American Society of Naturalists

Adrien Perrard (Feb 2020)

Coevolution of wings and body shapes suggests that some wasps were selected to fly fast and others to turn quickly

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About 400 million years ago, insects took to the sky before any other known animal. Today, we observe a tremendous diversity of insects, including many species with astonishing flight performances, but insect flight remains ill-understood. Since the morphology of an organism affects its performance, we need to understand better how the body parts related to flight in insects evolve to identify the components underlying these flight performances. For example, do the different body parts involved in flight evolve in concert, because of common selective pressure? If so, do they compensate each other to keep flight performances around a single optimum? To answer these questions, Dr. Adrien Perrard studied how the shapes of wings, thorax and abdomen change relative to each other in vespid wasps.

In these wasps, the most striking morphological variation is the elongation of the ‘petiole’, the segment connecting the equivalent of thorax and abdomen in wasps. Some species display a short petiole with a bullet-like silhouette likely minimizing drag forces, hence improving flight speed. Other species have a very elongated petiole, which would increase the efficiency of abdominal movements for flight stability. According to recent phylogenies, such a variation in petiole morphology occurred multiple times in the evolutionary history of wasps. But wings and thorax are also related to flight performances. Variation in wings or thorax shapes reflecting the petiole variation would be unlikely by chance. However, they would be expected if a change in petiole had an influence on flight performance, which in turn modified natural selection on the other two body parts. Therefore, the author tested whether wasps with a similar petiole also developed similar wings and thorax morphologies during their evolution, and whether these morphologies could be related to flight performances.

The results show a clear link between the morphology of the wings and that of the abdomen. Wasps with different body-types tend to have wing shapes more similar than expected by chance. In addition, those morphologies were related to similar flight performances, both wings and petiole promoting either speed or maneuverability. Surprisingly, the shape of the thorax was not related to wing shapes: the overall shape of the thorax may not be as important for flight as that of the wings or the petiole.

These results shed some light on the evolutionary mechanisms which drove the morphological diversity of these wasps. Previously, there was no clear explanation for the observed petiole shape elongation in these insects. However, wasps with different body types seem to have experienced different selective pressures regarding their flight performances, to optimize either their maximal speed or their maneuverability. So the diversity of selective regimes on flight-related structures may have contributed to the evolution of the diversity in body shapes in these wasps. In addition, these results strongly suggest that the evolution of wing shape was influenced by the shape of the body wings have to lift, and they stress the importance of abdomen in insect flight.

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Abstract

Insect flight is made possible by different morphological structures: wings produce the lift, the thorax drives the wings’ movements and the abdomen serves as a secondary control device. As such, the covariation of these structures could reflect functional constraints related to flight performances. This study examines evolutionary convergences in wasp body shapes to provide the first evidence for morphological integration among insect wings, thorax and abdomen. Shapes of the fore- and hindwings, thorax and petiole (connecting abdomen and thorax) of 22 Vespidae species were analyzed using computerized tomography and geometric morphometrics. Results show a clear relationship between petiole and wings or thorax shapes, but not between wings and thorax. Wasps with elongated bodies have pointed wings, both features thought to improve flight maneuverability. In contrast, stouter species have rounded wings, which may allow for higher flight speeds. These integration patterns suggest that multiple selective regimes on flight performance, some of them biased towards maneuverability or maximal speed, drove the morphological diversity in Vespidae. The results also suggest that wing shapes evolved under constraints related to the body type they have to lift. The abdomen morphology is thus another factor to take into account to understand the flight performance of insects.