Immune-challenged fish up-regulate their metabolic scope to support locomotion
Public Library of Science
This is the author accepted manuscript of an open access article available from PLoS via the DOI in this record. Distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/
Energy-based trade-offs occur when investment in one fitness-related trait diverts energy away from other traits. The extent to which such trade-offs are shaped by limits on the rate of conversion of energy ingested in food (e.g. carbohydrates) into chemical energy (ATP) by oxidative metabolism rather than by the amount of food ingested in the first place is, however, unclear. Here we tested whether the ATP required for mounting an immune response will lead to a trade-off with ATP available for physical activity in mosquitofish (Gambusia holbrooki). To this end, we challenged fish either with lipopolysaccharide (LPS) from E. coli or with Sheep Red Blood Cells (SRBC), and measured oxygen consumption at rest and during swimming at maximum speed 24h, 48h and 7 days post-challenge in order to estimate metabolic rates. Relative to saline-injected controls, only LPS-injected fish showed a significantly greater resting metabolic rate two days post-challenge and significantly higher maximal metabolic rates two and seven days post-challenge. This resulted in a significantly greater metabolic scope two days post-challenge, with LPS-fish transiently overcompensating by increasing maximal ATP production more than would be required for swimming in the absence of an immune challenge. LPS-challenged fish therefore increased their production of ATP to compensate physiologically for the energetic requirements of immune functioning. This response would avoid ATP shortages and allow fish to engage in an aerobically-challenging activity (swimming) even when simultaneously mounting an immune response. Nevertheless, relative to controls, both LPS- and SRBC-fish displayed reduced body mass gain one week post-injection, and LPS-fish actually lost mass. The concomitant increase in metabolic scope and reduced body mass gain of LPS-challenged fish indicates that immune-associated trade-offs are not likely to be shaped by limited oxidative metabolic capacities, but may instead result from limitations in the acquisition, assimilation or efficient use of resources.
We are very grateful to Noah Ashley for helpful comments on the manuscript, to all the participants of the Disease Group meeting of the University of Exeter (Cornwall) for useful discussion. All procedures were approved by a prefectorial order from Ariège, France (Agréments de l'établissement pour l’élevage et l'expérimentation no. 0108 and no. SA-013-PB-092; certificats d'autorisation d’élevage et d'expérimentation sur poissons vivants to Oliver Guillaume, no. 09-273 and no. A09-3) and by the University of Sydney Animal Ethics Committee (approval no. L04/10-2010/3/5411). This research was supported by a Marie Curie Reintegration Grant to C.B. (FP7-PEOPLE-IRG-2008 #239257) and an Australian Research Council grant to F.S.
Vol. 11, No. 11, Article number: e0166028