Evolution of insect flight: a stepwise model based on weight-supported locomotion on the surface of water

    

     Since Darwin's time, complex features such as the vertebrate eye and the ability to fly have posed a particular challenge for evolutionary biology. How can complex traits evolve in a stepwise fashion when it is unclear what function or selective advantage can be derived from "half an eye" or a "nub of a wing"? In the case of insect flight, the challenge is to explain how a flight-capable creature, with its complex interrelated nerves, muscles, articulations, and wings, evolved from nonflying ancestors. We have discovered that certain stoneflies use their wings to skim across water surfaces (i.e. nonflying two-dimensional aerodynamic locomotion). These surface-skimming stoneflies do not need to generate total weight support, and they demonstrate a pathway for gradual evolution beginning with rudimentary stages of wings and muscles, all the way to fully weight-supported "true" flight. My students and I have traveled the world (Australia, Chile, Europe) to survey the behavioral and mechanical diversity of stonefly locomotion, and we have constructed a molecular phylogeny to examine the evolutionary history of these traits across the entire order of Plecoptera. As a result of these studies, we now have a reasonably well supported synthetic theory for how flight originated in insects.


Speed increases as the amount of contact with water decreases in stoneflies that use their wings to move across the surface of water.  Our work has shown that insect flight may have evolved gradually along such a series of stages of wing propelled locomotion on the surface of water. Samples sizes refer to the number of species that we have studied that use each of these forms of locomotion.


Publications resulting from this project to date:

Marden, J.H. and M.G. Kramer. 1994. Surface-skimming stoneflies: a possible intermediate stage in insect flight evolution. Science 266, 427-430. 

Marden, J.H. 1995. Flying lessons from a flightless insect. Natural History 104 (2), 4-8

Marden, J.H. and M.G. Kramer. 1995. Locomotor performance of insects with rudimentary wings: sailing on water versus gliding in air. Nature 377, 332-334. 

Marden, J.H. How insects learned to fly. The Sciences 35, 26-30.

Marden, J.H. and M.G. Kramer. 1995. Plecopteran surface-skimming and insect flight evolution - reply. Science 270, 1685.

Kramer, M.G. and J.H. Marden. 1997. Almost airborne. Nature, 385, 403-404. 

Marden, J.H., B.C. O’Donnell, M.A. Thomas, and J.Y. Bye. 2000. Surface-skimming stoneflies and mayflies: the taxonomic and mechanical diversity of two-dimensional aerodynamic locomotion. Physiological and Biochemical Zoology 73, 751-764.

Thomas, M.A., K.A. Walsh, M.R. Wolf, B.A. McPheron, and J.H. Marden. 2000. Molecular phylogenetic analysis of evolutionary trends in stonefly wing structure and locomotor behavior. Proceedings of the National Academy of Science 97:13178-13183.

Marden, J.H. and M.A. Thomas. 2003. Rowing locomotion by a stonefly that possesses the ancestral pterygote condition of co-occurring wings and abdominal gills. Biological Journal of the Linnean Society 79: 341–349.

Marden, J.H.  2003. The surface-skimming hypothesis for the evolution of insect flight.  Proceedings of the 2nd International Congress of Paleoentomology. Acta Zoologica Cracoviensia. 46: 73-84.

Hagner-Holler, S., A. Schoen, W. Erker, J.H. Marden, R. Rupprecht, H. Decker, T. Burmester. 2004.  A respiratory hemocyanin from an insect. Proceedings of the National Academy of Sciences 101: 871-874.

Hagner-Holler, S., Pick, C., Girgenrath,S., Marden, J.H., and Burmester, T. 2007.  Diversity of stonefly hexamerins and implication for the evolution of insect storage proteins. Insect Biochem. Mol. Biol. 37:1064-74

Marden, J.H.  2008. Evolution and physiology of flight in aquatic insects.  In: Aquatic Insects: Challenges to Populations, ed. J. Lancaster.  CABI Press.

Marden, J.H. 2012. Reanalysis and experimental evidence indicates that the earliest trace fossil of a winged insect was a surface-skimming neopteran. Evolution, in press. DOI: 10.1111/j.1558-5646.2012.01743.x

Quick-time movies of Surface-skimming Stoneflies

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