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First published online November 14, 2008
Journal of Experimental Biology 211, 3653-3660 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.023903

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Weight and nutrition affect pre-mRNA splicing of a muscle gene associated with performance, energetics and life history

James H. Marden^1,*, Howard W. Fescemyer¹, Marjo Saastamoinen², Suzanne P. MacFarland¹, J. Cristobal Vera¹, Mikko J. Frilander³ and Ilkka Hanski²

¹ Department of Biology, 208 Mueller Laboratory, Pennsylvania State University, University Park, PA 16802, USA
² Department of Biological and Environmental Sciences, University of Helsinki, Viikinkaari 1, PL 65, 00014 Helsinki, Finland
³ Institute of Biotechnology, University of Helsinki, Viikinkaari 9, PL 56, 00014 Helsinki, Finland

^* Author for correspondence (e-mail: jhm10{at}psu.edu)

Accepted 2 October 2008

A fundamental feature of gene expression in multicellular organisms is the production of distinct transcripts from single genes by alternative splicing (AS), which amplifies protein and functional diversity. In spite of the likely consequences for organismal biology, little is known about how AS varies among individuals or responds to body condition, environmental variation or extracellular signals in general. Here we show that evolutionarily conserved AS of troponin-t in flight muscle of adult moths responds in a quantitative fashion to experimental manipulation of larval nutrition and adult body weight. Troponin-t (Tnt) isoform composition is known to affect muscle force and power output in other animals, and is shown here to be associated with the thorax mass-specific rate of energy consumption during flight. Loading of adults with external weights for 5 days caused an AS response nearly identical to equal increases in actual body weight. In addition, there were effects of larval feeding history on adult Tnt isoform composition that were independent of body weight, with moths from poorer larval feeding regimes producing isoform profiles associated with reduced muscle performance and energy consumption rate. Thus, Tnt isoform composition in striated muscle is responsive to both weight-sensing and nutrition-sensing mechanisms, with consequent effects on function. In free-living butterflies, Tnt isoform composition was also associated with activity level and very strongly with the rate of egg production. Overall, these results show that AS of a muscle gene responds in a quantitative fashion to whole-organism variables, which apparently serves to coordinate muscle strength and energy expenditure with body condition and life history.

Key words: feeding history, phenotypic plasticity, body condition, weight sensing, nutrient sensing, metabolic rate, muscle performance, oogenesis, alternative splicing

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