Holometabolism, also called complete metamorphism, is a form of insect development which includes four life stages – as an embryo or egg, a larva, a pupa and an imago or adult. Holometabolism is a synapomorphic trait of all insects in the superorder Endopterygota. In some species the holometabolous life cycle prevents larvae from competing with adults because they inhabit different ecological niches. Accordingly, their morphology can be adapted to just one phase of activity, such as larvae feeding for growth and development, as opposed to adults flying for dispersal and seeking new supplies of food for their offspring. In some insects, the adults can protect and feed the younger stages.
General developmental stages
There are four general developmental stages, each with its own morphology.
The first stage is from the fertilization of the egg inside the mother until the embryo hatches. The insect starts as a single cell and then develops into the larval form before it hatches.
The second stage lasts from hatching or birth until the larva pupates. In most species this mobile stage is worm-like in form. Such larvae can be one of several general varieties:
Other species however may be campodeiform (a form reminiscent of members of the genus Campodea, elongated, more or less straight, flattened, and active, with functional legs). This stage is variously adapted to gaining and accumulating the materials and energy necessary for growth and metamorphosis.
The third stage is from pupation until eclosion. The pupae of most species hardly move at all, although the pupae of some species, such as mosquitoes, are mobile. In preparation for pupation, the larvae of many species construct a protective cocoon of silk or other material, such as its own accumulated faeces. There are three types of pupae: obtect, exarate, and coarctate. Obtect pupae are compact, with the legs and other appendages enclosed. Exarate pupae have their legs and other appendages free and extended. Coarctate pupae develop inside the larval skin. In this stage, the insect's physiology and functional structure, both internal and external, change drastically.
Adult holometabolous insects usually have wings (excepting where secondarily lost) and functioning reproductive organs. In this stage, reproduction is the top priority for queens and males.
Evolutionary context of holometabolan development
Around 45% to 60% of all known living species are holometabolan insects. Juveniles and adult forms of holometabolan insects often occupy different ecological niches, exploiting different resources. This fact is considered a key driver in the unusual evolutionary diversification of form and physiology within this group.
According to the latest phylogenetic reconstructions, holometabolan insects are monophyletic, which suggests that the evolutionary innovation of complete metamorphosis occurred only once. Paleontological evidence shows that the first winged insects appeared in the Paleozoic. Carboniferous fossil samples (approximately 350 Ma) already display a remarkable diversity of species with functional wings. These fossil remains show that the primitive Apterygota and the ancient winged insects were ametabolous (completely lacking metamorphosis). By the end of the Carboniferous, and into the Permian (approximately 300 Ma), most pterygotes had post-embryonic development which included separated nymphal and adult stages, which shows that hemimetaboly had already evolved. The earliest known fossil insects that can be considered holometabolan appear in the Permian strata (approximately 280 Ma). Phylogenetic studies also show that the sister group of Endopterygota is paraneoptera, which includes hemimetabolan species and a number of neometabolan groups. The most parsimonious evolutionary hypothesis is that holometabolans originated from hemimetabolan ancestors.
Theories on the origin of holometabolan metamorphosis
The origin of complete metamorphosis in insects has been the subject of a long lasting, and at times fierce, debate. One of the first theories proposed was one by William Harvey in 1651. Harvey suggested that the nutrients contained within the insect egg is so scarce that there was selection for the embryo to be forced to hatch before the completion of development. During the post-hatch larval life, the ‘desembryonized’ animal would accumulate resources from the external environment and reach the pupal stage, which Harvey viewed as the perfect egg form. However, Jan Swammerdam conducted a dissection study and showed that pupal forms are not egg-like, but instead more of a transitional stage between larvae and adult.
In 1883, John Lubbock revitalized Harvey’s hypothesis and argued that the origin and evolution of holometabolan development can be explained by the precocious eclosion of the embryo. Hemimetabolan species, whose larvae look like the adult, have an embryo that completes all developmental stages (namely: ‘protopod’, ‘polipod’, and ‘oligopod’ stages) inside the eggshell. Holometabolan species instead have vermiform larvae and a pupal stage after incomplete development and hatching. The debate continued through the twentieth century, with some authors (like Charles Pérez in 1902) claiming the precocious eclosion theory outlandish, Antonio Berlese reestablishing it as the leading theory in 1913, and Augustus Daniel Imms disseminating it widely among Anglo-Saxon readers from 1925 (see Wigglesworth 1954 for review). One of the most contentious aspects of the precocious eclosion theory that fueled further debate in the field of evolution and development was the proposal that the hemimetabolan nymphal stages are equivalent to the holometabolan pupal stage. Critics of this theory (most notably, H.E. Hinton) argue that post-embryonic development in hemimetabolans and holometabolans are equivalent, and rather the last nymphal instar stage of hemimetabolans would be homologous to the holometabolan pupae. More modern opinions still oscillate between these two conceptions of the hemi- to holometabolan evolutionary trend.
J.W. Truman and L.M. Riddiford, in 1999, revitalized the precocious eclosion theory with a focus on endocrine control of metamorphosis. They postulated that hemimetabolan species hatch after three embryonic 'moults' into a nymphal form similar to the adult, whereas holometabolan species hatch after only two embryonic 'moults' into vermiform larvae that are very different from the adult. In 2005, however, B Konopova and J Zrzavý reported ultrastructural studies across a wide range of hemimetabolan and holometabolan species and showed that the embryo of all species in both groups produce three cuticular depositions. The only exception was the Diptera Cyclorrhapha (unranked taxon of ‘high’ Dipterans, within the infraorder Muscomorpha, which includes the highly studied D. melanogaster) which has two embryonic cuticles, most likely due to secondary loss of the third. Critics of the precocious eclosion theory also argue that the larval forms of holometabolans are very often more specialized than those of hemimetabolans. X. Bellés illustrates that the maggot of a fruitfly “cannot be envisaged as a vermiform and apodous (legless) creature that hatched in an early embryonic stage.” It is in fact extremely specialized: for example, the cardiostipes and dististipes of the mouth are fused, as in some mosquitoes, and these parts are also fused to the mandibles and thus form the typical mouth hooks of fly larvae. Maggots are also secondarily, and not primitively, apodous. They are more derived and specialized than the cockroach nymph, a comparable and characteristic hemimetabolan example.
More recently, an increased focus on the hormonal control of insect metamorphosis has helped resolve some of the evolutionary links between hemi- and holometabolan groups. In particular, the orchestration of the Juvenile Hormone (JH) and ecdysteriods in molting and metamorphosis processes has received much attention. The molecular pathway for metamorphosis is now well described: periodic pulses of ecdysteroids induce molting to another immature instar (nymphal in hememetabolan and larval in holometabolan species) in the presence of JH, but the programmed cessation of JH synthesis in instars of a threshold size leads to ecdysteroid secretion inducing metamorphosis. Experimental studies show that, with the exception of higher Diptera, treatment of the final instar stage with JH causes an additional immature molt and repetition of that stage. The increased understanding of the hormonal pathway involved in metamorphosis enabled direct comparison between hemimetabolan and holometabolan development. Most notably, the transcription factor Krüppel homolog 1 (Kr-h1) which is another important antimetamorphic transducer of the JH pathway (initially demonstrated in D. melanogaster and in the beetle T. castaneum) has been used to compare hemimetabolan and holometabolan metamorphosis. Namely, the Krüppel homolog 1 discovered in the cockroach B. germanica (a representative hemimatabolan species), ‘BgKr-h1’, was shown to be extremely similar to orthologues in other insects from holometabolan orders. Compared to many other sequences, the level of conservation is high, even between B. germanica and D. melanogaster, a highly derived holometabolan species. The conservation is especially high in the C2H2 Zn finger domain of the homologous transducer, which is the most complex binding site. This high degree of conservation of the C2H2 Zn finger domain in all studied species suggests that the Kr-h1 transducer function, an important part of the metamorphic process, might have been generally conserved across the entire class Insecta.
In 2009 a retired British planktologist Donald I. Williamson published a controversial paper in the journal Proceedings of the National Academy of Sciences (via Academy member Lynn Margulis through a unique submission route in PNAS that allowed members to peer review manuscripts submitted by colleagues), wherein Williamson claimed that the caterpillar larval form originated from velvet worms through hybridogenesis with other organisms, giving rising to holometabolan species. This paper was met with severe criticism, and spurred a heated debate in the literature.
The Orders that contain holometabolous insects are :