Testing hypotheses about the evolution of insect flight from surface-skimming ancestors

By Jim Marden, Penn State University

Type of Resource Class activity 
Topic Locomotion/motility 
Taxa Invertebrate 
Organizational Level Organismal 
Estimated time to do activity 30-50 min 
Background required/level Soph - Senior 
Role of activity in your course I use this to show how and why biologists use phylogenies to examine the evolutionary history of phenotypic traits, particularly behavioral and biomechanical traits. It stops well short of teaching analytical tools such as independent contrasts. 
What students might learn from this course or activity The behaviors shown in the quicktime movies and illustrated with drawings provide the students with a compelling set of behaviors and biomechanical features. Thus, they should be stimulated by the material and the evolutionary questions being posed. They will learn how to map traits onto a phylogeny and how to interpret the phylogenetic distribution of traits. The material should also get them thinking about a variety of interesting biomechanical topics such as surface tension, aerodynamics, and ground effects. 
Special tools, equipment or software needed Scissors, tape, a way to project quicktime movies or to view them on computer screens.
URLs Student version:

Instructor version: 
Safety precautions, possible permissions necessary The exercise involves evolution (and scissors), so creationists should exercise extreme caution. 
Miscellaneous advice - pitfalls to avoid The phylogenetic map of traits that the students create is not easy to interpret and does not conform to the expectations they are likely to have formed going into the exercise. It does not show that surface skimming is a trait derived from flying (i.e. a loss of flight), nor does it show a clear evolutionary progression in aerodynamic sophistication. This leaves students asking questions like "So what was this supposed to show?" My stock answer to that question is that 1) rejecting the loss of flight hypothesis is an important result, 2) history is very difficult to reconstruct, and many evolutionary questions are difficult to answer, and 3) that evolution meanders; it is not necessarily directional.  
Frequently asked questions by students What were we supposed to find?
- Answer = I don't know; you tell me. What were the hypotheses that you were testing, and what did you conclude about each of them? What does that tell you?

Hypothesis 1: skimming in stoneflies evolved as a loss of flight ability. This is not supported since both skimming and flying are shown by the exercise to be basal traits in Plecoptera. Thus, the origins of both skimming and flying are deeper than we can address with these data.

Hypothesis 2: skimming is retained in stoneflies from non-flying anscestors, perhaps dating back to the origins of insect wing flapping. This hypothesis cannot be rejected, but it cannot be accepted either. We would need to have these sorts of data (phylogeny and traits) for the earliest winged insects and all of the ancestors of moderns stoneflies to definitively assess this hypothesis. Lesson from this: history is very difficult to reconstruct, and many evolutionary questions are difficult to answer. One thing that you can bring in here is the notion that there might be other correlated traits that could shed light on the matter. In other words, if skimming is a retained ancestral trait, then perhaps stoneflies have retained other traits related to a transition from gills to wings. This is the line of thinking that led us to see if stoneflies have hemocyanin in their blood, since blood-based gas exchange is what other gill bearing arthropods use but was previously thought to be completely absent in insects. Stoneflies do indeed have hemocyanin in their blood, it reversibly binds oxygen (PNAS 101: 871-874), and it appears that no other pterygote insects possess this trait. This line of discussion can show how biologists think broadly and creatively when they encounter a deadend in one line of investigation.

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). This hypothesis is not supported, since there is no apparent order to the skimming traits on the phylogeny. Students then want to know why I had them do this if the result is so unsatisfying. In response to this, I ask if evolution must follow a particular directional trend. If they say yes, ask them why. If they say no, encourage them to elaborate. The pattern that they should see on their phylogenetic map is that surface skimming locomotion is an ancestral trait within stoneflies that has evolved in a meandering fashion among the modern taxa. The concept of evolution exploring a phenotypic trait landscape is likely to be novel but valuable concept for advanced undergraduates. 
Evaluation You have to love an exercise that involves scissors, tape, and movies. That said, most students are left somewhat befuddled. The best students are stimulated by the richness of the questions and the complexity of the answers, and that is why I continue to teach this. Overall I think that they learn something by working with their hands to perform a phylogenetic analysis and they retain a fair amount about why you need phylogenies to address evolutionary questions, and what sort of questions you can tackle using a phylogenetic approach. 
Description This is a classroom exercise related to a hypothesis regarding the evolution of insect wings from gills, and the evolution of flight via aquatic and semi-aquatic intermediate stages. The excercise involves using a phylogeny to map the evolutionary history of different forms of semi-aquatic winged locomotion in stoneflies (Insecta: Plecoptera). The phylogenetic map of traits can then be used to evaluate some hypotheses for the evolutionary history of surface skimming and the evolutionary origins of insect flight.  
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