What is metamorphosis?
The Henderson's dictionary of biology defines metamorphosis as "transformation of one structure into another" (Lawrence, 2005) but although accurate this is a fairly weak definition of one of the most spectacular phenomena in entomology and in biology as a whole. Not only insects and amphibians undergo this process, species from a wide variety of vertebrate and invertebrate groups also include some form of metamorphosis as part of their ontogeny (Bishop et al., 2006).
Even amongst the scientific community there are many different opinions of what constitutes metamorphosis. At the symposium "Metamorphosis: A multikingdom approach" in Florida in 2006, Andreas Heyland defined this process as "a life-history transition that involves radical changes in habitat, morphology and physiology" (Bishop et al., 2006).
However in contrast, at the same symposium, Christos Georgiou controversially describes metamorphosis as "the whole process whereby the final organisation and pattern of the organism is established" in all eukaryotes and that the word itself is "a synonym of morphogenesis".
Michael Hadfield stated that "there can be no absolute definition for metamorphosis" due to the wide variety of forms and mechanisms controlling it, and the different evolutionary pathways by which it arose, and so " the most important thing is that the person using the word defines what he or she means by metamorphosis in the context he or she is writing" (Bishop et al., 2006).
Different insect life histories
One of the reasons that insects are so successful is that all insects possess a complex chitinous outer cuticle, which as well as providing a strong support for the muscles needed for movement including flight (Gullan & Cranston, 2005), offers both physical protection and a barrier against desiccation (Gillott, 1995). However, when sclerotinized (a process of hardening the cuticle, also known as tanning), this rigid outer layer prevents continuous growth like that in animals with a less inflexible outer layer and the insect must episodically moult its cuticle, and produce a larger one in order to grow(Chapman, 1998; Gullan & Cranston, 2005). This discontinuous growth and subsequent movement towards increasing differences between juvenile and adult for the reasons mentioned in the previous section has lead to the evolution of three distinct life history patterns; ametaboly, hemimetaboly and holometaboly.
In the primitive developmental strategy, retained by the Thysanura and Archaeognatha which are wingless, eclosion reveals a miniature adult, with only the genitalia absent (Gillott, 1995; Gullan & Cranston, 2005). Moulting continues after the adult stage is reached and the number of moults can be vast, with the firebrat Thermobia domestica moulting as many as 60 times (Gillott, 1995).
Hemimetabolous development occurs in the primitive winged insects such as (*) and involves incomplete metamorphosis (Gullan & Cranston, 2005). The juvenile hemimetabolous insect, known as the nymph, is smaller than the adult and does not possess wings or genitalia, however some may have specialist nymphal features (Chapman, 1998) such as the gills of the aquatic nymphs of the Ephemoptera, Odonata and Plecoptera (Gullan & Cranston, 2005). The nymph undergoes a fixed number of moults, at each one external wing-buds increase in size until the final adult moult, at which the wings emerge, along with the genitalia and the nymphal features are lost (Erezyilmaz, 2006; Gillott, 1995).
In some phyla, such as the Odonata and the Orthoptera the hatchling that emerges at eclosion (Gullan & Cranston, 2005) resembles the holometabolous larva, but is in fact the first nymphal stage still enclosed in the second embryonic cuticle (Bernays, 1971; Bernays, 1972) this is known as the pronymph (Gullan & Cranston, 2005). The pronymph is normally the final stage before hatching occurs, feeding on yolk from the egg (Gullan & Cranston, 2005) however in Odonata and the Orthoptera it is the pronymph that hatches and undergoes independent movement in order to place itself in an area suitable for nymphal development (Gullan & Cranston, 2005) for example the eggs of many Orthoptera such as Schistocerca gregaria and Schistocerca nitens are laid underground and the pronymph hatches and digs upwards to reach the surface (Gillott, 1995)damage that may be caused while digging (Bernays, 1971).
Holometabolous insects are thought to have evolved from hemimetabolous insects in the Permian (Kukalov-Peck, 1978) and include some of the world's most successful and recognisable phyla such as the Hymenoptera and the Lepidoptera. This strategy is the most spectacular and involves three developmental stages after eclosion; a feeding larva, a non-feeding usually immotile pupa and a winged (or secondarily wingless) adult (Gillott, 1995; Gullan & Cranston, 2005). They are wingless, and unlike the hemimetabolous nymphal stages, bear no visible external wing precursors (Gillott, 1995). Instead, wings develop in the pupal stage from internal imaginal discs, cells laid aside for adult structures during the larval stage(Gillott, 1995; Gullan & Cranston, 2005)(needs more references). Larvae are different to adults both in morphology and habitat and may take one of three forms; oligopod (thought to be the most primitive), polypod (caterpillar-like) and apod (maggot-like)(Gillott, 1995). The non-feeding pupal stage defines this strategy in that it is the stage in which metamorphosis occurs. Within this period of accelerated growth, adult tissues are formed from larval structures, and imaginal discs are differentiated into adult organs such as wings (Gullan & Cranston, 2005). The immotile pupa faces a significant risk of predation and therefore may be protected by a cocoon made of silk and/or other materials such as small stones or it may reside underground (Gillott, 1995). Adult holometabolous insects are typically the dispersal and reproductive stage, and thus possess wings and genitals (Goodisman et al., 2005).
Larval transfer by hybridisation
Williamson proposed in 2009 that insects, as well as crustaceans and other marine invertebrates, obtained their larval forms by sexual hybridisation with another taxon rather than by Darwinian "decent by modification"(Williamson, 2009). He suggested that the nauplius larvae of Crustaceans resulted from a hybridisation event with a non-crustacean Arthropod (Williamson & Rice, 1996) and in 2001 he proposed that the name of this phylum should be "Naupliomorpha" (Williamson, 2001). In his most recent paper, Williamson applies his "larval transfer hypothesis" to insects and proposes that the holometabolous larva, such as the caterpillars of Lepidopterans, were "acquired larvae" originating as members of the visually similar Onychophora (Williamson, 2009). As part of this paper, almost as a substitute to supporting his claims with references from the academic texts, he suggests a "research proposal" to allow proof of his theory.
Williamson's 2009 radical 2009 paper sparked much interest in the field of evolutionary biology, not least because of its publishing in PNAS with a lack of peer review (Giribet, 2009). His "research proposal" also proved unfounded as much of the research he suggested had not only been completed previously but disproved his theory. For example, in contrast to his suggestion that holometabolous insects will have much larger genomes than insect phyla without larvae because they contain genes transferred from Onychophorans (Williamson, 2009), Hart and Grosberg (2009) consulted the genome size database compiled by Gregory (Gregory, 2009) and concluded that in reality, holometabolous insects have smaller genomes than many hemi- and ametabolous insects (Hart & Grosberg, 2009). In fact, all the holometabolous insects that have so far had their genomes analysed had numbers of base pairs that exceeded 1.956 x 109 whereas members of the Orthoptera, a well known hemimetabolous phylum had genomes that had numbers of base pairs reaching 1.5648 x 1010(Gregory, 2002) the largest Orthopteran genome found so far is the Mountain grasshopper, Podisma pedestris which has 1.655754 x 1010 base pairs (Gregory, 2009).
In addition, research carried out by Roeding et al in 2007 proves that contrary to Williamson's claims that the genomes of holometabolous insects will contain the genome of an Onychophoran (Williamson, 2009), Onychophorans have no closer genome similarity to holometabolan insects than they do to hemimetabolous insects or even to crustaceans (Roeding et al., 2007).
Williamson also uses the general scientific acceptance of the endosymbiont theory of the acquisition of eukaryote organelles as proof that "fusion of lineages" can occur and therefore as support to his theory of larval transfer (Williamson, 2001). However, two organisms living in symbioses, even though one may be an endosymbiont, is very different to his proposal that two organisms hybridised to form the larval and adult forms respectively of one of the original organisms, and is supported by molecular and genetic evidence (Dyall, Brown & Johnson, 2004) unlike Williamson's theory.
Balfour (1881)as cited in (Williamson, 2009) is quoted as having also "independently concluded" the same theory of hybridisation being the source of larval forms can be forgiven for this view that such a radical transformation of appearance within the life of an organism cannot be explained by the theory of evolution alone which is all that would have been available to him at his time of writing. However, this outmoded approach is unnecessary for Williamson as there is now a plethora of data available to categorically disprove this theory.
Bernays, E. A. (1971). The vermiform larva of Schistocerca gregaria (Forskl): Form and activity (Insecta, Orthoptera). Zoomorphology 70, 183-200.
Bernays, E. A. (1972). The muscles of newly hatched Schistocerca gregaria larvae and their possible functions in hatching, digging and ecdysial movements (Insecta: Acrididae). Journal of Zoology 166, 141-158.
Bishop, C. D., Erezyilmaz, D. F., Flatt, T., Georgiou, C. D., Hadfield, M. G., Heyland, A., Hodin, J., Jacobs, M. W., Maslakova, S. A., Pires, A., Reitzel, A. M., Santagata, S., Tanaka, K. & Youson, J. H. (2006). What is metamorphosis? Integrative and Comparative Biology 46, 655-661.
Chapman, R. F. (1998). The Insects: Structure and Function, 4 edition. Cambridge University Press.
Dyall, S. D., Brown, M. T. & Johnson, P. J. (2004). Ancient Invasions: From Endosymbionts to Organelles. Science 304, 253-257.
Erezyilmaz, D. F. (2006). Imperfect eggs and oviform nymphs: a history of ideas about the origins of insect metamorphosis. Integrative and Comparative Biology 46, 795-807.
Gillott, C. (1995). Entomology, 2 edition. Plenum Press.
Giribet, G. (2009). On velvet worms and caterpillars: Science, fiction, or science fiction? Proceedings of the National Academy of Sciences 106, E131-E131.
Goodisman, M. A. D., Isoe, J., Wheeler, D. E. & Wells, M. A. (2005). Evolution of Insect Metamorphosis: A Microarray-Based Study of Larval and Adult Gene Expression in the Ant Camponotus festinatus. Evolution 59, 858-870.
Gregory, T. R. (2002). Genome size and developmental complexity. Genetica 115, 131-146.
Gregory, T. R. (2009). Animal Genome Size Database.
Gullan, P. J. & Cranston, P. S. (2005). The insects: an outline of entomology, 3 edition. Blackwell Publishing.
Hart, M. W. & Grosberg, R. K. (2009). Caterpillars did not evolve from onychophorans by hybridogenesis. Proceedings of the National Academy of Sciences 106, 19906-19909.
Kukalov-Peck, J. (1978). Origin and evolution of insect wings and their relation to Metamorphosis, as documented by the fossil record. Journal of Morphology 156, 53-125.
Lawrence, E. (2005). Henderson's Dictionary of Biology, 13 edition. Pearson Education.
Roeding, F., Hagner-Holler, S., Ruhberg, H., Ebersberger, I., von Haeseler, A., Kube, M., Reinhardt, R. & Burmester, T. (2007). EST sequencing of Onychophora and phylogenomic analysis of Metazoa. Molecular Phylogenetics and Evolution 45, 942-951.
Williamson, D. I. (2001). Larval transfer and the origins of larvae. Zoological Journal of the Linnean Society 131, 111-122.
Williamson, D. I. (2009). Caterpillars evolved from onychophorans by hybridogenesis. Proceedings of the National Academy of Sciences 106, 19901-19905.
Williamson, D. I. & Rice, A. L. (1996). Larval Evolution in the Crustacea. Crustaceana 69, 267-287.