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The Evolution of Flightlessness in Insects.
Session Leader: Wendy Moore
"Although insects evolved in the Devonian, they did not become markedly successful until taxa capable of flight appeared in the lower Carboniferous" (Wagner and Liebherr 1992)
"Wings have contributed more to the success of insects than any other anatomical structure" (Daly, et al. 1978)
Flightlessness has evolved in the vast majority of insect orders, and multiple times within many of these orders (see table 1). Among insect species some are exclusively (i.e. monomorphic) flightless, some are exclusively (i.e. monomorphic) flyers, and others are dimorphic with both flying and non-flying individuals. Non-flying individuals may be wingless, or they may have reduced/shortened wings (i.e. brachyptery). Flying insects typically have fully-developed, "long" wings (i.e. macroptery).
The current paradigm of evolution of flightlessness views the dimorphic condition is viewed as an intermediate stage between a monomorphic, flying, macropterous ancestor and a monomorphic, flightless descendant. Nearly all published studies explicitly or implicitly incorporate this scenario.
WHY WOULD FLIGHTLESSNESS EVOLVE?
Why would natural selection repeatedly favor the loss of a structure which is generally attributed with being the key evolutionary innovation leading to the success of the group (see Daly, et al. quote above)? This question has intrigued insect systematists ever since Darwin.
Scientists have seeked to anwser this question through two approaches, process analysis and pattern analysis. Process analyses have included investigations into the genetic, hormonal, and environmental control of flightlessness of different species. Investigations into these processes have provided insights regarding how wing conditions are inherited, how their development is hormonally controlled, and what the influence of biotic and abiotic environmental factors are during development. Pattern analyses have included historical/phylogenetic analyses as well as analyses of flightlessness as correlated with latitude, altitude, isolation, habitat stability, and life style.
The most broadly accepted hypotheses for loss of flight in insects have focused on loss of wings resulting from increased fitness of individuals. For example, wingless females can theoretically divert more of their energy into making eggs (rather than making wings and flight muscles, the latter comprising 10-20 percent of most insect's body weight). Such hypotheses are supported by two primary avenues of evidence. First, in insect ontogeny, there is concurrent development of the flight apparatus and ovaries, this has been termed the "oogenesis -flight" syndrome (Darlington 1936, Johnson 1969). In addition, Roff (1986) found in 26 intraspecific comparisons of wing polymorphic species, 21 were more fecund as short winged and 3 were more fecund as long winged. Secondly, many winged females shed their wings and/or autolyse their flight muscles during egg production.
WHERE DOES FLIGHTLESSNESS OCCUR?
Flightless insects are most often found:
- In stable habitats where, theoretically, dispersal by flight is not necessary for long-term survival of populations. Cited examples of such stable habitats are: mountains, tropical montane forests, caves, Pleistocene refugia, the ocean surface, deserts, termite and hymenopteran nests, and the body surfaces of homeothermic vertebrates. Insects that live in stable habitats and do not have to rely on flight for daily activities may particularly be selected for flightlessness.
- In isolated areas. Isolated habitats where flightless insects are found include: caves, inland sand dunes, high montane and coastal strand communities (Wagner and Liebherr 1992). Darwin hypothesized that flightlessness occurs on oceanic islands where dispersing individuals should experience higher mortality than non-dispersing individuals. However, recent work has shown that the incidence of flightlessness on islands is comparable to that of the mainland, unless it is a high island (Roff 1990). High (mountainous) islands are considered stable for the same reason that mainland mountains are viewed as stable, because insects came move relatively short distances vertically to compensate for seasonal or long-term climatic fluctuations (rather than relying on flight to move great distances in search of better conditions).
- In areas requiring a great amount of energy for flight. Flightlessness is often encountered where the energetic costs of flight are high (i.e. cold regions or areas of high winds). In many insect groups there is a trend toward increased brachyptery with increasing altitude and latitude.
- As parasites and commensals. Vertebrate ectoparasites contain the oldest and most diverse clades of flightless insects. These include, the Cimicidae (bedbugs), Polyctenidae (batbugs), Phthiraptera (biting lice), and Siphonaptera (fleas). Wing reduction or loss is also seen in termitophiles, myrmecophiles, bee and wasp inquilines.
- As parthenogenetic insects.
HOW DID FLIGHTLESSNESS EVOLVE?
Studies have shown that for some dimorphic species wing length is controlled by a single gene locus operating in a simple Mendelian fashion with brachyptery dominant (see Lindroth 1945 and Aukema 1990 for carabids; see Jackson 1928 for weevils). However, work on field crickets (Harrison 1979, McFarlane 1962), Heteroptera (Honek 1976), and Homoptera (Rose, 1972) has shown that wing morphology in these groups is under the control of many genes.
Roff (1986) concluded that wing morphology could be controlled either by a single gene locus or a polygene complex, but both can be regulated by a hormonal threshold model. For instance, if the level of a hormone, such as juvenile hormone, exceeds a threshold value during a critical developmental stage of the insect, wing expression could be suppressed (i.e. increased levels in JH lead to more juvenile characters - brachyptery). Topical application of JH to Gryllus crickets during the ultimate and penultimate nymphal instar allowed Zera and Tiebel (1988, 1989) to redirect development from macroptery to brachyptery.
Environmental factors that influence wing development include abiotic factors such as temperature (Aukema 1990) and photoperiod (Kimura and Masaki 1977) as well as biotic factors such as food resources (Aukema 1990) and population density. It could be that these environmental factors are affecting levels of juvenile hormone in the developing embryos or larvae.
Table 1: The taxonomic distribution of flightlessness in insect orders. Complied from Andersen (1997).
All orders are linked to the respective page in the Tree of Life.
- Andersen, N M. 1997. Phylogenetic tests of evolutionary scenarios: The evolution of flightlessness and wing polymorphism in insects. In: Grandcolas, P. (ed.), The Origin of Biodiversity in Insects: Phylogenetic Tests of Evolutionary Scenarios. Memoires du Museum National D'Histoire Naturelle 173(0):91-108.
- Kavanaugh, D.H. 1985. On wing atrophy in carabid beetles (Coleoptera: Carabidae), with special reference to Nearctic Nebria. Pages 408-431 In G.E. Ball, editor. Taxonomy, phylogeny and zoogeography of beetles and ants. Dr. W. Junk Publications, Dordrecht, The Netherlands.
Full references list
- Andersen, N.M. 1973. Seasonal polymorphism and developmental changes in organs of flight and reproduction in bivoltine pondskaters (Hem. Gerridae). Entomol. Scand. 4:1-20.
- Andersen, N.M. 1993. The evolution of wing polymorphism in water striders (Gerridae): a phylogenetic approach. Oikos 67:433-443.
- Aukema, B. 1990a. Wing-length determination in two wing-dimorphic Calathus species (Coleoptera: Carabidae). Hereditas 113:189-202.
- Aukema, B. 1990b. Taxonomy, life history, and distribution of three closely related species of the genus Calathus (Coleoptera: Carabidae). Tijdschr. Entomology 133:121-141.
- Aukema, B. 1995. The evolutionary significance of wing dimorphism in Carabid beetles (Coleoptera: Carabidae). Researches on Population Ecology 37(1):105-110.
- Breuhl, C A. 1997. Flightless insects: A test case for historical relationships of African mountains. Journal of Biogeography 24(2):233-250.
- Colgan, D J. 1992. Glycerol-3-Phosphate Dehydrogenase Isozyme Variation In Insects. Biological Journal of the Linnean Society 47(1):7-47.
- Cuellar, O. 1994. Biogeography of parthenogenetic animals. Biogeographica 70(1):1-13.
- Czachorowski, S. 1993. How and what from did insect wings originate? Przeglad Zoologiczny 37(3-4):207-218.
- Darlington, P.J. 1970. Carabidae on tropical islands, especially the West Indies. Biotropica 2:7-15.
- Denno R.F. 1994. The evolution of dispersal polymorphisms in insects: The influence of habitats, host plants and mates. Researches on Population Ecology 36(2):127-135.
- Denno, R.F., G.K. Roderick, K.L. Olmstead, and H.G. Dobel. 1991. Density-related migration in planthoppers (Homoptera: Delphacidae): The role of habitat persistence. American Naturalist 138:1513-1541.
- Denno, R.F., M.J. Raupp, D.W. Tallamy, and C.F. Reichelderfer. 1980. Migration in heterogeneous environments: Differences in habitat selection between the wing forms of the dimorphic planthopper, Prokelisia marginata (Homoptera: Delphacidae). Ecology 61: 859-867.
- Emerson, B.C. and G.P. Wallis. 1995. Phylogenetic relationships of the Prodontria (Coleoptera: Scarabaeidae: subfamily Melolonthinae), derived from sequence variation in the mitochondrial cytochrome oxidase II gene. Molecular Phylogenetics & Evolution 4(4):433-447.
- Fairbairn, D.J. 1994. Wing dimorphism and the migratory syndrome: correlated traits for migratory tendency in wing dimorphic species. Researches in Population Ecology 36(2):157-163.
- Fong, D.W., T.C. Kane, and D.C. Culver. 1995. Vestigialization and the loss of nonfunctional characters. Annual Review of Ecology and Systematics 26: 249-268.
- Hamilton, W.D. and R.M. May. 1977. Dispersal in stable habitats. Nature 269:578-581.
- Harrison, R.G. 1979. Flight polymorphism in the field cricket Gryllus pennsylvanicus. Oecologia (Berlin) 40:125-132.
- Harrison, R.G. 1980. Dispersal polymorphism in insects. Annual Review of Ecological Systematics 11:95-118.
- Heinze, J. and B. Hoelldobler. 1993. Queen polymorphism in an Australian weaver ant, Polyrhachis doddi. Psyche 100:83-92.
- Jackson, D.J. 1928. The inheritance of long and short wings in the weevil, Sitonia hispidula, with a discussion of wing reduction among beetles. Transactions of the Royal Society of Edinburgh 55-655-735.
- Kimura, T. and S. Masaki. 1977. Brachypterism and seasonal adaptation in Orgyia thyellina Butler (Lepidoptera, Lymantriidae). Kontyu 45:97-106.
- Lamb, R.J. and P.A. MacKay. 1979. Variability in migratory tendency within and among natural populations of the pea aphid, Acyrthosiphon pisum. Oecologia 39:289-299.
- Langdor, D.W. and D.J. Larson. 1983. Alary polymorphism and life history of a colonizing ground beetle, Bembidion lampros Herbst (Coleoptera: Carabidae). Coleopterist's Bulletin 37:365-377.
- Liebherr, J.K. 1988. Gene flow in ground beetles (Coleoptera: Carabidae) of differing habitat preference and flight-wing development. Evolution 42(1):129-137.
- Lindroth, C.H. 1945. Inheritance and wing dimorphism in Pterostichus anthracinus I11. Hereditas 32:37-40.
- McCoy, E.D. and J.R. Rey. 1981. Patterns of abundance, distribution, and alary polymorphism among the salt marsh Delphacidae (Homoptera: Fulgoroidea) of northwest Florida. Ecological Entomology 6:285-291.
- Roff, D.A. 1986. The evolution of wing dimorphism in insects. Evolution 40(5):1009-1020.
- Roff, D.A. 1990. The evolution of flightlessness in insects. Ecological Monographs 60:389-421.
- Roff, D.A. 1994. Evidence that the magnitude of the trade-off in a dichotomous trait is frequency dependent. Evolution 48:1650-1656.
- Roff D.A. 1994. The evolution of flightlessness: Is history important? Evolutionary Ecology 8(6):639-657.
- Roff, D.A. 1994. Why is there is much genetic variation for wing dimorphism? Researches in Population Ecology 32(2):145-150.
- Roff, D.A. 1995. Antagonistic and reinforcing pleiotropy: A study of differences in development time in wing dimorphic insects. Journal of Evolutionary Biology 8:405-419.
- Roff, D.A. and D.J. Fairbarn. 1994. The evolution of alternate morphologies: Fitness and wing morphology in male sand crickets. Evolution 47:1572-1584.
- Rose, D.J.W. 1972. Dispersal and quality in populations of Cicadulina
species (Cicadellidae). Journal of Animal Ecology 41:589-609.
- Southwood, T.R.E. 1962. Migration of terrestrial arthropods in relation to habitat. Biol. Rev. 37:171-214.
- Taylor, V.A. 1981. The adaptive and evolutionary significance of wing polymorphism and parthenogenesis in Ptinella Motschulsky (Coleoptera: Ptiliidae). Ecological Entomology 6:89-98.
- Thayer, M.K. 1992. Discovery of sexual wing dimorphism in (Coleoptera: Staphylinidae) Omalium flavidum and a discussion of wing dimorphism in insects. Journal of the New York Entomological Society 100:540-573.
- Waloff, N. 1983. Absence of wing polymorphism in the arboreal, phytophagous species of some taxa of temperate Hemiptera: an hypothesis. Ecological Entomology 8:229-232.
- Wagner, D.L. and J K. Liebherr. 1992. Flightlessness In Insects. Trends in Ecology & Evolution 7(7):216-220.
- Westermann, F. 1993. Wing polymorphism in Capnia bifrons (Plecoptera: Capniidae). Aquatic Insects 15:135-140.
- Wigglesworth, V.B. 1961. Insect polymorphism -- a tentative synthesis. Symposium of the Royal Entomological Society - London 1:103-113.
- Zera, A.J. 1984. Differences in survivorship, development rate, and fertility between the long-winged and wingless morphs of the waterstrider, Limnoporus canaliculatus. Evolution 38:1023-1032.
- Zera, A.J. and S. Mole. 1994. The physiological costs of flight capability in wing-dimorphic crickets. Researches on Population Ecology 36:151-156.
- Zera, A.J. and R.F. Denno. 1997. Physiology and ecology of dispersal polymorphism in insects. In Mittler, T.E., F.J. Radovsky and V.H. Resh, editors. Annual Review of Entomology, Vol. 42. x+666p. 207-230. Annual Reviews Inc.: Palo Alto, California, USA. ISBN 0-8243-0142-0.
- Zera, A.J. and K. Tiebel. 1989. Differences in juvenile hormone esterase activity between presumptive macropterous and brachypterous Gryllus rubens: implications for the hormonal control of wing polymorphism. Journal of Insect Physiology 35:7-17.
Copyright 1998, Wendy Moore.