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 Holometabola. 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.
There are four general developmental stages, each with its own morphology and function.
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.
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. [1] It is not uncommon that larval tissue that is broken down during metamorphosis increase in size by cell enlargement, while cells and tissues that will turn into imago grows by an increase in numbers. [2]
Some insects, including species of Coleoptera, Diptera and Hymenoptera, have a prepupa stage after the larva stage and before the pupa stage. This is similar in shape to the larva and can still move around, but it does not feed. [1]
The flies of superfamily Hippoboscoidea are unusual in that a larva develops inside its mother and is born in the prepupa stage, whereupon it immediately progresses to the pupa stage. [3] If looking at only the time spent outside the mother, then the first stage of the life cycle in Hippoboscoidea would be the prepupa.
To enter the third stage of holometabolous 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. [4]
Around 45% to 60% of all known living species are holometabolan insects. [5] 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, [6] [7] 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). [8] [9] Phylogenetic studies also show that the sister group of Holometabola is Paraneoptera, which includes hemimetabolan species and a number of neometabolan groups. [10] The most parsimonious evolutionary hypothesis is that holometabolans originated from hemimetabolan ancestors.
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. [10]
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 [11] ). 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 [12] ) 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. [13] 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. [14] 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. [15]
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 Kr-h1 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. [16] 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. [17] This paper was met with severe criticism, and spurred a heated debate in the literature.
The holometabolous insect orders are:
Metamorphosis is a biological process by which an animal physically develops including birth transformation or hatching, involving a conspicuous and relatively abrupt change in the animal's body structure through cell growth and differentiation. Some insects, jellyfish, 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").
A larva is a distinct juvenile form many animals undergo before metamorphosis into their next life stage. Animals with indirect development such as insects, amphibians, or cnidarians typically have a larval phase of their life cycle.
In biology, a nymph is the juvenile form of some invertebrates, particularly insects, which undergoes gradual metamorphosis (hemimetabolism) before reaching its adult stage. Unlike a typical larva, a nymph's overall form already resembles that of the adult, except for a lack of wings and the emergence of genitalia. In addition, while a nymph moults, it never enters a pupal stage. Instead, the final moult results in an adult insect. Nymphs undergo multiple stages of development called instars.
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.
An instar is a developmental stage of arthropods, such as insects, which occurs 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 shedding their exoskeleton (moulting), 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.
The huhu beetle is a longhorn beetle endemic to New Zealand. It is the heaviest beetle found in New Zealand.
Arachnocampa is a genus of nine fungus gnat species which have a bioluminescent larval stage, akin to the larval stage of glowworm beetles. The species of Arachnocampa are endemic to Australia and New Zealand, dwelling in caves and grottos, or sheltered places in forests.
Arachnocampa luminosa, commonly known as New Zealand glowworm or simply glowworm, is a species of fungus gnat endemic to New Zealand. The larval stage and the imago produce a blue-green bioluminescence. The species is known to dwell in caves and on sheltered banks in native bush where humidity is high. Its Māori name is titiwai, meaning "projected over water".
Polygonia interrogationis, commonly called the question mark butterfly, 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."
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.
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.
Papilio demodocus, the citrus swallowtail or Christmas butterfly, is a swallowtail butterfly which commonly occurs over the entirety of sub-Saharan Africa, including Madagascar, besides the southern Arabian Peninsula. The caterpillars feed on various native plants of especially the family Rutaceae, but have also taken to the leaves of cultivated citrus trees.
Cynomya mortuorum belongs to the order Diptera, sometimes referred to as "true flies". In English, the only common name occasionally used is "fly of the dead". It has a bluish-green appearance, similar to other Calliphoridae and is found in multiple geographic locations with a preference for colder regions. Belonging to the family Calliphoridae, it has been shown to have forensically relevant implications due to its appearance on carrion. Current research is being done to determine C. mortuorum's level of importance and usage within forensic entomology.
The Sulawesi moon moth or Isis moon moth is a moth of the family Saturniidae first described by Léon Sonthonnax in 1899.
The wharf borer, Nacerdes melanura, belongs to the insect order Coleoptera, the beetles. They belong to the family Oedemeridae, 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 name 'wharf borer' comes from the larval stage of this insect, which often lingers on pilings and timbers of wharves, especially along coastal areas. The adult beetles are identifiable via a black band across the end of both elytra. In addition, wharf borers are distinct from other members of the family Oedemeridae due to the presence of a single spur on the tibia of the forelegs and the distance between both eyes. The female beetle oviposits eggs on rotten wood, on which the larvae hatch, burrow, then feed. Adults do not eat and depend on stored energy reserves accumulated as a larva. They are considered a pest because they damage wood used in building infrastructures.
Jalmenus evagoras, the imperial hairstreak, imperial blue, or common imperial blue, is a small, metallic blue butterfly of the family Lycaenidae. It is commonly found in eastern coastal regions of Australia. This species is notable for its unique mutualism with ants of the genus Iridomyrmex. The ants provide protection for juveniles and cues for adult mating behavior. They are compensated with food secreted from J. evagoras larvae. The ants greatly enhance the survival and reproductive success of the butterflies. J. evagoras lives and feeds on Acacia plants, so butterfly populations are localized to areas with preferred species of both host plants and ants.
Arsenura armida, the giant silk moth, is a moth of the family Saturniidae. It is found mainly in South and Central America, from Mexico to Bolivia, and Ecuador to south-eastern Brazil. It was first described by Pieter Cramer in 1779.
Sarcophaga crassipalpis is a species of flesh flies (insects in the family Sarcophagidae.
Eucheira socialis, commonly known as the Madrone butterfly is a lepidopteran that belongs to the family Pieridae. It was first described by John O. 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.
The prepupa is a stage in the life cycle of certain insects, following the larva or nymph and preceding the pupa. It occurs in both holometabolous and hemimetabolous insects.