With board and lodging: facultative endosymbionts come with energy costs for aphids

Clavé Corentin, Sugio Akiko, Morlière Stéphanie, Pincebourde Sylvain, Simon Jean-Christophe, Foray Vincent

This is a plain language summary of a Functional Ecology research article which can be found here.

Aphids form intimate associations with bacteria. These bacteria, also called endosymbionts, are hosted in specialized cells and are transmitted vertically from mother to offspring. While some endosymbionts are obligate (e.g., Buchnera aphidicola), others appear  to be facultative, raising the question of their function for the host. The former play an essential  nutritional role and are present in all aphid species, whereas the latter can confer benefits under  certain environmental conditions, like increased resistance to natural enemies and heat stress. Despite these benefits, facultative endosymbionts are found at variable frequencies in natural populations. This suggests the costs of carrying facultative endosymbionts can exceed the benefits  when the selective  pressures that favor the associations with facultative symbionts are weak. For example, under optimal thermal conditions or low abundance of natural enemies, the competitive ability of infected insects may be low relative to uninfected ones.

Young stages of pea aphids (Acyrthosiphon pisum) on a leaf of broad bean (Vicia faba) sucking the sap (credit: Vincent Foray)

Our study tests whether facultative endosymbionts generate fitness costs for aphids. We ask whether  this can be explained from an energetic point of view by the balance between the level of energetic reserves and the costs of maintenance. We are also interested in how these costs vary according to the bacterial species, the genotype of the host and the environmental conditions. To resolve these matters, we compared aphids carrying either the facultative endosymbionts Hamiltonella defensa or Regiella insecticola to their uninfected counterparts. We measured aphids’ fitness, energetic budget and metabolic rate with a respirometer to estimate their maintenance cost.

Our results show that aphids carrying facultative endosymbionts expressed a higher metabolic rate compared to aphids without facultative endosymbionts, but relatively similar energetic reserves, suggesting that facultative endosymbionts primarily influence the consumption of energy resources rather than their acquisition. Finally, we observed that metabolic rate increased with temperature, but unexpectedly the difference between aphids with and without facultative endosymbionts tended to disappear at high temperature. Our study highlights that energy metabolism improves our understanding of the maintenance of facultative  associations in aphids and must be investigated in other symbiotic associations.

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