A good year for mind-controlling ladybird-munchers

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Dinocampus coccinellae: a fearsome foe of ladybirds. Photo: Wikimedia Commons

For my Masters Research Project (MRP) I am taking a look at righting and death-feigning among beetles, including a couple of ladybird species. I made the decision that I would try and work with natural populations wherever possible – the only problem with that, of course, is that nature can be the cruellest cohabiter.

Upon setting up a colony of seven-spot ladybird (Coccinella septempunctata), it quickly became apparent that I had a bit of an issue; namely finding quite a few specimens protectively guarding yellow cocoons. Doing such a good job of it, in fact, that it was almost impossible to remove them from both cocoon and plant. Dinocampus coccinellae had joined my project uninvited.

I was aware of possible parasitism of beetle juvenile stages, including those of ladybirds, but not the wasps with a penchant for taking on adults. Little did I know that this is the Braconid wasp D. Coccinellae’s stock-in-trade – and one that it’s building up such a reputation for its it’s started to become a minor mainstream news story. Indeed, once I was aware of it, I started to see ladybirds in their natural habitat sitting on cocoons seemingly everywhere, like some strangely beautiful horror movie in the undergrowth.

Coccinella septempunctata in aggressive cocoon-cuddling mode. Photo: Brad Foster (Twitter @bradwaspfoster)

The parasitoid was first given a full biological description in 1926 after it was first noted in Europe, and since then, boy has it settled in.

One facet of the appeal of insects is a feeling that the aliens are among us already – and indeed parasitoids really did inspire that scene in the film Alien. With D. coccinellae, it is isn’t just about depositing an egg inside the ladybird and leaving its young to, all being well (from the wasp’s perspective of course), burst out of its host’s body an adult. It goes in for full-on control and manipulation, creating ‘zombies’ from ladybird hosts that guard a wasp cocoon spun between its legs by larvae after they’ve had their feeding fun. In its sensory-controlled state, the ladybird twitches to deter predators as the larvae pupates and hangs in there for adulthood. They do a fine ‘bodyguard’ job too, with studies showing only 15% survival against predators with host protection, and 65% with.

This may well be a problem of particular concern to the seven-spot ladybird, as research has shown that while it’s wily wasp enemy can decimate its populations, successful parasitism and emergence rates of the wasp are significantly lower when it makes an ovipositional attack on the invasive Harlequin ladybird, Harmonia axyridis, while the two-spot ladybird, Adalia bipunctata, is an unsuitable host altogether. To make matters much worse for C. septempunctata, it has been demonstrated that its toxic defence chemicals actually act as a considerable attractant to D. coccinellae. Bloody hell, nature.

It seems that a perfect storm is gathering, where a wasp, a highly-successful invasive competitor, a fairly narrow (and early in the year) breeding period and other environmental stressors are combining to make life extremely difficult for one of the UK’s classic ladybird species. Will it withstand the onslaught? Too early to tell – but there are certainly reasons for concern.

As for my experiment, maintenance of colony health since the first sightings has proved a game of watching intently for signs of parasitism, removing rapidly, rinsing and repeating. But stare into D. coccinellae’s intensely beautiful shiny green eyes under a microscope and you can’t help feeling this is an animal you’re never going to quite have the measure of. Allow me this excessive sweep of anthropomorphism: its gaze really does follow you around.

While my run-in with this small wasp has provided much by way of irritation, once you’ve taken a step back from your emotional response, it’s hard not to simply admire a highly-specialised species succeeding in its niche. That is, however, likely to be extremely cold comfort for those looking to conserve the UK’s native ladybirds.

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On Insect cocks

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Cock. Penis. Dick. Wang. Whatever you call the male appendage, this is an area of insect physiology where things get pretty wild. Or perhaps more accurately, wilder than the usual.

But let’s start scientifically-correct: in the insect world the closest thing to the human penis is more properly known as the aedeagus. But ‘closest thing’ does not in any way imply great similarity. It’s actually part of the insect abdomen, and the external part of the male’s sexual weaponry is a phallus of extremely various flaps, hairs and hooks. Still with this? Good.

When it comes to shape, describing the situation as complex doesn’t get anywhere near to doing it justice. Menno Schilthuizen’s account of genital evolution is a comprehensive overview (far more so than can be included here), highlighting a wonderfully alien world of ‘prongs’, ‘pegs’, ‘springs’ and ‘titillators’. If insects are purely in it for the passing of genes, they could’ve fooled us.

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Amazing aphid dicks: from Wieczorek et al, 2011 

There’s so much to say about the morphology of aphid appendages alone that the main journal paper on the matter comes in two parts. For relatively small insects, aphids come with a significant package – “relatively large and discernible under a hand lens or even with the naked eye”. The paper includes such descriptive gems as “a few circular pits distributed mostly in its medial part. Sclerotized arms with distal part rather long and thin, and proximal part shorter and wider. Aedeagus long, inverted question mark-shaped.” And that’s just the aphid Drepanosiphumplatanoidis. Big name, big aedeagus.

Smutty jokes aside (but not for long), in insect taxonomy, male sexual organs can be extremely helpful in establishing exactly what species you’re dealing with. In fact, it can often be the only way of making a certain identification. So far, so useful, to us as well as them. But how do insects actually, you know, do it? Again, this is no simple matter.

dragonfly dicks - miller 1991

Normal for dragonflies: from Miller, 1991

The ‘lock and key hypothesis’ is an idea that has persisted in entomology – and, naturally,
argued over. It asserts that male and female sexual organs of an insect species, whatever wacky shape and size they are, have evolved to only be the exact ‘fit’ for each other. The theory, however, has been largely discredited over the years.

What’s abundantly clear is that sex is rarely anything straightforward in the insect world – there’s little by way of proxy for missionary. Dragonflies are a good go-to example for the messiness of it all – so much so that their sexual antics inspired a New York Times article, in which the slaty skimmer (Libellula incesta) is described as having a “fairly rococo penis”. Sex begins with what constitutes foreplay – the male grabbing the female at the back of the head – while dragonfly dongs are not just about depositing sperm, they’re also about removing that of rivals. Naturally, females are tooled up to stop that happening, if at all possible.

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Brutal bruchid beetle bell-end: Wikimedia Commons

The mealworm beetle (Tenebrio molitor) also has a dick geared up to dispatch the genes of its rivals. In the words of this paper on the matter, it “comprises a central shaft enclosed within a flexible sheath covered with chitinous spines. As the shaft extends within the female’s copulatory bursa the sheath and its covering of spines rolls back producing a `scouring’ effect.” Lovely.

With schlongs often more resembling torture implements, things can get even more brutal. Males of the bruchid beetle (Callosobruchus maculatus) actually damage the female’s reproductive tract during sex, and females, understandably, kick them for it. If she doesn’t kick, injuries tend to be worse after a longer sex session. Yet according to this paper, the carnage is not a deliberate act of destruction by the males, just an unfortunate by-product of them evolving weapons that are literally weapons. Why, it’s not yet known, but the theory is its all about being able to cling tightly to their ‘loved’ one.

If this blog puts insects in danger of being adopted by the alt-right as beacons of ultra- masculinity, hold that thought right there. Transgression of gender norms is happening in Brazilian caves, don’t you know. In the louse genus Neotrogla, it’s the females with the penis-like protrusion, and the guys with a chamber comparable to a vagina. A very niche re-definition of ‘wearing the trousers’ for sure, and in marked contrast to the species of beetles and dragonflies using their phallus to screw over their rivals with a bit of sperm scooping, our ‘macho’ cave-based females are using theirs to collect it up. Through all the kink and horror, life finds a way.

So there, a piece about insect nobs has been published on the Entomology MSc blog. I can only hope this comes up in the exams in March, making things a little less hard. Too much smut? Probably.

 

Insect Bites: The Sunday Digest – Cheating the super-organism

A familiar sight for many people, whether they are entomologically inclined or not, is ants working in what appears to be a cohesive manner. Naturalists in the early twentieth century described these assemblies of individual ants as ‘super-organisms’.

Like bees, wasps and termites, ants are eusocial. This means within one species there are often workers, soldiers and queens. Each of these so called castes has its own unique role within the colony and appear very different to each other despite being the same species. Individuals in these complex societies would be unable to survive alone; colony life is essential for individual survival.

Despite ants being evolutionarily and behaviourally advanced when compared to many other organisms, one group of beetles have managed to exploit them in an incredible way.  This group of beetles are a sub-family of rove beetles called Pselaphinae, pronounced “Seh-LAH-Fin-Ee”. This sub-family contains around 10,000 described species with many still undiscovered in ecosystems all over the world, and many left in museum collections still un-named. They have evolved complex morphological (structural) features which mean they can co-exist with ants, utilise colony resources and benefit from the ants’ protection.

Within Pselaphinae, a group of 369 species collectively known as the Clavigeritae (“Cla-Ve-JEH-Ri-Tee”) have taken the cheating to a whole new level. They have managed to fool ants into trophallaxis, a phenomenon where the ants directly feed the beetles, mouth-to-mouth. This kind of behaviour makes it clear that Pselaphinae seem to be treated as just another ant in the colony, evading the usual aggressive behaviour that ants exhibit towards outsiders! To facilitate this mouth-to-mouth feeding, the Clavigeritae have evolved brush like features (Trichomes) on the base of the abdomen which exude a substance that the worker ants find attractive to feed on, and seems to calm any aggressive behaviour. In addition, the beetles’ mandibles are not designed for hunting or grabbing prey, but perfectly suited to direct feeding from ants, being non-serrated and often circular in shape.

The development of these close and complex relationships between ants and Pselaphinae must surely be the result of million years of co-evolution. With ants containing a similar number of species to Pselaphinae, this may go some way in explaining the incredible diversity of these ant-exploiting beetles as they have specialised and speciated (the formation of new species) in close accordance with ant diversification.

A recent paper, published in “Current Biology” by Joseph Parker and David Grimaldi, has shed light on when these advanced ant-loving beetles first evolved and backs up the idea that Pselaphinae and ants have co-evolved for tens of millions of years. A single ant-loving beetle found in Indian Cambay amber that is about 52 million years old shows that these ant-loving beetles were present before ants diversified and gained dominance in ecosystems.

The association between ants and the organisms that ‘love’ them is known as myrmecophily. Other than numerous myrmecophilous species of Pselaphinae, these interactions are also found in another sub-family of rove beetles, Aleocharinae. This sub-family is even more diverse than Pselaphinae, containing 13,000 or so described species. Some myrmecophilous species of Aleocharinae resemble ants with constricted waists and a tendency to walk among the long winding trails of ant workers where they blend in perfectly. They themselves do not produce a chemical that appeases the ants, as in Pselaphinae, but instead they groom and obtain odours directly from them, thus enabling them to co-exist with the ants and perhaps, more importantly, avoid predators.

The Aleocharinae species Thyreoxenus brevitibialis has integrated into termite colonies by evolving a body form extremely similar to that of termites. The most obvious feature this beetle has evolved is the swelling of the abdomen, also known as physogastry, a typical characteristic seen in its victim.

The clown and king of termitophily is without a doubt Coatonachthodes ovambolandicus. Physogastry (swelling of the abdomen) in this species enables it to mimic its host termites down to a tee. The illustration below does the talking, showing all legs and antennae replicated in the beetles abdomen.

 

Capture

Coatonachthodes ovambolandicus: the termite mimic. Side on illustration (left) and dorsal view (right). Dorsal view showing the physogastric abdomen from above with all appendages including antennae mimicking a termite worker. Illustration from Kistner (1968), adapted by Kleisner & Markoš (2005).

It seems social insects are a victim of their own success, and not by coincidence. It is said that ant biomass is similar to that of humans and their impact on the environment is significant due to hoarding of materials for nests. The same can be said of termites and their mounds. These resource rich locations are clearly attractive to other organisms. In particular, Pselaphinae and Aleocharinae rove beetles have managed to exploit these advanced social insects perfectly, evolving to cheat the super-organism.

 

Author – Joshua Jenkins Shaw (@jenksshaw)

Further reading

Kistner, D.H. 1968. Revision of the African species of the termitophilous tribe Corotocini (Coeloptera: Stapylinidae). I. A new genus and species from Ovamboland and its zoogeographic significance. Journal of the New York Entomological Society 76. P213–221.

Kleisner, K. & Markoš, A. 2005. Semetic rings: towards the new concept of mimetic resemblances. Theory in Biosciences 123. P203-222.

Parker, J. & Grimaldi, D.A. 2014. Specialized myrmecophily at the ecological dawn of modern ants. Current Biology 24. P1-7.

Wheeler, W.M. 1911. The ant colony as an organism. Journal of Morphology 22. P307-325.