Current Biology Dispatches 7. Baker, A.J., Haddrath, O., McPherson, J.D., and Cloutier, A. (2014). Genomic support for a moa-tinamou clade and adaptive morphological convergence in flightless ratites. Mol. Biol. Evol. 31, 1686–1696. 8. Mitchell, K.J., Llamas, B., Soubrier, J., Rawlence, N.J., Worthy, T.H., Wood, J., Lee, M.S., and Cooper, A. (2014). Ancient DNA reveals elephant birds and kiwi are sister taxa and clarifies ratite bird evolution. Science 344, 898–900. 9. Lee, M.S.Y., and Ho, S.Y.W. (2016). Molecular clocks. Curr. Biol. 26, R399–R402. 10. Jarvis, E.D., Mirarab, S., Aberer, A.J., Li, B., Houde, P., Li, C., Ho, S.Y., Faircloth, B.C., Nabholz, B., Howard, J.T., et al. (2014). Wholegenome analyses resolve early branches in the tree of life of modern birds. Science 346, 1320– 1331. 11. Prum, R.O., Berv, J.S., Dornburg, A., Field, D.J., Townsend, J.P., Moriarty Lemmon, E., and Lemmon, A.R. (2015). A comprehensive phylogeny of birds (Aves) using targeted nextgeneration DNA sequencing. Nature 526, 569–573. 12. Lartillot, N., and Poujol, R. (2011). A phylogenetic model for investigating correlated evolution of substitution rates and continuous phenotypic characters. Mol. Biol. Evol. 28, 729–744. 13. Houde, P. (1986). Ancestors of ostriches found in the Northern Hemisphere suggest a new hypothesis for origin of ratites. Nature 324, 563–565. 14. Nesbitt, S.J., and Clarke, J.A. (2016). The anatomy and taxonomy of the exquisitely preserved Green River Formation (Early Eocene) lithornithids (Aves) and the Relationships of Lithornithidae. Bull. Am. Mus. Nat. Hist. 406, 1–91. Insect Evolution: The Origin of Wings Andrew Ross Department of Natural Sciences, National Museum of Scotland, Chambers Street, Edinburgh EH1 1JF, UK Correspondence: a.ross@nms.ac.uk http://dx.doi.org/10.1016/j.cub.2016.12.014 The debate on the evolution of wings in insects has reached a new level. The study of primitive fossil insect nymphs has revealed that wings developed from a combination of the dorsal part of the thorax and the body wall. How animals acquired the ability to fly is a question of major interest to evolutionary biologists. Flight enables an animal to disperse across physical barriers, such as seas, live in comparatively safe places away from ground-dwelling predators, to access food sources that others cannot reach and to find a mate. Vertebrates evolved the ability for powered flight independently in several lineages, such as pterosaurs, birds and bats. However, the insects got there first and it is widely believed that they evolved wings and the ability to fly only once. A recent paper in Current Biology by Prokop et al. [1] has taken the long discussion of the origin of wings and flight in insects to the next level. The debate on the subject goes back to the 19th century when there were two main positions on the origin of insect wings, namely whether they developed as entirely new structures or from preexisting structures. As the latter gained acceptance, the discussion moved on to which structures, either tracheal gills (like those of mayfly nymphs) or paranota (lateral extensions of the nota, the dorsal part of thoracic body segments). The latter idea received support when Lithomantis carbonarius, one of the first articulated Carboniferous fossil insects, was discovered (Figure 1A) [2]. This species belongs to the extinct order Palaeodictyoptera, which is widely regarded as the most primitive group of winged insects. Its oldest known fossil representative (the oldest known winged insect), is the 325 million year old Delitzschala bitterfeldensis [3]. Palaeodictyoptera had their heyday in the Carboniferous and rapidly diversified into over 30 families though had become extinct by the end of the Permian (252 million years ago) [4]. They had a pointed beak for piercing and it is believed they fed on fluids from the seeds and stems of giant clubmosses and tree ferns, as holes of the right size have been found in fossils [5]. Palaeodictyoptera possessed two pairs of outstretched wings and veined paranotal lobes on the prothorax as can been seen on L. carbonarius. Thus the paranotal theory gained acceptance [6], though the tracheal gill theory did not go away and was championed by others later [7]. In the first half of the 20th century, there were two main theories for the origin of flight in insects, the ‘flying squirrel’ and ‘flying fish’ theories depending on whether the author believed flight originated on land (by launching off giant clubmosses) or from the surface of the sea. Both hypothesised that the extended paranotal lobes enabled the insect to glide, then to steer and finally to flap [8]. The ‘flying squirrel’ model became the generally accepted norm, particularly supported by the discovery of the then oldest known fossil ‘insect’, the 407 million year old springtail Rhyniella praecursor preserved in Rhynie Chert. The chert was deposited by hot volcanic springs and preserved the earliest known terrestrial ecosystem [9]. Springtails (Collembola) are wingless and have six legs (hexapods, like all insects) and today they, along with some other apterygotes (diplurans and proturans), are regarded as the sister group to the Insecta because they have internal rather than external mouthparts. Springtails have a unique structure, the furcula (spring) that they use to propel themselves into the air to escape hazardous situations. The furcula can be seen on Rhyniella [10] (Figure 1B). So even though springtails were the first to experience the wind Current Biology 27, R103–R122, February 6, 2017 ª 2016 Elsevier Ltd. R113 Current Biology Dispatches A Prothoracic lobes C B Furcula Figure 1. Early hexapods, showing adaptations for flight or propulsion into the air. (A) Lithomantis carbonarius, a palaeodictyopteran from the Upper Carboniferous of Scotland. Scale bar 10 mm. Photograph by Phil Crabb. Copyright Natural History Museum, London. (B) Abdomen of Rhyniella praecursor, a springtail from the Lower Devonian of Scotland. Scale bar 0.1 mm. Photograph by Peter York. Copyright Natural History Museum, London. (C) Idoptilus peachii, an early instar palaeodictyopteran nymph from the Upper Carboniferous of Scotland. Scale bar 5 mm. Photograph by Bill Crighton. Copyright National Museums Scotland, Edinburgh. R114 Current Biology 27, R103–R122, February 6, 2017 rushing through their antennae, they had no control on where (or which way up) they would land. At the time they were collectively included with all the other apterygotes and Rhyniella supported the theory that pterygotes evolved from apterygotes on land [11]. A true insect, Rhyniognatha hirsti, was subsequently recognised from the Rhynie Chert and although it’s jaws were mayfly-like, there was no evidence as to whether it had any vestiges of wings [12]. In the 1970s and 80s there was a rennaisance of discussion papers on the origin of flight in winged insects (pterygotes; e.g. [13,14]). One important suggestion to come from these was that the greater surface area provided by the paranotal lobes could have been used for thermoregulation, i.e. the quicker an insect warmed up by basking, the more active it would become, and it was argued that this was a driver for the lobes to become extended in the first place. The discussion moved on to exactly what part of the body did the protowings develop from, paranota or pleura (lateral extensions of the body wall), or even from a combination of the two [15]. Now the new paper by Prokop et al. [1] appears to have solved this issue from the close study of the nymphs of Palaeodictyoptera. The nymphs, although rare as fossils, possessed two pairs of wing pads on the thorax as well as a pair of prothoracic lobes, which they retained to adulthood (Figure 1C). Different sized instars (growth stages between moults) demonstrate the development of the rich wing venation that can be seen in the adults but it has not yet been possible to match nymphs and adults of the same species. Close examination of the wing pads of nymphs by Prokop et al. [1] provided support for the idea that they were not fixed but articulated, and that the amount of articulation increased as the nymph grew (the prothoracic lobes could also articulate but to a lesser degree). Prokop et al. [1] also conclude that insect wings and the hinge articulation developed from a combination of the nota and the lateral body wall, so they can’t be called ‘paranotal’ lobes any more. If the nymphs could articulate their wing pads, could they fly? The authors concluded no, but they could have been used for gliding to some extent. Current Biology Dispatches Thus Palaeodictyoptera nymphs support the theory that the ancestral pterygote had three pairs of veined thoracic lobes, enabling it to warm up and become more active faster. Extended lobes with some articulation enabled the insect to glide, perhaps to escape predators and to aid dispersal. The final step was for the articulation and musculature to develop to allow two pairs of wings to be actively flapped. This major development allowed insects to colonise the world. REFERENCES 1. Prokop, J., Pecharová, M., Nel, A., ska, E., Hörnschemeyer, T., Krzemin ski, W., and Engel, M.S. (2017). Krzemin Paleozoic nymphal wing pads support dual model of insect wing origins. Curr. Biol. 27, 263–269. 2. Ross, A.J. (2010). A review of the Carboniferous fossil insects from Scotland. Scot. J. Geol. 46, 157–168. 3. Brauckmann, C., and Schneider, J. (1996). Ein unter-karbonisches Insekt aus dem Raum Bitterfeld/Delitzsch (Pterygota, Arnsbergium, Deutschland). Neu. Jahr. Geol. Pal., Monat. 1996, 17–30. Rhynie, Scotland. In Terrestrial Conservation €tten: Windows into the Evolution of Lagersta Life on Land, N.C. Fraser and H.-D. Sues (eds). (Edinburgh: Dunedin Academic Press Ltd). 4. Nicholson, D.B., Mayhew, P.J., and Ross, A.J. (2015). Changes to the fossil record of insects through fifteen years of discovery. PLoS One 10, 1–61. 10. Whalley, P., and Jarzembowski, E.A. (1981). A new assessment of Rhyniella, the earliest known insect, from the Devonian of Rhynie, Scotland. Nature 291, 317. 5. Labandeira, C.D., and Phillips, T.L. (1996). Insect fluid-feeding on Upper Pennsylvanian tree ferns (Palaeodictyoptera, Marattiales) and the early history of the piercing-and-sucking functional feeding group. Ann. Ent. Soc. Am. 89, 157–183. 11. Scourfield, D.J. (1940). The oldest known fossil insect. Nature 145, 799–801. 6. Crampton, G. (1916). The phylogenetic origin and the nature of the wings of insects according to the paranotal theory. J. New York Ent. Soc. 24, 1–38. 13. Kingsolver, J.G., and Koehl, M.A.R. (1985). Aerodynamics, thermoregulation, and the evolution of insect wings: differential scaling and evolutionary change. Evol. 39, 488–504. 7. Wootton, R.J. (1986). The origin of insect flight: where are we now? Antenna 10, 82–86. 14. Kukalová-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). Can. J. Zool. 65, 2327–2345. 8. Forbes, W.T.M. (1943). The origin of wings and venational types in insects. Am. Mid. Nat. 29, 381–405. 9. Trewin, N.H., and Kerp, H. (in press). The Rhynie and Windyfield cherts, Early Devonian, 12. Engel, M.S., and Grimaldi, D.A. (2004). New light shed on the oldest insect. Nature 427, 627–630. 15. Grimaldi, D., and Engel, M.S. (2005). Evolution of the Insects (Cambridge: Cambridge University Press). Motor Control: Winging It with a Few Good Muscles Troy R. Shirangi Department of Biology, Villanova University, Villanova, PA 19085, USA Correspondence: troy.shirangi@villanova.edu http://dx.doi.org/10.1016/j.cub.2016.12.027 A recent study reveals how flies achieve their remarkable aerodynamic agility with only a small number of wing muscles. Few flying animals are as agile as flies. Centuries of frustrated fly swatters can attest to that. In a split second, a fly can change direction at will or react to turbulence to stay on course. Amazingly, this agility is achieved along three axes of rotation [1]. While terrestrial animals only rotate about the vertical axis and turn left or right, flies can also rotate nose-up or nose-down and roll from side to side. To manoeuver rapidly and stably along these three axes requires a highly sophisticated flight control system. Anatomists have long recognized, however, that flies control their flight with a strikingly small number of wing muscles: the fruit fly Drosophila, for instance, uses only a dozen wing muscles to control flight, each supplied by a single motoneuron. How such a sparse motor system can allow flies to fly with such finesse has eluded neuroethologists for decades. That is, until now. In this issue of Current Biology, Lindsay et al. [2] report the secret to a fly’s remarkable aerial agility. They discovered that the wing musculature of Drosophila, while consisting of only a few muscles, is functionally organized in a far more ‘stratified’ and logical fashion than we previously appreciated. To crack the mystery of fly flight, neuroethologists have sought to understand how each wing muscle contributes to flight stability and steering. Traditionally, this problem has been approached using electrophysiology: a fly is tethered to the tip of a tiny rod, and an electrode is inserted into an individual muscle to record the muscle’s firing pattern during flight. By correlating patterns of muscle activity with changes in wing kinematics during flight, scientists can infer the role of that muscle in flight control. These types of experiments have provided great insights into how wing muscles control flight, particularly during rapid turns [3]. Most muscles examined were found to be inactive during straight flight, but transiently activated when the fly steered. Moreover, the activity of each wing muscle was associated with specific changes in the motion of the wing located Current Biology 27, R103–R122, February 6, 2017 ª 2016 Elsevier Ltd. R115
