Eating Mum from the Inside Out

Micromalthus debilis feeding on rotting wood. The large specimen on the left may or may not be a mature female. Photo courtesy of Alex Wild.

Life doesn't always go with the easiest way to do things. Sometimes things get complicated. But sometimes things get so complicated, so seemingly unnecessarily confusing and baroque, that one can't help wondering that someone, somewhere, is taking the piss.

Micromalthus debilis is a tiny, wood-boring beetle that has the dubious claim of going through what is perhaps the most complicated life-cycle in the animal kingdom. You have to look at obscure parasites such as Buddenbrockia and Mesozoa before you find possible competitors. Only one species of Micromalthus is currently recognised. This species is found more or less pan-tropically and pan-subtropically in rotten wood, but its range may have been increased by human transport (Pollock & Normark, 2002). Within the beetles, Micromalthus debilis holds a decidedly isolated phylogenetic position - it belongs to the small relictual group known as Archostemata which comprises the sister group to all other beetles, and while fossils of the Micromalthus lineage are only known from amber (dating back to the Cretaceous), the possible sister-group of Micromalthus, the Cupedidae, has a fossil record dating back to the Triassic (Beutel & Hörnschemeyer, 2002; Grimaldi & Engel, 2005).

Most Micromalthus don't even look like beetles. Micromalthus are usually female and become mature while still effectively larvae (Pollock & Normark, 2002). Such females produce eggs asexually by parthenogenesis. Such egg production is usually thelytokous - asexual eggs produced by diploid females hatch into diploid females. Like some other insect lineages (including, most famously, Hymenoptera), Micromalthus has haplodiploid sex determination - females are diploid while males are haploid. Production of males in Micromalthus is rare (more on that in a moment). Like Strepsiptera, Micromalthus is hypermetamorphic (it goes through multiple larval stages). When thelytokous Micromalthus eggs first hatch, out come highly mobile, legged larvae called triungulins. The triungulins feed for a few weeks, then moult to become legless cerambycoid larvae which live a few months more. Remarkably, the ovaries begin to develop in the cerambycoid larva, which then moults directly into the mature paedogenetic adult without going through a pupal stage, making the adult a true reproductive larva. In most holometabolous insects such as beetles, flies and wasps, the reproductive organs don't begin to develop until the pupal stage.

As if the production of parthenogenetic, reproductive larvae was not remarkable itself, that's not actually where the process becomes complicated. Some females at the end of the cerambycoid stage, instead of moulting straight through to adults, actually do go into a pupal stage. When those pupae reach maturity, instead of becoming larviform like their sisters, they produce a fully-developed, winged adult beetle. These winged females are presumably able to disperse to new feeding grounds, though what determines whether a larva becomes a paedogenetic or winged adult seems to be unknown.


One of the rare fully developed adults of Micromalthus debilis. Photo again courtesy of Alex Wild.

An few female larvae differ further from their sisters in that they don't start developing ovaries while still larva, but not until they reach the final instar. These females, instead of producing numerous thelytokous eggs, produce just one arrhenotokous egg - a parthenogenetically produced egg that will develop into a haploid male. When she lays this single egg, it remains attached to her until it hatches into yet another larval type, a legless curculionoid larva. The instant the male larva is hatched, it plunges its head back into its mother, and proceeds to devour the contents of her body. Once it has finished consuming its hapless mother, the cannibalistic offspring will go through a series of moults culminating in a winged adult male. Some arrhenotokous females, if the male egg fails to develop properly or is lost before it hatches, may switch to producing thelytokous eggs that hatch into other females.

Ironically, in light of the terminal cost to the female of producing a male offspring, no matings between males and females and sexually-produced eggs have been observed in Micromalthus, and some authors have suggested that the males produced in this way are all sterile. Reproduction in Micromalthus would then be entirely parthenogenetic. This seems very unlikely - as females that produce males only ever produce a single offspring, surely there would be a strong selective pressure for eliminating production of males entirely if they were completely non-functional. Arrhenotokous females make no attempt to elude the attentions of their hungry sons, but submit readily to their fates. Male production is also more likely when resources become stretched. It seems much more likely that sexual reproduction does occur, probably between the males and the rare winged females, though the two are generally not produced by a colony at the same time and inbreeding between males and females of the same colony would be unlikely.


The full life cycle of Micromalthus debilis, taken from Pollock & Normark (2002).

Why does Micromalthus have such an obscenely complicated and sordid life cycle? Like other wood-living insects, Micromalthus rely on endosymbiotic bacteria to digest the wood they feed, and these endosymbionts may be transmitted to offspring through the ovarian tissue. For bacteria transmitted in such a way, males represent a reproductive dead end, and many such bacteria in insects have been shown to negatively affect male production in order to increase the ratio of female offspring and improve their own chances of transmission (Hurst & Jiggins, 2000; the most famous examples are species of Wolbachia). Pollock & Normark (2002) suggest that endosymbiotic bacteria may be transmitted to female offspring but not to males, and that male cannibalism may be a means of circumventing this handicap. The high cost of producing males would have resulted in selective pressure to keep the number produced to a bare minimum, explaining their rarity. Unfortunately, while this is an intriguing idea, it currently suffers from a dire shortage of evidence. The Micromalthus will not give up their secrets easily.

REFERENCES

Beutel, R. G., & T. Hörnschemeyer. 2002. Larval morphology and phylogenetic position of Micromalthus debilis LeConte (Coleoptera: Micromalthidae). Systematic Entomology 27 (2): 169-190.

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

Hurst, G. D. D., & F. M. Jiggins. 2000. Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerging Infectious Diseases 6 (4): 329-336.

Pollock, D. A., & B. B. Normark. 2002. The life cycle of Micromalthus debilis LeConte (1878) (Coleoptera: Archostemata: Micromalthidae): historical review and evolutionary perspective. Journal of Zoological Systematics and Evolutionary Research 40 (2): 105-112.