Facultative symbiont infections affect aphid reproduction.

Jean-Christophe Simon,Yannick Outreman,Sébastien Boutin,Adrien Frantz,Jean-François Le Gallic,Takema Fukatsu,Tsutomu Tsuchida,Ryuichi Koga,Richard Cordaux

doi:10.1371/journal.pone.0021831

Abstract

Some bacterial symbionts alter their hosts reproduction through various mechanisms that enhance their transmission in the host population. In addition to its obligatory symbiont Buchnera aphidicola, the pea aphid Acyrthosiphon pisum harbors several facultative symbionts influencing several aspects of host ecology. Aphids reproduce by cyclical parthenogenesis whereby clonal and sexual reproduction alternate within the annual life cycle. Many species, including the pea aphid, also show variation in their reproductive mode at the population level, with some lineages reproducing by cyclical parthenogenesis and others by permanent parthenogenesis. While the role of facultative symbionts has been well studied during the parthenogenetic phase of their aphid hosts, very little is known on their possible influence during the sexual phase. Here we investigated whether facultative symbionts modulate the capacity to produce sexual forms in various genetic backgrounds of the pea aphid with controlled symbiont composition and also in different aphid genotypes from natural populations with previously characterized infection status and reproductive mode. We found that most facultative symbionts exhibited detrimental effects on their hosts fitness under sex-inducing conditions in comparison with the reference lines. We also showed that the loss of sexual phase in permanently parthenogenetic lineages of A. pisum was not explained by facultative symbionts. Finally, we demonstrated that Spiroplasma infection annihilated the production of males in the host progeny by inducing a male-killing phenotype, an unexpected result for organisms such as aphids that reproduce primarily through clonal reproduction.

Highlights

Many organisms engage in symbiotic relationships with a wide range of microbes
These facultative symbionts have been mostly studied in the pea aphid Acyrthosiphon pisum, whereas such microorganisms have been screened in many more aphid species [5,6,7]
The effects of the facultative symbiont infections on fitness components of their hosts varied according to the tested pea aphid genotypes

Summary

Introduction

Many organisms engage in symbiotic relationships with a wide range of microbes These sustained and intimate associations provide conditions for the evolution of complex phenotypes on which natural selection may operate and favor one or both partners of the symbiosis. Such symbionts frequently modify the ecology and physiology of their hosts to enhance their own transmission. Buchnera provides the host with essential amino acids lacking in the host diet and may be involved in thermal adaptation in certain circumstances [4] In this case of obligate symbiosis, inheritance of bacterial symbionts is strictly vertical and both partners are mutualistically dependent on each other. In the pea aphid, such effects include host plant utilization [17], body color change [13], heat tolerance [18] and protection against natural enemies [12,19,20,21]

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Discussion

Conclusion