From molecules to mating success: Integrative biology of muscle maturation in a dragonfly1

SYNOPSIS. Dragonflies begin adult life as comparatively weak fliers, then mature to become one of nature's ultimate flying machines. This ontogenetic transition provides an opportunity to investigate the relationship between life history, phenotypic plasticity, and changing ecological demands on organismal performance. Here we present an overview of a wide-ranging study of dragonfly muscle maturation that reveals i) ecological changes in the need for efficient versus high-performance flight, ii) organism-level changes in performance, thermal physiology, locomotor mechanics, and energy efficiency, iii) tissue-level changes in muscle ultrastructure and sensitivity to activation by calcium, and iv) molecular-level changes in the isoform composition of a calcium regulatory protein in flight muscle (troponin-T). We discuss how these phenomena may be causally related, and thereby begin to show linkages across many levels of biological organization. In particular, we suggest that alternative splicing of troponin-T mRNA is an important component of the "gearing" of muscle contractile function for developmental changes in wingbeat frequency and ecological demands on flight performance. Age-variable gearing of muscle function allows energetically economical flight during early adult growth, whereas power output is maximized at maturity when aerial competition determines success during territoriality and mating.