tissues. The plant defenses interact directly with nutrient availability by decreasing uptake (e.g., plugged sieve tubes) or impeding digestion (e.g., protease inhibitors), myriad mechanisms have been described for how herbivores adapt to or avoid defenses [1]. In addition to these deterrents, plant tissues typically maintain high carbon to nitrogen ratios, and plant fluids are depleted in many essential amino acids, making it more difficult for herbivores to acquire nitrogen-based nutrients. The transitions in and out of symbioses have left genomic signatures such as reduced genome structure and function for many obligate symbionts [3, 4], the effects of symbiosis on herbivore genomes with or without symbionts is unknown

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