Twisted wings, twisted sex

Some time ago, I wrote a post on here. It was reasonably popular, but I deleted it for foolish reasons. However, I no longer care about those reasons, so now I’ve edited it slightly and it’s back! Enjoy? ENJOY!

If you’re the type of person who frequents animal behaviour blogs, you probably love yourself some animal sex posts (I sometimes feel like I should put some sort of “it’s science so it’s not weird OKAY” disclaimer or something here, but you should be used to it by now… and also I get so many hits from people googling ‘dolphin rape’ that I don’t think it would really make any difference). Such a predilection for tales of animal mating systems will mean you’re most likely well acquainted with the ornaments, weapons and displays that males (for the most part) of a huge variety of shapes, sizes, and species use to improve their chances of mating. Perhaps you’ve tired of pictures of peacock trains and scarab beetle horns; those videos of jumping spiders shaking their curiously colourful buttflaps (erm, you should get used to this level of technical terminology) or bowerbirds prancing around their ornately decorated nests just don’t cut it for you these days.

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(I’m really sorry to the people who took the original photographs that I have ruined there)

Even Stephen Stearns doing his sage grouse impression isn’t enough.

Give us more, you cry: we need more sexual dimorphism! More weird behaviours! Different body shapes! Life histories! Displays, weapons, ornaments, EVERYTHING!

Well, I was flicking through my copy of Thornhill and Alcock’s seminal (hurr hurr) work, ‘The Evolution of Insect Mating Systems’, and happened upon a short passage describing the Strepsipteran order of insects. ‘Strepsiptera’ translates as ‘twisted wing’, but the curious wing shape that gives these insects their name is not the main reason that they piqued my interest. No, it’s because the sub-order Stylopidia has some extreme sexual dimorphism going on: only the males actually grow wings, legs, antennae, mouthparts, eyes, or any of the traits that we associate with adult insects; the females, meanwhile, have none of these features. Male flight is required because they need to find a female to mate with, and quick, because these guys only live for a few hours after emerging as adults.

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Male (left) and female (right) Xenos vesparum.

So while males are flying around in a desperate sexual frenzy, what are their rather curious female counterparts doing? And where are the females, if they have no means of locomotion? The Strepsiptera are ‘obligate parasites’, meaning that some part of their life cycle must take place within a host animal. Hosts include a whole variety of different insects, including silverfish, crickets, stink bugs, wasps, bees, flies… In one particular family, the Myrmecolacidae, males parasitise ants while females parasitise Orthopteran insects. Female Strepsipterans never leave their hosts, instead sitting pretty – at least, about as pretty as a wingless, eyeless, mouthless parasite can get – and waiting for a male to come along. To move things along, virgin females help out by releasing a pheromone that males can use to home in on a potential mate before suffering an early death.

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Females poking out from betwixt the thoracic segments of a Polistes wasp.

Well, you may say, that is some fairly intense sexual dimorphism. But is that all? Males have wings and fly about? It’s not really setting the world on fire. I mean, there are those huge beetles which climb giant trees and throw each other off branches in order to reach the demure, hornless female at the top – it’s not even as good as that, is it?

Oh, ok. I get it. People are immune to weird sexual dimorphisms in insects these days. Fur and feathers, that’s what you want. Maybe if it were a lion with wings flying around briefly in search of a weird giant worm thing to hump, then you’d be impressed? Also, the giant no-face lion-worm would probably live in a giraffe’s bum. Then you’d care. Then you’d ALL care. You want to know something else about the Stylopidae? Well, there’s some controversy over how they mate, but one of the main hypotheses is that mating occurs via TRAUMATIC INSEMINATION.

…also known as HYPODERMIC INSEMINATION.

Why is it called that? Well, males have a pointed, hook-like aedaegus, which is an appendage used to transfer sperm to the female. It’s a bit like a penis, although in deference to this particular method of reproduction, let’s just call it a STABBYCOCKDAGGER*. The male, without so much as a by-your-leave, simply shunts his STABBYCOCKDAGGER straight into the female, releasing sperm into her body cavity.

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STABBYCOCKDAGGER

This isn’t controversial because of the process itself – after all, traumatic insemination is well-characterised in various other species (in particular, the Cimicidae – or bedbug – family: one of the most interesting talks I’ve ever seen was Mike Siva-Jothy presenting some of his work on bedbugs at the ESEB conference in Tuebingen, 2010) – but more due to the lack of detail as to how or why this might have evolved. The reasons for such an adaptation include the following: bypassing ‘mating plugs’ (in many species, a male can inject a secretion into the female’s reproductive tract, ‘gluing’ it closed, or can even break off its penis – or STABBYCOCKDAGGER – in the female so as to block access by rivals); getting round female resistance to mating; eliminating any time that would otherwise be required for courtship; or even in terms of sperm competition, by enabling males to deposit their sperm closer to female ovaries. However, studies indicate that short-lived Stylops males are unlikely to encounter many competitors, and the females stop producing the attractive pheromone just a few days after mating (so the period during which she may attract males is reasonably brief). A study using scanning and transmission electron microscopy in Xenos vesparum failed to either support or rule out traumatic insemination as a mating strategy, but did provide further evidence (adding to studies dating back to the 1840s) that males could simply be using their STABBYCOCKDAGGER to spread sperm fluid into the female’s ‘ventral canal’, which sounds like a much more soothing process. In fact, a ‘spread into a ventral canal’ sounds like a nice holiday that you might take in the Cotswolds. It is possible that this latter method was actually the ancestral form of mating, and that traumatic insemination has developed more recently – potentially so as to bias paternity.

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Yes, I know that isn’t a face, it’s the female’s ventral canal. POETIC LICENCE, YEAH?

Are you happy now?

Happy?, you might ask, happy that you just did the text-based equivalent of screaming STABBYCOCKDAGGER in my face, over and over again?

Oh. Well, then you might be interested to hear about ‘hemocelous viviparity’. Doesn’t sound so bad, right? It’s just that the eggs hatch inside the female, and the offspring eat their mother from the inside out; the larvae then escape from the host and use tiny little legs to run around and find new hosts.

Also, in the case of X. vesparum, the host is a wasp named Polistes dominulus; parasitised female wasps become sterile, inactive, and leave their colony to form aggregations where the parasites can perform their curious mating. Cappa et al. describe them memorably as “idle, gregarious ‘zombies’”. There is also evidence that ants parasitised by other Strepsipterans tend to linger on the tips of grass stems, even in bright sunlight, which may increase the chances of males finding a mate, or even just give the males a good start when emerging from their own host. Such behaviours may be due to our twisted little parasites somehow manipulating their hosts to their own ends.

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To conclude: extreme sexual dimorphism, traumatic insemination, cannibalisation of their own parents, and turning hosts into sterile zombies? Safe to say these strange little flies do a little bit of everything. And maybe, just maybe, you’re glad that creatures the size of lions don’t behave like this after all.

*I asked on Twitter whether people had a preference towards either ‘STABBYCOCKDAGGER’ or ‘STABBYCOCKNEEDLE’. The results were overwhelmingly in favour of ‘STABBYCOCKDAGGER’.

References

Wojcik, D.P. (1989). Behavioral interactions between ants and their parasites. Florida Entomologist, 72(1), 43-51.

Hughes, D. P., Kathirithamby, J., Turillazzi, S., Beani, L. (2004). Social wasps desert the colony and aggregate outside if parasitized: parasite manipulation? Behavioral Ecology, 15(6) 1037-1043.

Beani, L., Giusti, F., Mercati, D., Lupetti, P., Paccagnini, E., Turillazzi, S. and Dallai, R. (2005). Mating of Xenos vesparum (Rossi) (Strepsiptera, Insecta) revisited. J. Morphol., 265: 291–303. doi: 10.1002/jmor.10359

Beani, L. (2006). Crazy wasps: when parasites manipulate the Polistes phenotype. Annales Zoologici Fennici., 43(5-6), 564-574.

Cappa, F., Manfredini, F., Dallai, R., Gottardo, M., Beani, L. (2014). Parasitic castration by Xenos vesparum depends on host gender. Parasitology, 141(8), 10808-7.

All strepsiptera images modified from Beani et al., 2005.

Other images used under a creative commons licence.

Additional links

There is a flickr group for all things Strepsiptera; not many pics, but they are quite wonderful.

Gregory Paulson has a nice bunch of SEM images of strepsiptera here.

Immediately prior to my posting this (well, the first time around), Sam Evans asked on Twitter whether I was writing about bed bugs, and sent me this cartoon. It’s basically a ‘Simpsons did it!’ for anyone blogging about traumatic insemination. THANKS GUY.

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