Chordodes formosanus

For most insects (and other small animals), the praying mantis is a creature out of their worst nightmare; a deadly predator with giant compound eyes, a nasty set of high-speed spiky grasping limbs, and an appetite to boot. But Chordodes formosanus is a parasite that would give mantis nightmares - it is a hairworm - and regular readers of this blog will know immediately why that is justified.

From Fig. 2 of this paper

The worm starts out as a microscopic larva hidden inside the body of small insects - the mantis' usual prey - but once it is ingested by a mantis, it can then grow to several centimetres long inside its abdomen. By the time it is ready to bid farewell to its reluctant host, which comes when it reaches sexual maturity, the worm has already taken up most of the space within the mantis, leaving it a half-empty husk. The modus operandi of a horsehair worm is to then get into the water, which involves the host taking a dunk - whether it wants to or not. Apart from commandeering the mantis to go for a terminal end to their relationship, during the worm's development, it takes a massive toll. After all, one does not simply host a giant worm inside one's abdomen without any consequences.

But the said consequences is not equally distributed within the mantis population - this hairworm seems to affect male mantis more severely - especially in regards to their reproductive capacity. In a nutshell - C. formosanus shrink their testes and in some cases, they disappear altogether. However, this parasite seems more forgiving when it comes to female mantis; infected female mantis can harbour the worm and still retain intact reproductive organs. Not to say it doesn't exact a toll, just that the female mantis can still have some babies before her end comes. So why this sex bias? The reason lies in how this parasite alters the host's physiology.

When researchers looked at various aspects of the infected mantis' physical appearance, they also noticed some external changes in both sexes - they had comparatively shorter walking legs, smaller wings, and altered antennae - but it was more pronounced in the infected male mantis. Overall, the infected individuals have an appearance which bears closer resemblance to that of late-stage juvenile rather than adults. This suggest that C. formosanus might be tempering with the mantis' so-called "juvenile hormones" which control development in insects. But why is it that only the male mantis lose their reproductive organs? At this point, it is not entirely clear, but it might have something to do with the different role played said hormones in the development of each sex.

So why has C. formosanus evolved to castrate their male mantis host? From the parasite's perspective, host castration is a very effective strategy - the host does not need its gonad to survive, only to reproduce. So by tapping into this energy source, the parasite can keep the host alive while maximising the amount of resources it draws from the host.

For that, the host pays a double cost in terms of evolutionary fitness. Usually with such parasite infection which inevitably results in the host's death, the best thing for the host to do to make the best of a bad situation and reproduce as much as possible before they are eventually killed by the parasite. But in this case, the male mantis doesn't even get to do that - thanks to C. formosanus, long before it bid farewell to life, it has to bid farewell to its junk as well

Reference:
Chiu, M. C., Huang, C. G., Wu, W. J., & Shiao, S. F. (2015). Morphological allometry and intersexuality in horsehair-worm-infected mantids, Hierodula formosana (Mantodea: Mantidae). Parasitology 142: 1130-1142