Holometabola

Fossil wing of stem-hymenopteran Avioxyela gallica, from Nel et al. (2013). Scale bar = 1 mm.

Belongs within: Pterygota.
Contains: Neuropterida, Coleopterida, Panorpoidea, Eusymphyta, Unicalcarida.

The Holometabola are the major clade of insects, accounting for nearly 85% of all insect species, characterised by the evolution of a complete metamorphosis with distinct larval, pupal and adult stages. The larval stage is more or less soft-bodied and lacks external wing buds, with the larval cuticle being more or less entirely replaced during the quiescent pupal stage by adult cuticle derived specialised pockets of epidermal cells called imaginal discs or anlage (Grimaldi & Engel 2005).

Beetles, lacewings and related taxa form a clade Neuropteriformia within the holometabolans, characterised by development of a median gular sclerite on the underside of the head and modification of the gonostyli of the female genital organs into vaginal palps (Ax 1999). The Mecopteriformia, including Hymenoptera, Lepidoptera, Diptera and allies, may be united by the formation of the pupal cocoon from silk secreted by labial glands, and presence of unpaired pretarsal claws in larvae (Ax 1999). Alternatively, some authors have regarded the Hymenoptera as the sister taxon of the remaining holometabolans.

The Hymenoptera include the wasps and their derivative taxa such as bees and ants. Members of the group are primitively characterised by the presence of hamuli, small hooks on the anterior margin of the hind wing that hook onto the fore wing and hold the wings locked together. The fore wings are the principal flight organs with a concordant increase in the mesothoracic musculature. The prothorax is firmly connected to the mesothorax, and the first abdominal segment is integrated into the mesosoma with its sternite much reduced. The order exhibits haplo-diploid sex determination with females emerging from fertilised eggs and males from unfertilised eggs (Ax 1999). Molecular phylogenetic analysis of the order by Peters et al. (2017) divides hymenopterans between the ectophytophagous Eusymphyta and the endophytophagous and parasitic/carnivorous Unicalcarida.

The earliest well-established holometabolans are known from the Late Carboniferous of Europe. These include the stem-hymenopteran Avioxyela gallica, represented by two preserved fore wings from the Moscovian of Pas-de-Calais, France. It shares the presence of only a few large large rectangular cells between the main veins with modern Hymenoptera, with RP+MA divided in two parallel veins only, and MP and CuA simple (Nel et al. 2013).

The really abominable mystery
Published 21 January 2009
Saddleback caterpillar. Photo by Ross Hutchins.

One topic that both of my regular readers may have noticed I don’t cover here that much is the creationist/intelligent design movement and supposed anti-evolution “arguments” (use of quotation marks entirely deliberate). One reason is that I have the good fortune to live in a country where the creationist movement is not currently (tap lignin) a serious issue. But the main reason is that these days, I find the whole thing to be so incredibly dull. Dull, dull, dull. The supposed arguments trotted out at every opportunity are just so hackneyed and unimaginative. The evolution of whales? The divide between man and monkey? Puh-lease! Since when have these trivialities ever been really worthwhile mysteries? I could probably give you four better enigmas before I even had time to pull my socks on. If you’re going to insist on positing a God of the Gaps argument, then at least extend the poor block the consideration of giving him a decent-sized gap to run around in*.

*For some reason, as I wrote that I got the image of the aforementioned “gap” as something like a sort of cosmic rabbit hutch, with a bunch of onlookers exclaiming, “Oh look, a preternatural omnipotent deity! Isn’t he just the cutest?”

So what are some of these great mysteries? Well, the origins of the nucleus, endoplasmic reticulum and Golgi apparatus in eukaryotes would have to be one. The development of the macronucleus and micronucleus in ciliates is probably another. But for my money, the biggest head-scratcher in evolutionary biology would have to be the origin of the holometabolous insect larva.

Nymph of the sandgroper (Cylindrachaeta), a hemimetabolous insect. Sandgropers are a type of burrowing Orthoptera. Photo from here.

Insect development can be characterised as ametabolous, hemimetabolous or holometabolous. Ametabolous development is the simplest. Among modern insects it is only found in a few basal wingless orders such as silverfish and bristletails, though one very early fossil group of winged insects, the Palaeodictyopteroidea (which I must describe in detail some day, because they’re simply fantastic), seems to have had an ametabolous or near-ametabolous development. Ametabolous insects hatch out of the egg as pretty much miniature versions of the adults, and change little as they grow up. The next stage, hemimetabolous development, is found in insects such as dragonflies, grasshoppers and Hemiptera (true bugs). Hemimetabolous insects have distinct nymphal and adult stages, but they don’t have a pupal stage between nymph and adult. Wings, in those species that have them, grow folded up in wing buds and are not extended until the final adult instar. It should be noted that there is not necessarily a clear dividing line between ametabolous and hemimetabolous development—in some hemimetabolous insects, such as grasshoppers, there may be relatively little morphological distinction between nymphs and adults except for some features such as wings. In others, such as some Hemiptera, the distinction between nymph and adult may be quite notable.

Holometabolous development, on the other hand, is an entirely distinct prospect. Holometabolous insects include moths and butterflies, flies, and beetles. In these taxa there is a distinct larval and adult phase. The larvae are soft-bodied and often vermiform (wormlike), and look completely different to the adults. While nymphs of hemimetabolous insects might develop wingbuds, holometabolous larvae possess not even a trace of visible wings. They may lack the appendages of the adult, and they may possess appendages of their own (such as the tendrils of some caterpillars) that are lost by the adult. Between the larval and adult stages is a non-feeding, usually immobile pupal stage, within which the insect undergoes a complete developmental overhaul before emerging as the adult.

Though holometabolous insects comprise the significant majority of modern taxa, they all fall within a single derived clade, the Holometabola, that probably appeared about the beginning of the Permian (Grimaldi & Engel 2005). Phylogenetic bracketing indicates that they were derived from hemimetabolous ancestors, but how? How did such a significant change occur?

Larva of hoverflies (Syrphidae), commonly known as “rat-tailed maggots”. The “tail” is a breathing tube, allowing the maggots to survive in anoxic environments by extending the tube to somewhere where oxygen is available. Photo from here.

One theory that was popular for some time was that the larval and pupal stages of holometabolans correspond to the nymphal stage of other insects. As I’ve already noted, many hemimetabolous insects also show significant differentiation between nymph and adult. There may be selective advantages to such differentiation, as the different stages may utilise different resources and not compete with each other. The holometabolous larva, it was suggested, was simply an exaggeration of this differentiation. However, the details of holometabolan metamorphosis refute this idea. In hemimetabolous nymphs, the cuticle is divided into sclerotised plates as in the adults. Holometabolan larvae in contrast, have a soft cuticle that is not divided into plates, and is ultrastructurally distinct from nymphal cuticle. During the pupal stage, collections of cells within the developing insect called imaginal discs proliferate and spread through the body, giving rise to adult organ systems such as eyes and wings, as well as the distinct adult cuticle divided into plates. Hemimetabolous nymphs have a fully developed nervous system much like that of their adults. In holometabolan larvae, the development of the nervous is halted at a rudimentary stage, and is not carried to completion until pupation. Even organ systems present in some form in the larva, such as the legs, may be partially or completely replaced by the products of imaginal discs during pupation, with little or nothing remaining of the larval tissue at maturity.

Recently, Truman & Riddiford (1999, 2002) have revitalised an earlier theory that holometabolan larvae actually correspond to the pronymph of hemimetabolous insects*. The pronymph is essentially the final stage of embryonic development. Pronymphs have an underdeveloped nervous system like holometabolan larvae, and an soft undivided cuticle with a similar ultrastructure to that of a larva. In some hemimetabolous insects, the pronymph molts through to the first nymphal instar prior to hatching from the egg. In others, the insect hatches while still in the pronymph stage. The pronymph does not feed in these taxa, but lives off its yolk reserves before moulting to a nymph within a few hours or few days. It may be motile—dragonflies, for instance, are able to move from land to water as pronymphs. Pronymphs and holometabolan larvae also show high levels of JH, juvenile hormone. The role of JH in insects seems to be to retard development, so if an insect moults in the presence of high levels of JH the resulting instar will be much like the previous (Erezyilmaz 2006). In hemimetabolous insects, levels of JH decline before the pronymph moults, allowing development of the nymph, but in holometabolous insects JH levels remain high until the final larval instar.

*The larva-as-pronymph theory is generally attributed to Berlese in 1913, but the idea that the larva was a sort of free-living embryo (a “crawling egg”) was suggested by William Harvey in 1651, and its origins go all the way back to the writings of Aristotle in 322 BC (Erezyilmaz 2006).

The figure above, from Truman & Riddiford (1999), shows suggested stages in the evolution of the holometabolan larva from the pronymph. Stages (a) and (b), as already noted, are both found in living hemimetabolous insects. The major step, which remains undocumented, would have been the evolution of the ability to feed in the pronymph, allowing maintenance of the pronymphal stage through more than one instar – stage (c) in the figure. Lengthening of the pronymphal stage seems to have been matched by a shortening of the nymphal stage, though again, the exact mechanics of this are as yet undocumented. It is possible that once the pronymphal stage became the main feeding and growing stage, then the multiple nymphal instars became fairly redundant, in which case there may have been a selective pressure for their rapid loss.

Eventually, we reach stage (d)—a single nymphal instar. This may be represented in the modern fauna by the Raphidioptera (snakeflies) and Megaloptera (dobsonflies). In these orders, the pupal stage remains mobile with well-developed legs (Grimaldi & Engel, 2005), as shown in the photo above of the pupa of Nigronia fasciatus (Megaloptera) (copyright Atilano Contreras-Ramos). The loss of mobility then leads to the fully-developed pupal stage. In some holometabolan insects, the imaginal discs don’t develop until the end of the larval stage—(e) in the figure above—but in others—stage (f)—they develop early on and then remain quiescent until pupation. Examples are also known where development of adult tissues has been reactivated during the larval stage, such as the larviform reproductives of the beetle Micromalthus, perhaps by the development of localised resistance to the effects of JH.

If we were able to understand how the holometabolan larva evolved, it could have further interesting implications for our understanding of evolution. Morphological change in evolution is generally assumed to happen gradually, but researchers have suggested at least some situations where it could theoretically happen much more rapidly. Such saltatory suggestions have been derided as “hopeful monster” scenarios, and are currently regarded with some skepticism. One of the main issues with the “hopeful monster” is that these deviant individuals would need to reproduce in order to successfully found a new lineage, and it might be difficult to find a willing mate if you look too unusual. However, when the holometabolous larva first evolved, it may have still developed into an adult that looked little different from its hemimetabolous ancestors. What would the implications of this be for the establishment of the new developmental pathway? Could the larval stage have spread through the population unhindered by questions of reproductive liabilities? Is this one situation where the hopeful monster might just have had a little more hope?

Systematics of Holometabola
<==Holometabola [Endopterygota, Halteria, Meronida, Oligoneoptera, Panorpatae, Scarabaeiformes]
    |  i. s.: MormolucoidesP02
    |         Baryshnyala Ilger & Brauckmann 2011 [Baryshnyalidae]IB11
    |           `--*B. occulta Ilger & Brauckmann 2011IB11
    |--Metabolarva Kirejtshuk, Prokin et al. in Nel, Roques et al. 2013NR13
    |    `--*M. bella Kirejtshuk, Prokin et al. in Nel, Roques et al. 2013NR13
    |--NeuropteriformiaA99
    |    |--NeuropteridaGE05
    |    `--ColeopteridaKN13
    `--MecopteriformiaA99
         |--PanorpoideaGE05
         `--+--Avioxyela Nel, Engel et al. in Nel, Roques et al. 2013 [Avioxyelidae]NR13
            |    `--*A. gallica Nel, Engel et al. in Nel, Roques et al. 2013NR13
            `--Hymenoptera (see below for synonymy)GE05
                 |  i. s.: StenopolybiaZ02
                 |         Orisema uchancoiH03
                 |         Ophrynopus schauinslandiG27
                 |         Amalthea Rafinesque 1815BR05
                 |         Giraudia Foerster 1868 non Derbès & Solier in Castagne 1851 (ICBN)BR05
                 |         Dineura virididorsata (Retzius 1783)HP-W05
                 |         MyzinaE12
                 |           |--M. guerinii Lucas 1848E12
                 |           `--M. oraniensis Lucas 1848E12
                 |         Tarpa levaillantii Lucas 1849E12
                 |         Scleroderma ruficornis Lucas 1849E12
                 |         ‘Promachus’ Cresson 1887 nec Loew 1848 nec Stål 1875Z01
                 |         Triassoxyela foveolataPK17
                 |         Gigantoxyela quadrifurcataNR13
                 |         Baeosomus Thomson 1891Z93
                 |         Patasson nitensM94
                 |         CephaleiaF92
                 |           |--C. abietisF92
                 |           `--C. alashanicaF92
                 |         Lygaeonematus laricisF92
                 |         Hoplocampa Hartig 1837M99
                 |           |--H. chrysorrhaea (Klug 1816)M99
                 |           `--H. fulvicornis (Panzer 1801) [incl. H. rutilicornis (Klug 1816)]M99
                 |         Aprosthema Konow 1899M99
                 |           `--A. melanura (Klug 1814) [incl. A. tarda (Klug 1814)]M99
                 |         Heptamelus Haliday 1855M99
                 |           `--H. ochroleucus (Stephens 1835)M99
                 |         Strongylogaster Dahlbom 1835M99
                 |           `--S. multifasciata (Geoffroy 1785) [incl. S. lineata (Christ 1791)]M99
                 |         Dulophanes Konow 1907 [incl. Nesoselandria Rohwer 1910]M99
                 |         Ardis Konow 1886M99
                 |           `--A. pallipes (Serville 1823) [incl. A. brunniventris (Hartig 1837)]M99
                 |         Claremontia Rohwer 1909M99
                 |           |--C. alternipes [=Monophadnoides alternipes]M99
                 |           |--C. confusa [=Monophadnoides confusa]M99
                 |           |--C. tenuicornis [=Monophadnoides tenuicornis]M99
                 |           `--C. waldheimii [=Monophadnoides waldheimii]M99
                 |         Fenusa Leach 1817M99
                 |           `--F. pumila Leach 1817 [incl. F. pusilla (Lepeletier 1823)]M99
                 |         Fenusella Enslin 1912 [incl. Messa Leach 1817 (n. n.)]M99
                 |         Scolioneura Konow 1890M99
                 |           |--S. betuleti (Klug 1916)M99
                 |           `--S. vicina Konow 1894M99
                 |         Empria Lepeletier & Serville 1828M99
                 |           |--E. abdominalisF92
                 |           |--E. candidataF92
                 |           |--E. klugii (Stephens 1835) [incl. E. waldstaetterense Liston 1980]M99
                 |           `--E. pulverataF92
                 |         Harpiphorus Hartig 1837M99
                 |           `--H. lepidus (Klug 1818)M99
                 |         Apethymus Benson 1939M99
                 |           |--A. braccatus (Gmelin 1790)M99
                 |           `--A. serotinus (Müller 1776)M99
                 |         Siobla Cameron 1877M99
                 |           `--S. sturmii (Klug 1817)M99
                 |         Aglaostigma Kirby 1882M99
                 |           |--A. fulvipesF92
                 |           `--A. nebulosum (André 1881)M99
                 |         Elinora Benson 1946 [incl. Cuneala Zirngiebl 1956]M99
                 |           `--E. longipes (Konow 1886) [=Allantus longipes; incl. *Cuneala tricolor Zirngiebl 1956]M99
                 |         Blankia Lacourt 1997M99
                 |           `--*B. koehleri (Klug 1817) [=Allantus koehleri]M99
                 |         Sharliphora Wong 1969M99
                 |           `--S. nigella (Förster 1854) [incl. S. ambigua (Fallén 1808) (preoc.)]M99
                 |         Konowia Brauns 1884M99
                 |           `--K. betulae (Enslin 1911) [incl. K. guntionensis Zombori 1969]M99
                 |         Trachelus Jurine 1807M99
                 |           `--T. troglodytus (Fabricius 1787) [=T. troglodyta]M99
                 |         Iota Saussure 1855S00
                 |         Coeloides dendroctoniS00
                 |         Cephenopsis mirabilis Hong 1985RJ93
                 |         PararchexyelidaeRJ93
                 |         Spategaster blattarumR13
                 |         Poecilosoma pulveratumR13
                 |         Pogonius variegatusR13
                 |         Tachus Jurine 1807KM20
                 |         Christolia Brullé 1846EH19
                 |         Myrapetra scutellarisL89
                 |--EusymphytaPK17
                 `--UnicalcaridaPK17

Hymenoptera [Chalastrogastra, Neohymenoptera, Orthandria, Piezata, Siricina, Siricomorpha, Symphyta, Tenthredines, Tenthredinetae, Urocerata, Vespida, Vespidea]GE05

*Type species of generic name indicated

References

[A99] Ax, P. 1999. Das System der Metazoa II. Ein Lehrbuch der phylogenetischen Systematik. Gustav Fisher Verlag: Stuttgart (transl. 2000. Multicellular Animals: The phylogenetic system of the Metazoa vol. 2. Springer).

[BR05] Bouchet, P., & J.-P. Rocroi. 2005. Classification and nomenclator of gastropod families. Malacologia 47 (1–2): 1–397.

[EH19] Énay, R., & M. K. Howarth. 2019. Part L, revised, volume 3B, chapter 7: Systematic descriptions of the Perisphinctoidea. Treatise Online 120: 1–184.

Erezyilmaz, D. F. 2006. Imperfect eggs and oviform nymphs: a history of ideas about the origins of insect metamorphosis. Integrative and Comparative Biology 46 (6): 795–807.

[E12] Evenhuis, N. L. 2012. Publication and dating of the Exploration Scientifique de l’Algérie: Histoire Naturelle des Animaux Articulés (1846–1849) by Pierre Hippolyte Lucas. Zootaxa 3448: 1–61.

[F92] Fan Z. 1992. Key to the Common Flies of China 2nd ed. Science Press: Beijing.

[G27] Gourlay, E. S. 1927. Notes on the New Zealand wood-wasp Ophrynopus schauinslandi Ashmead. Transactions and Proceedings of the New Zealand Institute 57: 691–693.

[GE05] Grimaldi, D., & M. S. Engel. 2005. Evolution of the Insects. Cambridge University Press: New York.

[H03] Heads, M. 2003. Ericaceae in Malesia: vicariance biogeography, terrane tectonics and ecology. Telopea 10 (1): 311–449.

[HP-W05] Heitland, W., & H. Pschorn-Walcher. 2005. Biology and parasitoids of the peculiar alder sawfly, Platycampus luridiventris (Fallen) (Insecta, Hymenoptera, Tenthredinidae). Senckenbergiana Biologica 85 (2): 215–231.

[IB11] Ilger, J.-M., & C. Brauckmann. 2011. The smallest Neoptera (Baryshnyalidae fam. n.) from Hagen-Vorhalle (early Late Cretaceous: Namurian B; Germany). ZooKeys 130: 91–102.

[KN13] Kirejtshuk, A. G., & A. Nel. 2013. Skleroptera, a new order of holometabolous insects (Insecta) from the Carboniferous. Zoosystematica Rossica 22 (2): 247–257.

[KM20] Kury, A. B., A. C. Mendes, L. Cardoso, M. S. Kury & A. A. Granado. 2020. WCO-Lite: Online world catalogue of harvestmen (Arachnida, Opiliones). Version 1.0—Checklist of all valid nomina in Opiliones with authors and dates of publication up to 2018. Published by the author: Rio de Janeiro.

[L89] Lucas, H. 1889. Note suivante relative à des hyménoptères sociaux de la division des méliponides. Annales de la Société Entomologique de France, 6e série 9: cvii–cviii.

[M99] Magis, N. 1999. Répertoire des mouches à scie reconnues en Belgique et au Grand-Duché de Luxembourg (Hymenoptera: Symphyta). Additions et corrections. Notes Fauniques de Gembloux 36: 85–93.

[M94] May, B. M. 1994. An introduction to the immature stages of Australian Curculionoidea. In: Zimmerman, E. C. Australian Weevils (Coleoptera: Curculionoidea) vol. 2. Brentidae, Eurhynchidae, Apionidae and a chapter on immature stages by Brenda May pp. 365–728. CSIRO Australia.

[NR13] Nel, A., P. Roques, P. Nel, A. A. Prokin, T. Bourgoin, J. Prokop, J. Szwedo, D. Azar, L. Desutter-Grandcolas, T. Wappler, R. Garrouste, D. Coty, D. Huang, M. S. Engel & A. G. Kirejtshuk. 2013. The earliest known holometabolous insects. Nature 503: 257–261.

[PK17] Peters, R. S., L. Krogmann, C. Mayer, A. Donath, S. Gunkel, K. Meusemann, A. Kozlov, L. Podsiadlowski, M. Petersen, R. Lanfear, P. A. Diez, J. Heraty, K. M. Kjer, S. Klopfstein, R. Meier, C. Polidori, T. Schmitt, S. Liu, X. Zhou, T. Wappler, J. Rust, B. Misof & O. Niehuis. 2017. Evolutionary history of the Hymenoptera. Current Biology 27 (7): 1013–1018.

[P02] Ponomarenko, A. G. 2002. Superorder Myrmeleontidea Latreille, 1802 (=Neuropteroidea Handlirsch, 1903). In: Rasnitsyn, A. P., & D. L. J. Quicke (eds) History of Insects pp. 176–189. Kluwer Academic Publishers: Dordrecht.

[R13] Reuter, O. M. 1913. Lebensgewohnheiten und Instinkte der Insekten bis zum Erwachen der sozialen Instinkte. R. Friedländer & Sohn: Berlin.

[RJ93] Ross, A. J., & E. A. Jarzembowski. 1993. Arthropoda (Hexapoda; Insecta). In: Benton, M. J. (ed.) The Fossil Record 2 pp. 363–426. Chapman & Hall: London.

[S00] Siddiqi, M. R. 2000. Tylenchida: Parasites of plants and insects 2nd ed. CABI Publishing: Wallingford (UK).

Truman, J. W., & L. M. Riddiford. 1999. The origins of insect metamorphosis. Nature 401: 447–452.

Truman, J. W., & L. M. Riddiford. 2002. Endocrine insights into the evolution of metamorphosis in insects. Annual Review in Entomology 47: 467–500.

[Z02] Zherikhin, V. V. 2002. Insect trace fossils. In: Rasnitsyn, A. P., & D. L. J. Quicke (eds) History of Insects pp. 303–324. Kluwer Academic Publishers: Dordrecht.

[Z93] Zimmerman, E. C. 1993. Australian Weevils (Coleoptera: Curculionoidea) vol. 3. Nanophyidae, Rhynchophoridae, Erirhinidae, Curculionidae: Amycterinae, literature consulted. CSIRO Australia.

[Z01] Zompro, O. 2001. A review of Eurycanthinae: Eurycanthini, with a key to genera, notes on the subfamily and designation of type species. Phasmid Studies 10 (1): 19–23.

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