Sexual selection is responsible for much of the morphological diversity among animals and is often expressed in the form of male ornamental displays. Sexual selection theory indicates that these display traits do not come without costs, such that the displays and their costs are countered by natural selection. Stalk-eyed flies provide the ideal model system to test for costs and tradeoffs related to male ornamentation. All species in this extraordinary family display exaggerated head morphology, with eyes and antennae displaced at the end of long stalks, and interspecific variation in eye span can be more than ten-fold. Furthermore, all available evidence indicates that eye stalks are critical sexual signals used in both male-male competition and female choice. This study will examine the effects of elongated eye stalks on flight performance and survivorship of stalk-eyed flies to assess whether these effects run counter to the effects of sexual selection. To achieve this goal, the PI will integrate information from three distinct avenues of research. First, to establish a link between morphology and performance, variation in eye span and locomotor performance will be measured in a single species, Cyrtodiopsis dalmanni, to test for trade-offs between secondary sexual traits and adaptations for flight. For this study, lines of C. dalmanni that have been bidirectionally selected for increased and decreased eye span will be used to increase the natural variation seen in this species. Direct measurements of acceleration, speed and maneuverability during flight will be made using computer-integrated high speed video cameras. Additionally, load lifting capacity and energy used during flight will be measured. Second, the fitness consequences of impaired flight performance will be directly measured in a series of predation avoidance experiments in greenhouse enclosures. Third, patterns of correlated evolution between morphology and flight performance measured on many species within the family Diopsidae will reveal evolutionary consequences of sexual selection. If eye stalks impair locomotor ability, compensatory changes in body design are predicted to evolve within the family to reduce the locomotor cost. Such compensatory changes would indirectly suggest that such reduction in performance was selectively important. This research program incorporates multiple disciplines and will certainly result in new insights regarding interactions between the costs of locomotion and the evolution of secondary sexual ornaments. The PI's educational activities will focus primarily on disadvantaged pre-college students from Native American reservation schools and rural schools. Both of these groups, particularly Native Americans, are traditionally underrepresented in both college and the sciences. South Dakota has both a large Native American population (~ 10%) and a large rural population. Through cooperation with the instructors affiliated with the Mobile Science Laboratory (MSL), the PI will develop a contribution on "Sexual selection and insect diversity: secondary sexual ornaments" for the MSL. Outreach projects developed for the MSL will expose K-12 students from Native American reservation and rural schools to the process of science and discovery. This outreach program has the potential to positively influence thousands of people throughout the state of South Dakota.
Sexual selection acts on an animal’s ability to find mates and successfully reproduce. Because any feature that helps an animal obtain a mate is selected for, sexual selection explains why males have evolved an array of conspicuous ornaments, behaviors, and weapons. The assumption has been that the benefits that come with exaggerating one physical or behavioral characteristic for the sake of mating success do not come without costs that affect survival, such as being more vulnerable to disease, starvation or predation. The peacock’s tail is a textbook example of this assumption. My lab’s work with stalk-eyed flies shows that this assumption overlies a much more complex situation. Stalk-eyed flies are a useful model for investigating the costs of carrying around a sexually selected ornament. All stalk-eyed flies are endowed with a bizarre T-shaped head, where the eyes and antennae are laterally displaced on the ends of elongated narrow stalks. In some species, this elongation is so extreme that eye span exceeds body length. Eyestalks play an important role in stalk-eyed fly mating success; in species in which males have larger eye stalks than the females, male mating success is associated with large eye span. Females prefer males with longer eye spans. Additionally, males compete for access to groups of females. Males engage in ritualized behaviors in which they display and compare their eye stalks and sometimes these displays escalate into physical fights. What keeps eye stalks from growing to even more extravagant lengths is unknown. To fully understand what prevents "run-away" elaboration of male eye stalk length, it is important to understand the costs associated with producing and maintaining eye stalks. Somewhat surprisingly, we showed that despite an elevated moment of inertia associated with increased eye-span that would require ~1.5 fold larger torques to rotate their bodies during aerial turning, males engaged in maneuvers that were equal to, or surpassed, those of females with shorter eye stalks. We suggest that the increase in eye span does indeed result in an increase in the mechanical requirements for aerial turning but that male stalk eyed flies are capable of compensating for the constraint of longer eye stalks during the range of turns observed. Thus, our best evidence for costs derives, indirectly, from our within and between species studies (e.g. thorax muscle mass, wing morphology, wing beat frequency, etc.) which have clearly documented correlated evolution of traits that appear to mitigate these costs. We propose that, because compensatory traits coevolve with ornaments, they may obscure the true costs of bearing an ornament and, as a consequence, that simply testing for bivariate relationships between ornament size and some proxy for fitness (e.g., performance, survival) is an incomplete approach and can lead to inconclusive or misleading results. Confirming these studies of flight performance, staged laboratory interactions between flies and a predator revealed that females did not have higher survival than males when facing a predator; males in fact had higher survival. Our work has resulted in 18 publications in peer-reviewed academic journals, one book chapter, and seven published abstracts. With support from this grant, four post-doctoral scientists, four graduate students, and many undergraduate students, several of whom defended honors theses, have been mentored. In collaboration with a Middle School 7th grade science teacher, we developed a two-week inquiry-based program to simultaneously introduce students to stalk-eyed flies, the concept of sexual selection, and the scientific method. Hundreds of local middle school students were led through the process of observation, question and hypothesis generation, and data collection. In addition, we also developed a website that allows middle school students from across the nation to explore issues of ornament size in relationship to body size and sexual selection. This web site (http://people.usd.edu/~jswallow/flies/html/flies%20interactive%20home.html) is up and running. In addition, we ran hands-on laboratory exercises for junior high and high school students attending the South Dakota Governor's Science Camp, the Lawrence Brothers Science Camp, as well as the Math Science Initiative Project, a program designed to increase interest in and aptitude for science in underrepresented minorities, including Native Americans. To teach students about the biomechanics of torque and what the predicted effects eye span elongation would have on flight performance, we devised a "stalk-eyed fly" relay race. Students ran an obstacle course with two 1-gallon jugs of water which they carried either close to their center of mass or displaced away from the center of mass on a 5-foot pole. Times were recorded and compared between treatments. In addition, we had students observe aggressive interactions between male pairs fighting over a food resource or anti-predators interactions between flies and a spider. They were asked to make hypotheses regarding the outcome of the interactions based on their experience with the relay race. Students experienced, first hand, the importance of the scientific process and also learned that science can be fun.
