Written by Joe Ballenger

If someone begins a statement with ‘this might be a dumb question, but…’ my ears usually perk up, because it’s very likely that something interesting is about to follow.

@Stylopidae whoa! this is a dumb question, but can caterpillars ever NOT go through metamorphosis?

— Sarah Emerson (@SarahNEmerson) August 19, 2016

This is a great question, because she’s asking about lifestyles which aren’t really commonly known outside the entomology community.

Male Acanthopsyche moth. A female is pictured below the fold. Image credit: Janet Graham, via Flickr. License info: CC-BY-2.0

In the laboratory, we can suppress the process of metamorphosis by treating insects with growth regulators. Many of these growth regulators are also used as pesticides, specifically for mosquitoes.

Although it pays for humans to be able to control this process, there are some benefits to abandoning metamorphosis altogether. In fact there are many moths, beetles, flies, and an obscure group of parasitic insects called Strepsipterans, which have abandoned this process. Some of these insects just look like larvae as adults, but others have completely done away with the process altogether.

So what do these lifestyles look like, why do they develop this way, and how does this system work?

Abandoning Metamorphosis

Extreme reduction of body parts in the female Acanthopsyche bagworm moth. Note the lack of a hardened cuticle, legs, and wings. Eggs are visible through the body wall. Image credit: Janet Graham via Flickr. License info: CC-BY-2.0

I guess the first question which should be answered is this: why have some insects abandoned metamorphosis?

Wings are important for most insects. They allow the insects to move around, find new habitats, and find mates. In terms of biological innovations, it’s a rather important one and it seems counter-intuitive that some insects would opt out of such an important process.

To get a good feel for this answer, it pays to understand what metamorphosis is. Nancy wrote an excellent post on this awhile back, where you can learn about the process in great detail. From the perspective of the insect, metamorphosis is a very risky process because the pupa is unable to move and is relatively helpless against predators and parasitoids. The structures this process creates are very energetically expensive, and the pupa is unable to feed to acquire new energy reserves at the time.

Adult female atlas moth, showing the huge wing-to-body ratio. Image credit: Alias 0591, via Flikr. License info: CC-BY-2.0

Ultimately, the answer to the question is one of economy. Most insects which have abandoned the process have made a trade-off between adult dispersal and reproductive capacity. It might be a little harder for the larvae to disperse, but not having to make stuff like wings and legs allows you to put that energy into making babies. In many cases, those babies can take care of dispersal all on their own.

Consequently, it’s always the females which have made this trade-off. It’s extremely rare for males to look like larvae, and no known species of insect has males which reproduce as larvae.

Neoteny: Adults which look like larvae

Adult female Dahlica bagworm moth, showing remains of pupal casing. Image credit: Carl D. Barrentine, used with permission from BugGuide.net.

Neoteny is a lifestyle where the adults resemble larvae. It’s not abandoning metamorphosis per se, but neotenic females look like insect larvae. They still go through the process of metamorphosis, but the final adult has features which make it resemble a larval insect.

This is a typical trade-off between developing wings and having higher reproductive output. Some species which have this lifecycle have to deal with an environment where they have abundant food sources that will quickly go away. Others may live in the opposite extreme, an extremely stable environment where dispersal is not really needed.

Bagworm moths are a good example of neotenic insects. They live on trees, and are notorious for defoliating them very quickly. Females look a lot like caterpillars, but the males look like what you’d expect a moth to look like. Their larvae can disperse by ballooning, or they can lay eggs which are dispersed by birds.

Paedogenesis: Larvae which never grow up

Lifecycle of M. speyeri. The switch between metamorphosis (left) and paedogenesis (right) seems to be environmental, specifically triggered by bad food. Image credit: Hodin & Rididiford, 2000

There are cases where insects have completely abandoned complete metamorphosis, and where the adult females do not go through complete metamorphosis. In this lifestyle, it’s the larvae themselves which reproduce. This is called paedogenesis.

In cases where males are present, they go through complete metamorphosis. In some cases, the females only produce females. In other cases, both females and males are produced. Alternating between paedogenesis and complete metamorphosis is common.

As a larva, the fungus feeding gall midge Mycophila feeds on fungi, and favors the younger growth. When it’s ready to reproduce, it’s eggs hatch inside the mother’s body and the larvae live as parasites within the mom. After the larvae have consumed the mother, they eat their way out and complete their lifecycle by feeding on fungal strands.

However, when the young fungus is all used up, the midge switches to a lifecycle more typical of flies. The larvae pupate, and both males and females can be produced from these adults. These midges go off to find a new patch of fungus, and lay their eggs in the new growth.

Why do these insects never grow up?

With these insects, there’s some rather interesting genetic things going on. The females retain larval features in the case of neoteny, but males develop in a more typical manner. In the case of paedogenesis, their reproductive organs become active much earlier than they normally would.

So what gives?

The best model to study this stuff is a parasitic insect called Xenos vesparum, a Strepsipteran. These are extremely odd insects which have males that go through metamorphosis and females which don’t. Females are paedogenic, whereas males are not.

Lifecycle of the Strepsipteran Xenos vesparum. Note that males have pupae, but females are essentially identical to their larvae. Image credit: Erezyilmaz et. al 2014

In this insect, paedogenesis seems to be related to sex-specific transcription of a protein called broad. This protein is a part of the Juvenile Hormone pathway, which tells the insect when it’s time to turn into an adult. When it’s time to pupate, Juvenile Hormone goes away and broad is produced…and this protein tells the insect to get it’s adult features.

In Strepsipterans, the protein broad is expressed in a sex-specific manner. The core of the protein is expressed in males just before they pupate, but it’s not expressed in the females which do not pupate. So males get the signal to turn into adults, and females don’t.

In addition to the lack of adult features, there also needs to be the presence of adult reproductive organs in reproducing larvae. In adult insects, the activation of the reproductive organs is regulated by the receptor for the molting hormone ecdysone. In the midge Mycophila, low quality food causes these receptors to be produced in the reproductive organs earlier than normal.

Exactly how these changes happen isn’t clear. All we know is that paedogenesis seems to be the result of a combination of things that suppress some adult features, while causing other adult features to appear much earlier than they do in other insects.

The Bottom Line

There are insects which have abandoned metamorphosis, and it’s an extremely rare lifestyle. The benefits to abandoning this lifestyle revolve around being able to trade metabolically expensive features like wings and legs for increased reproductive output. Additionally, many insects which have neotenic or paedogenic lifecycles need to take advantage of quickly depleting resources.

The lifecycle isn’t very well understood, either. The most famous case, the Micromalthus , beetle, apparently produces vestigial adults. They’re capable of mating, but don’t appear to be capable of reproducing. Their roles in the biology of this insect aren’t very well understood, and speculation about their function is highly controversial. There are also some insects for which paedogenesis has been reported, but never confirmed.

These insects hold the answers to some rather interesting genetic questions about how insects develop, and given that a lot of insects aren’t doing too well at the moment…we may be depriving ourselves of these answers by not protecting some of the ecologically fragile places where they live.

Works Cited:

1. Bray, T. C., & Bocak, L. (2016). Slowly dispersing neotenic beetles can speciate on a penny coin and generate space-limited diversity in the tropical mountains. Scientific Reports, 6.
2. Erezyilmaz, D. F., Hayward, A., Huang, Y., Paps, J., Acs, Z., Delgado, J. A., … & Kathirithamby, J. (2014). Expression of the pupal determinant broad during metamorphic and neotenic development of the strepsipteran Xenos vesparum Rossi. PloS one, 9(4), e93614.
3. Hodin, J., & Riddiford, L. M. (2000). Parallel alterations in the timing of ovarian ecdysone receptor and ultraspiracle expression characterize the independent evolution of larval reproduction in two species of gall midges (Diptera: Cecidomyiidae). Development genes and evolution, 210(7), 358-372.
4. Jindra, M., Palli, S. R., & Riddiford, L. M. (2013). The juvenile hormone signaling pathway in insect development. Annual review of entomology, 58, 181-204.
5. Konopova, B., & Jindra, M. (2008). Broad-Complex acts downstream of Met in juvenile hormone signaling to coordinate primitive holometabolan metamorphosis. Development, 135(3), 559-568.
6. MCMAHON, D. P., & HAYWARD, A. (2016). Why grow up? A perspective on insect strategies to avoid metamorphosis. Ecological Entomology.
7. Perotti, M. A., Young, D. K., & Braig, H. R. (2016). The ghost sex-life of the paedogenetic beetle Micromalthus debilis. Scientific reports, 6, 27364.
8. Pollock, D. A., & Normark, B. B. (2002). The life cycle of Micromalthus debilisLeConte (1878)(Coleoptera: Archostemata: Micromalthidae): historical review and evolutionary perspective. Journal of Zoological Systematics and Evolutionary Research, 40(2), 105-112.

Acknowledgements:

A special thanks to Anthony Caravaggi and an anonymous Friend of the Blog for helping us to get research for this post.

In addition, I would like to thank Carl Barrentine for donating his photograph of the Dahlica bagworm moth alongside its pupal casing. More of Carl’s pictures can be found at the Dakota Naturalist blog.