Variation in flight performance in the dragonfly Libellula pulchella:
causes and consequences






     My laboratory is using dragonflies as model organisms to examine how variation at the molecular level (mRNA transcripts that differ because of alternative splicing and encode functionally distinct muscle protein isoforms) affects tissue level traits (muscle contraction) and whole organism performance (flight ability and success in territorial interactions and competition for mates). We seek to understand both the mechanisms and ecological context in which this occurs, and how variation in performance affects male reproductive fitness. This is a challenging and stimulating project because it requires us to employ a wide variety of methods and to integrate different types of data from multiple levels of biological organization.

   

Left: Alternative splicing of the muscle calcium regulatory gene, troponin-t, affects muscle performance in L. pulchella dragonflies (Marden et al. 2001).  The relative abundance of two of the six splice variants that occur in flight muscle are correlated with greater muscle force and power output, presumably because these splice variants make the muscle more sensitive to activation by calcium.  Right: individual males with higher muscle power output have higher territorial and lifetime mating success (Marden & Cobb, 2004)
 
     Alternative splicing is a mechanism that individuals use to create different phenotypes from a single gene (i.e. not an allelic difference).  Why do some individual dragonflies make low-power muscle that reduces their ability to compete for territories and mates?  The likely answer comes from studies that we have done showing that muscle performance increases duirng the course of adult maturation (Fitzhugh & Marden, 1997), that muscle performance is positively correlated with energy reserves (Marden & Cobb, 2004), and that about two-thirds of newly emerged adult L. pulchella starve before reaching adult maturation (Marden & Rowan, 1999).  Thus, we think that dragonflies use alternative splicing of troponin-t to adjust their energy consumption to that they either conserve energy when necessary or maximize flight performance and mating sucess when they are in a favorable energetic state.


A conceptual model for the pivotal role of alternative splicing of a muscle regulatory gene.


    We have recently begun to examine how infection of dragonflies by protozoan gut parasites (gregarines) affects the regulation of protein expression in flight muscle, how these changes affect contractility and territorial defense, and the signaling and metabolic pathways by which gut parasites achieve systemic effects.  We are also discovering some very interesting things about among-pond variation in gregarine infection rates, and we are testing hypotheses that relate the variation in infection rates to the ecology of the ponds.
    



Left: Male L. pulchella dragonfles infected with greganrine parasites are seldom territory holders; rather they frequently adopt the alternative mating strategy of lurking inconspicuously near the territories of other males in order to sneak copulations with females.  Center: A fairly heavy infection of a dragonfly midgut (sliced open longitudinally in this image) by gregarine parasites.  Right: An individual gregarine trophozoite.

I find this project to be particularly exciting because it provides a rare opportunity to integrate information from molecular, cellular, organismal, and ecological levels in order to arrive at a robust understanding of the biology of a wild species

      


Publications resulting from this project to date:

Schilder, R.J. and J.H. Marden.  2006.  Metabolic syndrome and obesity in an insect.  Proceedings of the National Academy of Sciences, in press.

Marden, J.H.  2006.  Quantitative and evolutionary biology of alternative splicing: how changing the mix of alternative transcripts affects phenotypic plasticity and reaction norms.  Heredity, Sept. 27 Epub ahead of print .

Marden, J.H. and J. R. Cobb.  2004. Territorial and mating success of dragonflies that vary in muscle power output and presence of gregarine gut parasites.  In press, Animal Behaviour 68, 657–665..

Marden, J.H.  2004. Functional and ecological effects of isoform variation in insect flight muscle.  In: Nature’s Versatile Engine: Insect Flight Muscle Inside and Out, ed. J. Vigoreaux. Landes Bioscience, Georgetown, Texas.

Schilder, R.J. and Marden J.H.  2004.  A hierarchical analysis of the scaling of force production by dragonfly flight motors. Journal of Experimental Biology 207, 767-776.

Marden, J. H., G.H. Fitzhugh, M. Girgenrath, M. R. Wolf, and S. Girgenrath. 2001. Alternative splicing, muscle contraction and intraspecific variation: associations between troponin T transcripts, calcium sensitivity, and the force and power output of dragonfly flight muscles during oscillatory contraction. Journal of Experimental Biology 204: 3457-3470.

Marden, J.H. 2000. Variability in the size, composition, and function of insect flight muscles. Annual Review of Physiology 62, 157-178.

Marden, J.H. and B. Rowan. 2000. Growth, differential survival, and shifting sex ratio of free-living Libellula pulchella (Odonata: Libellulidae) dragonflies during adult maturation. Annals of the Entomological Society of America 93, 452-458.

Marden, J.H., G.H. Fitzhugh, M.R. Wolf, K.D. Arnold, and B. Rowan. 1999. Alternative splicing, muscle calcium sensitivity, and the modulation of dragonfly flight performance. Proceedings of the National Academy of Science 96, 15304-15309 (cover).

Marden, J.H., G.H. Fitzhugh, and M.R. Wolf. 1998. From molecules to mating success: integrative biology of muscle maturation in a dragonfly. American Zoologist 38, 528-545. (abstract & cover)

Fitzhugh, G.H. and J.H. Marden. 1997. Maturational changes in troponinT expression, calcium sensitivity, and twitch contraction kinetics in dragonfly flight muscle. Journal of Experimental Biology 200, 1473-1482.
(abstract)

Marden, J.H., M.G. Kramer, and J. Frisch. 1996. Age-related variation in body temperature, thermoregulation, and activity in a thermally polymorphic dragonfly. Journal of Experimental Biology 199, 529-535. (abstract)

Marden, J.H. 1995. Large-scale changes in thermal sensitivity of flight performance during adult maturation in a dragonfly. Journal of Experimental Biology 198, 2095-2102. (abstract & cover)


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