Rowing Locomotion by a Stonefly That Possesses the Ancestral Pterygote
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lackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 2003? 2003 79? 341349 Original Article ROWING BY AN ADULT STONEFLY WITH GILLSJ. H. MARDEN and M. A. THOMAS Biological Journal of the Linnean Society, 2003, 79, 341–349. With 6 figures Rowing locomotion by a stonefly that possesses the ancestral pterygote condition of co-occurring wings and abdominal gills JAMES H. MARDEN* and MICHAEL A. THOMAS† 208 Mueller Laboratory, Department of Biology, Pennsylvania State University, University Park, PA 16802, USA Received 17 July 2002; accepted for publication 14 November 2002 A leading hypothesis for the origin of insect wings is that they evolved from thoracic gills that were serial homologues of the abdominal gills present in fossil pterygotes and in the nymphs of some modern mayflies, damselflies and stone- flies. Co-occurrence of thoracic wings and abdominal gills is the primitive condition for fossil pterygote insects, whereas the winged stage of modern insects almost exclusively lacks abdominal gills. Here we examine the locomotor behaviour and gill morphology of a stonefly, Diamphipnopsis samali (Plecoptera), which retains abdominal gills in the winged adult stage. This species can fly, but also uses its forewings as oars to accomplish rowing locomotion along the surface of water. The abdominal gills are in contact with both air and water during rowing, and their elaborately folded surface suggests an ability to contribute to gas-exchange. D. samali nymphs also have behaviours that place them in locations where their gills are exposed to air; they forage at night at the stream margin and within bubble curtains in rapids. These traits may exemplify an early pterygote condition in which gill and protowing function over- lapped in an amphibious setting during a transition from aquatic to aerial locomotion and gas exchange. Rowing loco- motion provides a novel and mechanically intermediate stage for the wings-from-gills and surface-skimming hypotheses for the origin of insect wings and flight. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 79, 341–349. ADDITIONAL KEYWORDS: amphibious – Chile – Diamphipnopsis – evolution – flight – insect – Plecoptera – surface skimming. INTRODUCTION The evolution of flight in insects appears to have trig- gered an unparalleled radiation and diversification, ‘Adult tracheal gills are probably “living fossils” among the and today the pterygote insects comprise over half of organs of modern adult pterygotes. Their development appar- all described species (Hammond, 1992). However, the ently was so deeply rooted in the epigenotypes of the ancestors fossil record contains none of the early transitional of modern perennibranchiate [i.e. gilled adult] species that it stages leading to or between apterygote and pterygote has not been entirely suppressed by metamorphosis and long non-functionality during the more than 300 million years of insects. As a result, the evolutionary origin of insect the terrestrial existence of adult pterygotes. Hence, perenni- flight remains uncertain and is a popular topic for branchiality is not merely an interesting aberrant phenome- study and lively debate by biologists and palaeontolo- non, but a remnant of a memorable and still largely unknown gists (e.g. Kukalova¢-Peck, 1978; Kingsolver & Koehl, past of insects, and probably also a partial key to it.’ Sˇ tys & 1985; Ellington, 1991; Marden & Kramer, 1994; Soldán (1980: 432–433). Dudley, 2000). Key issues in these debates are the phylogenetic ori- gin of insects and the anatomical origin of wings. One prominent hypothesis is that insects are a sister clade of myriapods, whose wings arose from lateral out- *Corresponding author. E-mail: [email protected] growths of the dorsal thorax. This hypothesis envi- †Present address: The Medical College of Wisconsin’s Bioinformatics Research Center, 8701 Watertown Plank Road, sions flight originating in a terrestrial environment, Milwaukee, WI 53226. most probably by a sequence involving parachuting, © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 79, 341–349 341 342 J. H. MARDEN and M. A. THOMAS gliding, and ultimately flapping, during which the caution regarding this interpretation). In addition, the immobile lateral outgrowths of the thorax (proto- wings of modern insects carry sensilla and chemore- wings) gradually acquired the articulation, muscula- ceptors that are present on arthropod appendages ture and neural pattern necessary for powered flight. (such as the leg exites that are hypothesized to have This hypothesis has traditionally maintained a prom- became gills) but not on the thoracic body wall (Dick- inent place in all debates and is favoured by many con- inson, Hannaford & Palka, 1997). Together, these temporary authors (e.g. Grodnitsky, 1999; Dudley, studies support the hypothesis that insects and their 2000). wings evolved from crustacean-like ancestors with A competing hypothesis is that insects are a sister moveable leg-derived gills. clade of crustaceans, whose wings evolved from mobile Additional support for the wings-from-gills model gills that already had the articulation, musculature comes from fossils of early pterygotes. A number of and neural pattern required for creating fluid dynamic early fossil insects possess both thoracic wings and forces. This hypothesis has received support from gill-like structures on their abdomen; these fossils recent phylogenetic and developmental studies (see have led Kukalova¢-Peck (1991) to conclude that the below), yet it remains to be determined precisely how coexistence of wings and abdominal plate gills is the gills could have evolved into wings. In the study pre- primitive pterygote condition. Fossil insects possess- sented here, our aim is not to resolve competing phylo- ing both wings and what appear to be gills, from the genetic and anatomical hypotheses, but rather to use upper Carboniferous and lower Permian, are abun- the wings-from-gills model as a starting point to dant and taxonomically diverse (see Fig. 1a–d; examine the behaviour and morphology of one modern Kukalova¢-Peck, 1978, 1991), including examples from species, Diamphipnopsis samali Illies (Plecoptera, the stem groups that led to modern Ephemeroptera, Eusthenioidea, Diamphipnoidae), that may have par- Hemiptera and Plecoptera, along with the extinct ticular bearing on how gills could have evolved into order Megasecoptera. Although it cannot be deter- wings. mined with certainty that these structures did in fact Recent phylogenetic analyses based on molecular serve as gills, or even if these insects were associated (Friedrich & Tautz, 1995; Regier & Schultz, 1997; with water, the similarity of the structures in Aguinaldo & Lake, 1998; Boore, Lavrov & Brown, Figure 1a–c with gills of modern mayflies, Euphaeid 1998; Winnepenninckx, Van de Peer & Backeljau, damselflies and Eusthenioid stoneflies makes this a 1998; Garcia-Machado et al., 1999; Hwang et al., reasonable interpretation. 2001), morphological (Strausfeld, 1998; Strausfeld The foregoing evidence is part of the empirical basis et al., 1998) and combined data sets (Giribet, for the wings-from-gills model, but for this hypothesis Edgecombe, & Wheeler, 2001) support the hypothesis to be robust it also requires a plausible mechanical that insects are a sister clade of the Crustacea (see pathway that could have transformed the structure also Annales de la Société Entomologique de France and function of appendages that served originally as (N.S), 2001, 37(1–2) for a mixture of supporting and gills to appendages that served ultimately as wings. In conflicting viewpoints). Recent data also indicate a this regard, the behaviour and mechanics of modern homology between crustacean gills and insect wings, Plecoptera and Ephemeroptera (stoneflies and may- based on the demonstration that two of the genes flies; these two orders arose near the base of the early involved in morphogenesis of a dorsal exite of the split between Neoptera and Palaeoptera and are brine shrimp gill are involved in a similar stage of thought to have retained many primitive morphologi- development in Drosophila wings (Averof & Cohen, cal features) are potentially informative. Various 1997). Drosophila carrying mutant forms of ultra- stoneflies and mayflies use aerodynamic locomotion to bithorax and abdominal-a homeotic genes develop move in two dimensions across the surface of water, in appendage primordia on their abdominal segments some cases by using fairly rudimentary wings and (Carroll, Weatherbee & Langeland, 1995) in the same wing motions (Marden & Kramer, 1994, 1995; Kramer locations that both fossil and certain modern insect & Marden, 1997; Ruffieux, Elouard & Sartori, 1998; nymphs have gills. Based on fossil evidence, these gills Marden et al., 2000). In stoneflies, these behaviours have long been argued to be serial homologues of the are basal and phylogenetically diverse (Thomas et al., thoracic appendages that became wings (Kukalova¢- 2000). Here we extend that line of studies by examin- Peck, 1978, 1983, 1987, 1991). Thus, it appears that ing D. samali stoneflies that possess the primitive modern homeotic regulation represses the initiation of pterygote condition of co-occurring wings and abdom- wing/gill development on all but the meso- and met- inal gills. athorax of extant adult pterygotes (Averof & Akam, Traditionally, a fundamental difficulty for the 1995; Carroll et al., 1995; Galant & Carroll, 2002; Ron-