Classroom exercise: Testing hypotheses about the evolution of insect flight from surface-skimming ancestors
Jim Marden, Dept. of Biology, Penn State University
In 1994, we proposed a novel hypothesis for the evolutionary origins of insect flight. This hypothesis was based on our discovery of a form of two-dimensional aerodynamic locomotion, called surface-skimming, which certain stoneflies and mayflies use to move across the surface of water. The body weight of a surface-skimmer is supported by water, and this makes it a particulary likely intermediate form for the evolutionary pathway that led from non-fliers to fliers. Because flight requires a sophisticated set of wings, wing hinges, muscles, and neural stimulation, the evolutionary origin of flight is a difficult puzzle. If early forms of wings, wing hinges, and flight muscles are not sufficient to allow flying, how could natural selection act to gradually improve their function? Surface-skimming is much less demanding than flying; even very small amounts of aerodynamic thrust can propel an insect across the water surface. Thus, we proposed that surface-skimming is a solution to the old riddle "what good is a nub of a wing". We even went so far as to speculate that surface-skimming is a retained ancestral trait in modern stoneflies, perhaps dating back to a stage in insect evolution that predates flying.
Like many new ideas, this one had potential holes in it. As pointed out in a short communication by Will (1995) we had not rigorously examined how our surface-skimming species was related to other stoneflies. Using a phylogeny based on morphological characters, Will argued that our original surface skimmer was a relatively derived species, therefore placing skimming on an isolated branch of the stonefly tree (i.e. almost certainly a recent loss of flight). At face value, this critique was devestating for our new idea, but its logic completley crumbled when examined a bit more closely. Will's analysis implicitly assummed that skimming was used only by the species in which it had first been described, which also happened to be the only species that had ever been examined for this trait. How much weight should be placed on an evolutionary analysis that lacks even a rudimentary knowledge of the phylogenetic distribution of the trait in question?
With this background, we set out to examine surface-skimming behavior over the entire order of Plecoptera. Many stonefly families are restricted to the Southern Hemisphere, so this project required us to go to places like Australia, Tasmania, and southern Chile to bump around on remote gravel roads and check hundreds of pristine streams and rivers for adult stoneflies. We had a grand time!!!! Here is some of what we found.
2. Movies of different types of surface-skimming:
(these require Quicktime software; click to view, then save to your own disk)
1. Six-leg skimming
3. Hind-leg skimming
4. Four-leg skimming
7. Initiation of flight by jumping from water
3. Icons that represent different forms of skimming
Suggested use: Print this page, cut out the individual icons, then arrange these icons according to a hypothetical evolutionary progression based on decreasing contact with water and increasing wingbeat amplitude. Does this sample of behaviors form a reasonable series of steps that lead from non-flying to flying?
4. Testing your hypothesized evolutionary progression
What you have constructed in step 3 is simply a more fleshed out version of our original hypothesis from 1994. What is still lacking is an understanding of how these behaviors are distributed on a phylogeny. How might you use a phylogeny to test the validity of your hypothesis about progressive evolution of insect flight through these stages of surface skimming?" Here is a simplified version of the phylogeny that we obtained for families of stoneflies. This tree is based on a combination of 18s rDNA sequence data and morphological data (Thomas et al. 2000). Branches that do not have strong bootstrap support are shown as polytomies (i.e. our data cannot resolve the order of origin of certain subsets of families). Tape the skimming icons (which you cut out in step 3 above) onto the tree at the appropriate places. What can you conclude from this "map" in regard to both the original debate (Will 1995) and your hypothesized mechanical progression?
Hypotheses to test:
Hypothesis 1: skimming in stoneflies evolved as a loss of
Hypothesis 2: skimming is retained in stoneflies from non-flying anscestors, perhaps dating back to the origins of insect wing flapping.Hypothesis 3: Stonefly skimming has evolved as a progression from the simplest forms (sailing, rowing) to the most flight-like forms (4-leg and hind-leg skimming).
What does your map of traits on the phylogeny indicate about each of these hypotheses?
5. To learn more about this topic:
Kramer, M.G. and J.H. Marden. 1997. Almost airborne. Nature 385, 403-404.
Marden, J.H. 1995. Flying lessons from a flightless insect. Natural History 104, 4-8.
Marden, J.H. 1995. How insects learned to fly. The Sciences 35, 26-30.
Marden, J.H. and M.G. Kramer. 1994. Surface-skimming stoneflies: a possible intermediate stage for insect flight evolution. Science 266, 427-430.
Marden, J.H. and M.G. Kramer. 1995. Locomotor performance of insects with rudimentary wings. Nature 377, 332-334. (cover)
Marden, J.H. and M.G. Kramer. 1995. Plecopteran surface-skimming and insect flight evolution - reply. Science 270, 1685.
Marden, J.H., B.C. O'Donnell, M.A. Thomas, and J.Y. Bye. 2000.
stoneflies and mayflies: the taxonomic and mechanical diversity of
aerodynamic locomotion. Physiological and Biochemical Zoology
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:
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.
Ruffieux, L., J. Elouard, and M. Sartori. 1998. Flightlessness in mayflies and its relevance to hypotheses on the origin of insect flight. Proceedings of the Royal Society B 265:2135-2140.
Samways, M.J. 1996. Skimming and insect evolution. Trends in Ecology & Evolution 11:471.
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
Thomas, A.L.R. 1996. Skimming and insect evolution- reply. Trends in Ecology & Evolution 11:471.
Thomas, A.L.R. and R.A. Norberg. 1996. Skimming the surface - the origin of flight in insects? Trends in Ecology & Evolution 11:187-188.
Will, K.W. 1995. Plecopteran surface-skimming and insect flight evolution. Science 270:684.
A sample of other papers regarding wing and flight origins:
Averof, M. and S. Cohen. 1997. Evolutionary origin of insect wings from ancestral gills. Nature 385:627-630.
Burgers, P. and L.M. Chiappe. The wing of Archaeopteryx as a primary thrust generator. Nature 399:60-62.
Carroll, S.B., S.D. Weatherbee, and J.A. Langeland. 1995. Homeotic genes and the regulation and evolution of insect wing number. Nature 375:58-61.
Dickinson, M.H., S. Hannaford, and J. Palka. 1997. The evolution of insect wings and their sensory apparatus. Brain, Behavior and Evolution 50:13-24.
Dudley, R. 1998. Atmospheric oxygen, giant Paleozoic insects and the evolution of aerial locomotor performance. Journal of Experimental Biology 201:1043-1050.
Gould, S.J. 1985. Not necessarily a wing: which came first, the function or the form? Nat. Hist. 94, 12-25.
Kingsolver, J.G. and M.A.R. Koehl. 1985. Aerodynamics, thermoregulation, and the evolution of insect wings: differential scaling and evolutionary change. Evolution 39:488-504.
Kingsolver, J.G. and M.A.R. Koehl. 1994. Selective factors in the evolution of insect wings. Annual Review of Entomology 39,425-51.
Kukalova Peck, J. 1983. Origin of the insect wing and wing articulation from the arthropodan leg. Canadian Journal of Zoology 61:2327-2345.
Kukalova-Peck, J. 1978. Origin and evolution of insect wings and their relation to metamorphosis, as documented by the fossil record. Journal of Morphology 156:53-125.
Kukalova-Peck, J. 1987. New Carboniferous Diplura, Monura, and Thysanura, the hexapod ground-plan, and the role of thoracic side lobes in the origin of wings (Insecta). Canadian Journal of Zoology 65: 2327-45.
Kukalova-Peck, J. 1991. Fossil history and the evolution of hexapod structures. In The Insects of Australia, I.D. Naumann, Ed. (Melbourne Univ. Press, Melbourne, ed. 2, 1991), pp. 141-179.
Toms, R.B. 1984. Were the first insects terrestrial or aquatic? South African Journal of Science 80:319-323.
Recent papers about the phlylogenetic origins of insects:
Boore JL, Lavrov DV, Brown WM. 1998. Gene translocation links insects and crustaceans. Nature 392:667-8.
Garcia-Machado E, Pempera M, Dennebouy N, Oliva-Suarez M, Mounolou JC, Monnerot M. 1999. Mitochondrial genes collectively suggest the paraphyly of Crustacea with respect to Insecta. J Mol Evol.49:142-9.
Popadic A, Panganiban G, Rusch D, Shear WA, Kaufman TC. 1998. Molecular evidence for the gnathobasic derivation of arthropod mandibles and for the appendicular origin of the labrum and other structures. Dev Genes Evol 208:142-50
Regier, J.C. and J.W. Schultz. 1997. Molecular phylogeny of the major arthropod groups indicates polyphyly of crustaceans and a new hypothesis for the origin of hexapods. Molecular Biology and Evolution 14:902-913.
Scholtz G, Mittmann B, Gerberding M. 1998. The pattern of Distal-less expression in the mouthparts of crustaceans, myriapods and insects: new evidence for a gnathobasic mandible and the common origin of Mandibulata. Int J Dev Biol. 42:801-10.
Strausfeld, N.J. 1998. Crustacean-insect relationships: the use of brain characters to derive phylogeny amongst segmented invertebrates. Brain, Behavior and Evolution 52:186-206.
Strausfeld, N.J., L. Hansen, L. Yongsheng, R.S. Gomez, and K. Ito. 1998. Evolution, discovery, and interpretations of arthropod mushroom bodies. Learning & Memory 5:11-37.
Wilson K, Cahill V, Ballment E, Benzie J. 2000. The complete sequence of the mitochondrial genome of the crustacean Penaeus monodon: are malacostracan crustaceans more closely related to insects than to branchiopods? Mol Biol Evol. 2000 17:863-74.