Flightlessness in mayflies and its relevance to hypotheses on the origin of insect flight

Ruffieux, Laurence; Elouard, Jean-Marc; Sartori, Michel

doi:10.1098/rspb.1998.0550

Cited by 22 publications

(16 citation statements)

References 30 publications

(27 reference statements)

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“…This interpretation fits nicely with the hypothesis that predation by modern surface-feeding fish makes skimming a dangerous form of locomotion for most extant species (6,7) and thus a largely obsolete behavior that is now used primarily for emergency escape from accidental contact with water. Winter stoneflies (taeniopterigids and capniids), which are active during seasons when fish do not feed at the surface, make routine use of skimming (3)(4), as do certain flightless mayflies (Ephemeroptera) that inhabit rivers in Madagascar that lack insectivorous fish (6). For stoneflies and insects in general, a gradual increase in the intensity of predation at the water surface may have driven a radiation away from routine use of skimming.…”

Section: Discussionsupporting

confidence: 68%

“…How can tiny wings, simple wing hinges, and weak muscles provide a functional advantage over no wings at all? A novel solution to this riddle was recently provided by the discovery of surface skimming, a nonflying form of aerodynamic locomotion used by certain stoneflies (Plecoptera) and mayflies (Ephemeroptera) to move in two dimensions across water surfaces (3)(4)(5)(6)(7). By flapping their wings or by using them as nonflapping sails while their weight is supported by water, skimmers can achieve effective aerodynamic locomotion even with small wings and weak flight muscles (3,4).…”

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confidence: 99%

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Molecular phylogenetic analysis of evolutionary trends in stonefly wing structure and locomotor behavior

Thomas

Walsh

Wolf

et al. 2000

Proc. Natl. Acad. Sci. U.S.A.

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Insects in the order Plecoptera (stoneflies) use a form of two-dimensional aerodynamic locomotion called surface skimming to move across water surfaces. Because their weight is supported by water, skimmers can achieve effective aerodynamic locomotion even with small wings and weak flight muscles. These mechanical features stimulated the hypothesis that surface skimming may have been an intermediate stage in the evolution of insect flight, which has perhaps been retained in certain modern stoneflies. Here we present a phylogeny of Plecoptera based on nucleotide sequence data from the small subunit rRNA (18S) gene. By mapping locomotor behavior and wing structural data onto the phylogeny, we distinguish between the competing hypotheses that skimming is a retained ancestral trait or, alternatively, a relatively recent loss of flight. Our results show that basal stoneflies are surface skimmers, and that various forms of surface skimming are distributed widely across the plecopteran phylogeny. Stonefly wings show evolutionary trends in the number of cross veins and the thickness of the cuticle of the longitudinal veins that are consistent with elaboration and diversification of flight-related traits. These data support the hypothesis that the first stoneflies were surface skimmers, and that wing structures important for aerial flight have become elaborated and more diverse during the radiation of modern stoneflies.

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Section: Discussionsupporting

confidence: 68%

mentioning

confidence: 99%

Molecular phylogenetic analysis of evolutionary trends in stonefly wing structure and locomotor behavior

Thomas

Walsh

Wolf

et al. 2000

Proc. Natl. Acad. Sci. U.S.A.

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“…, 1985). Energy reserves, mainly lipid, have been determined in some mayfly species, but seasonal changes have not been examined extensively (Landrum & Poore, 1988; Meyer, 1990; Bell, Ghioni & Sargent, 1994; Ghioni, Bell & Sargent, 1996; Ruffieux, Elouard & Sartori, 1998; Meier, Meyer & Meyns, 2000).…”

Section: Introductionmentioning

confidence: 99%

Temporal variation of energy reserves in mayfly nymphs (Hexagenia spp.) from Lake St Clair and western Lake Erie

et al. 2003

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Summary 1. We analysed changes in energy reserves (lipid and glycogen) and length–weight relationships of burrowing mayflies (Hexagenia spp.) in 1997–99 to compare an established population in Lake St Clair with a recovering population in western Lake Erie of the Laurentian Great Lakes. In addition, we measured changes in water temperature and potential food in both water columns and sediments. 2. Although overall mean values of lipid and glycogen levels of Hexagenia nymphs from Lake St Clair and western Lake Erie were not significantly different, there were differences in seasonal patterns between the two lakes. In Lake St Clair, levels were highest in early spring, declined throughout the year, and reached their lowest levels in fall during all 3 years of study. In contrast, levels in western Lake Erie were lower in spring, increased to a maximum in summer, then declined in fall. Seasonal patterns in length–weight relationships were similar to those for lipid and glycogen. 3. Total lipid as a percentage of dry weight did not increase with developmental stage of nymphs until just prior to metamorphosis and emergence from water. However, the major reserve lipid, triacylglycerols, increased systematically with development stage. In the final stage of development, triacylglycerols declined, probably as a result of energy consumption and its conversion to other biochemical components for metamorphosis and reproduction. 4. Indicators of potential food (algal fluorescence in the water column and chlorophyll a and chlorophyll a/phaeophytin ratio in sediments) suggest that Hexagenia in Lake St Clair have a food source that is benthic based, especially in early spring, whereas in western Lake Erie nymphs have a food source that is water column based and settles to the lake bottom during late spring and summer.

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“…Protopterygotes could also have used wing-like structures in air either to drift passively or to skim actively along water surfaces, as do many extant insect taxa (118)(119)(120)(121)(122). This behavior is probably a derived rather than a retained ancestral trait of winged insects (61,123,124). Although improbable for reasons outlined above, biomechanical considerations suggest that aquatic protopterygotes would have been unlikely to evolve wings that served aerodynamic functions.…”

Section: Origins Of Flight In Insectsmentioning

confidence: 99%

The Evolutionary Physiology of Animal Flight: Paleobiological and Present Perspectives

Dudley

2000

Annu. Rev. Physiol.

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Recent geophysical analyses suggest the presence of a late Paleozoic oxygen pulse beginning in the late Devonian and continuing through to the late Carboniferous. During this period, plant terrestrialization and global carbon deposition resulted in a dramatic increase in atmospheric oxygen levels, ultimately yielding concentrations potentially as high as 35% relative to the contemporary value of 21%. Such hyperoxia of the late Paleozoic atmosphere may have physiologically facilitated the initial evolution of insect flight metabolism. Widespread gigantism in late Paleozoic insects and other arthropods is also consistent with enhanced oxygen flux within diffusion-limited tracheal systems. Because total atmospheric pressure increases with increased oxygen partial pressure, concurrently hyperdense conditions would have augmented aerodynamic force production in early forms of flying insects. By the late Permian, evolution of decompositional microbial and fungal communities, together with disequilibrium in rates of carbon deposition, gradually reduced oxygen concentrations to values possibly as low as 15%. The disappearance of giant insects by the end of the Permian is consistent with extinction of these taxa for reasons of asphyxiation on a geological time scale. As with winged insects, the multiple historical origins of vertebrate flight in the late Jurassic and Cretaceous correlate temporally with periods of elevated atmospheric oxygen. Much discussion of flight performance in Archaeopteryx assumes a contemporary atmospheric composition. Elevated oxygen levels in the mid-to late Mesozoic would, however, have facilitated aerodynamic force production and enhanced muscle power output for ancestral birds, as well as for precursors to bats and pterosaurs.

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Flightlessness in mayflies and its relevance to hypotheses on the origin of insect flight

Cited by 22 publications

References 30 publications

Molecular phylogenetic analysis of evolutionary trends in stonefly wing structure and locomotor behavior

Molecular phylogenetic analysis of evolutionary trends in stonefly wing structure and locomotor behavior

Temporal variation of energy reserves in mayfly nymphs (Hexagenia spp.) from Lake St Clair and western Lake Erie

The Evolutionary Physiology of Animal Flight: Paleobiological and Present Perspectives

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