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Lifestages of a holometabolous insect (wasp). Egg is not shown. Third, fourth, and fifth images depict different ages of pupae. Ontwikkelstadia wespenpoppen.jpg
Lifestages of a holometabolous insect (wasp). Egg is not shown. Third, fourth, and fifth images depict different ages of pupae.

Holometabolism, also called complete metamorphosis , is a form of insect development which includes four life stages: egg, larva, pupa, and imago (or adult). Holometabolism is a synapomorphic trait of all insects in the superorder Endopterygota. Immature stages of holometabolous insects are very different from the mature stage. In some species the holometabolous life cycle prevents larvae from competing with adults because they inhabit different ecological niches. The morphology and behavior of each stage are adapted for different activities. For example, larval traits maximize feeding, growth, and development, while adult traits enable dispersal, mating, and egg laying. Some species of holometabolous insects protect and feed their offspring. Other insect developmental strategies include ametabolism and hemimetabolism.


Developmental stages

There are four general developmental stages, each with its own morphology and function.

Various insect eggs. PSM V48 D269 Insect eggs.jpg
Various insect eggs.


The first stage of the insect life cycle is the egg, or embryo, for all developmental strategies. The egg begins as a single cell which divides and develops into the larval form before hatching. Some insects reproduce by parthenogenesis or may be haplodiploid, and produce viable eggs without fertilization. The egg stage in most insects is very short, only a few days. However, insects may hibernate, or undergo diapause in the egg stage to avoid extreme conditions, in which case this stage can last several months. The eggs of some types of insects, such as tsetse flies, or aphids (which are hemimetabolous), hatch before they are laid.

Scarabaeiform larva and exarate pupae of a rhinoceros beetle. Annual report of the Regents (1891) (14595203290).jpg
Scarabaeiform larva and exarate pupae of a rhinoceros beetle.


The second stage of the holometabolous life cycle is the larva (plural: larvae). Many adult insects lay their eggs directly onto a food source so the larvae may begin eating as soon as they hatch. Larvae never possess wings or wing buds, and have simple rather than compound eyes. [1] In most species, the larval stage is mobile and worm-like in form. Larvae can be classified by their body type:

The larval stage is variously adapted to gaining and accumulating the materials and energy necessary for growth and metamorphosis. Most holometabolous insects pass through several larval stages, or instars, as they grow and develop. The larva must moult to pass from each larval stage. These stages may look very similar and differ mostly in size, or may differ in many characteristics including, behavior, color, hairs, and spines, and even number of legs. Differences between larval stages are especially pronounced in insects with hypermetamorphosis. The final larval stage in some insects is called a prepupa. Prepupae do not feed, and become inactive. [1]

Rhopalomyia solidaginis, pupa and emerging adult. Emergent midge. Rhopalomyia solidaginis.jpg
Rhopalomyia solidaginis , pupa and emerging adult.


To enter the third stage of homometabolous development, the larva undergoes metamorphosis into a pupa. The pupa is a quiescent, non-feeding developmental stage. Most pupae move very little, although the pupae of some species, such as mosquitoes, are mobile. In preparation for pupation, the larvae of many species seek protected sites or construct a protective cocoon of silk or other material, such as its own accumulated feces. Some insects undergo diapause as pupa. In this stage, the insect's physiology and functional structure, both internal and external, change drastically.

Pupae can be classified into three types: obtect, exarate, and coarctate. Obtect pupae are compact, with the legs and other appendages enclosed, such as a butterfly chrysalis. Exarate pupae have their legs and other appendages free and extended. Coarctate pupae develop inside the larval skin.


The final stage of holometabolous insect development is the adult, or imago. Most adult insects have wings (excepting where secondarily lost) and functioning reproductive organs. Most adult insects grow very little after eclosion from the pupa. Some adult insects do not feed at all, and focus entirely on mating and reproduction. Some adult insects are postmitotic at adult emergence, with dividing cells restricted to specific organs. Cyrtodiopsis dalmanni is one such species, that does feed in the adult stage but does not grow in size. Nutrition is utilized in adults for growth of the internal reproductive structures. [2]

Evolutionary context of holometabolan development

Around 45% to 60% of all known living species are holometabolan insects. [3] 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, [4] [5] 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).[ citation needed ] 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). [6] [7] Phylogenetic studies also show that the sister group of Endopterygota is paraneoptera, which includes hemimetabolan species and a number of neometabolan groups. [8] 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 are 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. [8]

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 [9] ). 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 [10] ) 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. [11] In 2005, however, B. Konopová 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. [12] The only exception was the Diptera Cyclorrhapha (unranked taxon of "high" Dipterans, within the infraorder Muscomorpha, which includes the highly studied Drosophila 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. Belles 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. [13]

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 ecdysteroids 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 hemimetabolan 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 Tribolium castaneum) has been used to compare hemimetabolan and holometabolan metamorphosis. Namely, the Krüppel homolog 1 discovered in the cockroach Blattella 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. [14] 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. [15] This paper was met with severe criticism, and spurred a heated debate in the literature.


The Orders that contain holometabolous insects are:

See also

Related Research Articles

Metamorphosis Profound change in body structure during the postembryonic development of an organism

Metamorphosis is a biological process by which an animal physically develops after birth or hatching, involving a conspicuous and relatively abrupt change in the animal's body structure through cell growth and differentiation. Some insects, fish, amphibians, mollusks, crustaceans, cnidarians, echinoderms, and tunicates undergo metamorphosis, which is often accompanied by a change of nutrition source or behavior. Animals can be divided into species that undergo complete metamorphosis ("holometaboly"), incomplete metamorphosis ("hemimetaboly"), or no metamorphosis ("ametaboly").

Larva Juvenile form of distinct animals before metamorphosis

A larva is a distinct juvenile form many animals undergo before metamorphosis into adults. Animals with indirect development such as insects, amphibians, or cnidarians typically have a larval phase of their life cycle.

Whitefly Family of insects

Whiteflies are Hemipterans that typically feed on the undersides of plant leaves. They comprise the family Aleyrodidae, the only family in the superfamily Aleyrodoidea. More than 1550 species have been described.

Pupa Life stage of some insects undergoing transformation

A pupa is the life stage of some insects undergoing transformation between immature and mature stages. Insects that go through a pupal stage are holometabolous: they go through four distinct stages in their life cycle, the stages thereof being egg, larva, pupa, and imago. The processes of entering and completing the pupal stage are controlled by the insect's hormones, especially juvenile hormone, prothoracicotropic hormone, and ecdysone. The act of becoming a pupa is called pupation, and the act of emerging from the pupal case is called eclosion or emergence.

Instar Developmental stage of arthropods between moults

An instar is a developmental stage of arthropods, such as insects, between each moult (ecdysis), until sexual maturity is reached. Arthropods must shed the exoskeleton in order to grow or assume a new form. Differences between instars can often be seen in altered body proportions, colors, patterns, changes in the number of body segments or head width. After moulting, i.e. shedding their exoskeleton, the juvenile arthropods continue in their life cycle until they either pupate or moult again. The instar period of growth is fixed; however, in some insects, like the salvinia stem-borer moth, the number of instars depends on early larval nutrition. Some arthropods can continue to moult after sexual maturity, but the stages between these subsequent moults are generally not called instars.

<i>Manduca sexta</i> Species of moth

Manduca sexta is a moth of the family Sphingidae present through much of the American continent. The species was first described by Carl Linnaeus in his 1763 Centuria Insectorum.

In animal dormancy, diapause is the delay in development in response to regularly and recurring periods of adverse environmental conditions. It is a physiological state with very specific initiating and inhibiting conditions. The mechanism is a means of surviving predictable, unfavorable environmental conditions, such as temperature extremes, drought, or reduced food availability. Diapause is observed in all the life stages of arthropods, especially insects. Embryonic diapause, a somewhat similar phenomenon, occurs in over 130 species of mammals, possibly even in humans, and in the embryos of many of the oviparous species of fish in the order Cyprinodontiformes.

<i>Polygonia interrogationis</i> Species of butterfly

Polygonia interrogationis, the question mark, is a North American nymphalid butterfly. It lives in wooded areas, city parks, generally in areas with a combination of trees and open space. The color and textured appearance of the underside of its wings combine to provide camouflage that resembles a dead leaf. The adult butterfly has a wingspan of 4.5–7.6 cm (1.8–3.0 in). Its flight period is from May to September. "The silver mark on the underside of the hindwing is broken into two parts, a curved line and a dot, creating a ?-shaped mark that gives the species its common name."

Imaginal disc One of the parts of a holometabolous insect larva

An imaginal disc is one of the parts of a holometabolous insect larva that will become a portion of the outside of the adult insect during the pupal transformation. Contained within the body of the larva, there are pairs of discs that will form, for instance, the wings or legs or antennae or other structures in the adult. The role of the imaginal disc in insect development was first elucidated by Jan Swammerdam.

Culicinae Subfamily of flies

The Culicinae are the most extensive subfamily of mosquitoes (Culicidae) and have species in every continent except Antarctica, but are highly concentrated in tropical areas. Mosquitoes are best known as parasites to many vertebrate animals and vectors for disease. They are holometabolous insects, and most species lay their eggs in stagnant water, to benefit their aquatic larval stage.

<i>Cynomya mortuorum</i> Species of fly

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Wharf borer Species of beetle

The wharf borer, Nacerdes melanura, belongs to the insect order Coleoptera, the beetles. They belong to the family Oedemeridae, which are commonly known as false blister beetles. Wharf borers are present in all the states of the USA except for Florida. It takes about a year to develop from an egg to an adult. The insect is called the 'wharf borer' because the larval stage of this insect is often found on pilings and timbers of wharves, especially along coastal areas. The adult beetles can be identified via a black band across the end of both elytra, or wing covers. In addition, wharf borers can be distinguished from other members of the family Oedemeridae via the presence of a single spur on the tibia of the forelegs, and the distance between both eyes. Eggs are oviposited on rotten wood where larvae hatch and burrow to feed on rotten wood. Adults do not feed and depend on stored energy reserves accumulated during the larval stage. They are considered to be a pest because they damage wood used in building infrastructures.

Juvenile-hormone esterase

In enzymology, juvenile hormone esterase (JH esterase) is an enzyme that catalyzes the hydrolysis of juvenile hormone. For example, the juvenile hormone II (found in Lepidoptera):

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<i>Jalmenus evagoras</i> Species of butterfly

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<i>Chloridea virescens</i> Species of moth

Chloridea virescens, commonly known as the tobacco budworm, is a moth of the family Noctuidae found throughout the eastern and southwestern United States along with parts of Central America and South America.

<i>Protophormia terraenovae</i> Species of fly

Protophormia terraenovae is commonly called northern blowfly, blue-bottle fly or blue-assed fly. It is distinguished by its deep blue coloration and large size and is an important species throughout the northern hemisphere. This fly is notable for its economic effect as a myiasis pest of livestock and its antibiotic benefits in maggot therapy. Also of interest is P. terraenovae’s importance in forensic investigations: because of their temperature-dependent development and their prominent presence on corpses, the larvae of this species are useful in minimum post-mortem interval (mPMI) determination.

<i>Arsenura armida</i> Species of moth

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Sarcophaga crassipalpis is a species of flesh flies (insects in the family Sarcophagidae.

Madrone butterfly Species of butterfly

Eucheira socialis, commonly known as the Madrone butterfly is a lepidopteran that belongs to the family Pieridae. It was first described by Westwood in 1834. Locally known as Mariposa del madroño or tzauhquiocuilin, it is endemic to the highlands of Mexico, and exclusively relies on the Madrone as a host-plant. The species is of considerable interest to lepidopterists due to gregarious nest-building in the larval stages, and heavily male biased sex ratio. It takes an entire year for this adult butterfly to develop from an egg. The eggs are laid in the month of June and the adults emerge the following May–June. The adults have a black and white pattern on their wings, and the males are generally much smaller and paler than the females. The larvae do not undergo diapause and continue to feed and grow communally in the coldest months of the year. There are two subspecies of E. socialis, named E. socialis socialis and E. socialis westwoodi.


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