Why protective parenting is key for the survival of tropical insects

Shield bug guarding her eggs in the Ecuadorean rainforest. Andreas Kay/Flickr (CC BY-NC-SA 2.0)

As humans, the concept of parenting and care giving is often ingrained so far into our lives that it is easy to take it for granted. On a recent visit to the zoo, my two-year-old recently asked, “but where’s the tortoise’s mummy?” She made the quite reasonable assumption that all animals come in nuclear families, and are just as committed parents as are most of us humans.

Perhaps we take parental care for granted because we are mammals, and every mammal species cares for offspring – at least to some extent. But aside from us mammals, most species – including almost all tortoises – actually abandon their offspring as soon as they can, making species that actually parent a tiny minority. Especially species like us, where dads are typically involved as well as mums.

Another group where most parents usually abandon their eggs immediately is the arthropods – a large group including insects, spiders, crustaceans and many others. But of the arthropod species that do care for their offspring, some are among nature’s most devoted parents. And our new study shows that this parental care often evolves because of the risk of predators.

Extreme parenting

Parental arthropods have long fascinated generations of scientists, and as early as 1764, the Swedish naturalist Adolph Modeer patiently watched a tiny – but very brave – “parent bug” stand over its offspring and challenge attackers instead of fleeing.

Female parent bug defending her offspring.

Others take parenting behaviour to extremes – such as some female spiders, who allow their babies to eat them. These mothers only ever have one brood of offspring, so technically they have nothing to lose – why let your nutritious corpse go to waste? And research has shown that by eating mum, spider babies actually grow to be bigger adults. This gives them a kickstart that boosts their chances of reproduction compared to those babies that are lumbered with more stingy, non-suicidal parents.

Females of some spiders in the family Eresidae are eaten by their offspring.

Compared to suicidal spider mothers though, most arthropods that provide childcare are slightly less gung-ho about it. But they can still help to boost their babies’ survival prospects. Bromeliad crabs, for instance, lay eggs in rainwater pools formed in the spiral or “rosette” of rain-forest plants. The mother crab patiently drops snail shells into the water, which elevates calcium levels just enough for the baby crabs to form their tiny shells.

Predator pressure

An obvious question then is why only some – and not all – arthropods care for their offspring. And one longstanding idea is that care evolves in places where undefended offspring are more vulnerable to predators. The great biologist E.O. Wilson suggested that we could test this idea by looking at where the parent and offspring happen to be living. This is because insect predators are cold blooded – and their level of activity depends on temperature. So the hotter it is, the more active they are – and so the more intense the risk from predation tends to be.

Based on this idea, it would stand to reason that leaving offspring unattended in the tropics would be more risky – because unattended offspring would encounter more predators in the tropics than offspring in cooler, drier environments. This idea is simple and intuitive, but it has gone untested for over 40 years.

Harvestman guarding eggs.

Over the years, many insect studies have involved removing the parent to observe what happens to the offspring. This allows scientists to see the difference in survival between experimental groups without a parent, and control groups with a parent. This difference can be interpreted as the benefit of parental care.

In some species, broods are entirely destroyed by predators when parents are removed. Others incur more minor losses. In at least one case, offspring actually survive better without their parents. Despite their best efforts at defence, females of one particular species of stink bug actually attractparasitoid wasps” – rogue insect robbers that hijack and consume eggs and larvae. The mother bugs act as signposts for wasps who might otherwise have passed over the eggs without noticing.

Love in a warm climate

In our study, we analysed data from many of those removal experiments conducted over the years, to find out whether – as Wilson suggested – the benefits of care are greater in the tropics.

The results showed that almost all the control groups – the ones that hadn’t had the parents removed – survived better than the removal groups who were left to fend for themselves. Critically, the culprits were almost always predatory insects, mostly ants. This shows that parental care is generally an effective defence against predators. And, as we predicted, the effect of removing parents tended to be greater in tropical locations than in cooler, drier climates – finally confirming Wilson’s hypothesis.

In tropical locations, offspring have a greater need for protection from predators.

But this was only the case in species whose eggs are completely undefended without their parents. For species who also have a back-up defence – such as nests, burrows, or eggs covered in mucus – eggs in the tropics fared no worse than eggs in cooler locations, once parents were removed.

This shows that there are other strategies open to arthropod mothers for keeping offspring safe as well as physically guarding them. And in the tropics, where parental care may not always be enough, mothers may well need several lines of defence against predators.

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Reality bites: the mutant giant-penised fleas invading the tabloids

Coming to a dog near you… photo: Cosmin Manci

 

 

Here we go again. The latest wave of shouty headlines about outsized monster invaders is rolling in. The latest crop – fantastically – are the “billions of super fleas with giant penises” invading British homes.

These monsters are giants, said The Mirror – “far bigger than normal fleas”. And, according to The Express, they “have mutated to have large manhoods and are now immune to poisons”. The Sun went even further, suggesting that their penises were all “erect”. Save yourselves!

Hysteria around arthropods (insects, spiders and their allies) is common fodder for newspapers – it’s been barely a month since a completely different swarm of “giant cannibal spiders” was “invading British bedrooms”. Pholcids, the spiders in question, are not only utterly harmless but are in fact beneficial because they eat other less harmless insects.

Such headlines pour oil on an unhelpful fire of general fear and aversion towards arthropods. This fear is unnecessary and avoidable. An awesome experiment involving Doctor Who in 2011 demonstrated that there is nothing innate or evolutionary about this fear – and it most likely persists through cultural reinforcement. So if we don’t teach our kids to be afraid of bugs, they won’t grow up afraid of bugs. And that means they won’t miss out on a whole world of awesome.

At least with fleas there is something to be genuinely concerned about – they are, after all, obligate bloodsuckers and can be vectors for several important diseases including bubonic plague. But we have been living and dealing with fleas for centuries. Caution is sensible; blind panic is not.

But what’s all the fuss about these fleas and their penises? A flea’s penis, however giant, is quite the wrong end of a flea to get worried about.

Let’s try and unpick this story a little.

Are fleas invading?

To begin with, fleas are not “invading” – they are already found everywhere except the Arctic. Fleas typically follow cycles with adult populations booming in summer and generally dying away in winter. They thrive in damp, humid conditions but cannot develop below about 13°C, meaning winter usually halts their activity.

However, there has been a succession of increasingly wet summers and mild winters, which provides good conditions for flea breeding. So fleas may be proliferating in the balmy weather. Some veterinary organisations and charities have reported increases in cases. And these reports appear to have been cherry-picked by tabloids in an effort to create panic.

But Natalie Bungay of the British Pest Control Association said: “There have certainly not been any reports of any anomalies in flea reports whether it be the size of them or frequency of them.”

Pesticide-resistant mutants?

Neither is there any truth in the claim that these insects are resistant to current pesticides. While fleas may have become resistant to many older insecticides, there is no conclusive evidence of any resistance to more modern chemical treatments. Concerns about what looks like resistance are mostly down to failure to follow, or stick to, product directions.

There is also no obvious evidence that fleas are getting any bigger. Neither, disappointingly, are their penises.

How giant, exactly? Asking for a friend

However, it has to be said: there is at least truth in the rumour of “giant-penised fleas”. Fleas do have extraordinarily long penises. Being in possession of a 3.3mm appendage may not sound like much, but it is up to 2.5 times the flea’s own body length – on an average man that’d be a four-metre member. But this was the case anyway – there is no new breed of particularly monstrously hung mutants, just the regular well-endowed ones.

The penis size of the flea is a record for insects, although not for animals generally as is sometimes claimed. That honour goes to the barnacle (eight times its body length, which would be 14 metres on a human in case you are wondering).

But flea genitalia are hardly a clear and present threat. On the contrary – what flea penises are is fascinating. They have been described as “the most elaborate genital organ in the animal kingdom”. The penis is an immensely long wispy ribbon-like structure, kept coiled up inside the abdomen when not in use. It is so thin that it is “only faintly discernible”, even under a microscope, and cannot enter the female by itself. It must be supported by extra structures called “penis rods” which, along with external claspers, help to manoeuvre the whole apparatus into place for mating to occur.

Left: The flea penis, 2.5 times its body length, is kept coiled up inside the structure shaded red in the abdomen when not in use. Top right: Human flea Pulex irritans. Bottom right: isolated male genitalia of P. irritans Left:TB Cheetham 1987, PhD, Iowa State/Entomology Commons; Top right:KatijaZSM/Wikipedia/CCBY3.0; Bottom right: F Abang 1993, PhD, Iowa State/Entomology CommonsLeft: The flea penis, 2.5 times its body length, is kept coiled up inside the structure shaded red in the abdomen when not in use. Top right: Human flea Pulex irritans. Bottom right: isolated male genitalia of P. irritans Left:TB Cheetham 1987, PhD, Iowa State/Entomology Commons; Top right:KatijaZSM/Wikipedia/CCBY3.0; Bottom right: F Abang 1993, PhD, Iowa State/Entomology Commons

The precise function of the penis rods is not entirely clear – one end is shaped “like a cobra’s hood”, so they may act to scoop out rivals’ sperm. Alternatively they may help to transfer the sperm to the female – one author observed sperm with tails “wound around the penis rods like spaghetti on a fork”. Nobody really knows.

Such a delicate, fragile organ is hardly something to strike terror into the hearts of the nation, so why all the tabloid hate?

Maters gonna mate

Maybe they were thinking of Strepsipteran penises, or possibly bedbug penises. Those are a whole different, rather stabbier ball game: genuinely the stuff of nightmares. Look them up if you dare. Or maybe bushcricket genitals, some of which resemble bear traps and handcuffs.

The mechanical details of how males and females mate is enormously important in determining whether – and which – DNA is passed on. It’s therefore somewhat central to the process of evolution. Genitals are used as anchors, hooks, locks and keys, turnstiles, advertisements, titillators, manhole-covers, crowbars, weapons, mazes and many more – and with such a bewildering array of functions they are some of the fastest-evolving structures in nature.

Insect genitals, particularly, are a smorgasbord of delightful weirdness. Male damselflies have shovel-shaped penises for removing rivals’ sperm. Some male spiders snap off one of their two detachable penises inside their mate, both to deter future lovers and to prolong sex while they run away. Female barklice’s vaginas are shaped like a prehensile penis and literally reach into the male to grab his sperm.

The point being: insect genitals are compelling enough already, without the need to invent reasons to be scared or disgusted by them “invading our bedrooms”.

So fleas may be enjoying a bit of a comeback in some warm, wet weather. But they are not invading, and neither are they mutants with giant penises. Fleas, in general, have impressive members – but the flea class of 2016 has no particular claim to endowment over previous alumni.

This fathers’ day, be grateful your dad is a human

A hungry assassin bug munches on one of his babies

This post originally appeared [a shockingly long time ago – my apologies!] on The Conversation on 20 June 2015. Read the original article here.

Each father’s day we celebrate male parental care. But this year – perhaps while getting the old man an appreciative gift -– maybe have a think about why men want to care for their children at all. As opposed to, say, eating them alive.

Fatherhood comes so naturally to us that we can easily forget to ask about how and why it might have evolved. In fact, most fathers in the animal kingdom don’t do it. We fall into a rather rare group of species where males provide any care at all.

In our primate relatives, for instance, males are not at all doting – with a few exceptions, like male marmosets, who carry babies on their backs. This lightens the load on the female – presumably allowing her to make the male’s babies bigger, or to have more of them.

Absence makes the heart grow fonder?

Among mammals, dads rarely contribute to offspring beyond a single sperm – the mother generally nurses offspring alone. Except in Dayak fruit bats, where males have been found lactating (although still contentious).

Male and female grey jays feeding chicks. Dan Strickland/Wikipedia

It is in birds that male-female cooperation is most common, probably because feeding chicks and keeping them safe and warm is a two-person job. But in other birds – where newborn chicks can get up and walk for themselves, like chickens and ducks – the male is typically nowhere to be seen. He’s off soliciting new mates.

Best of a bad job

Males will sometimes help females out if they are unlikely to find another mate. Burying beetles breed on fresh mouse carcasses, which are very scarce. Having finally found a carcass, a male will stick around and help the female care because he is unlikely to find another – but he will also keep signalling to attract other females. The resident female is understandably not on board with this, and knocks him over while he’s trying to signal.

In many familiar species like gorillas and lions, males that appear to be caring are really mostly concerned about guarding their baby-mamas from rival males; the offspring are kept safe as a byproduct.

Ranitomeya poison frogs cooperate to raise offspring. Nicop69/Wikipedia

Yet some amazing examples of biparental care exist. In Peruvian poison frogs, the male carefully carries his tadpoles to a water pool. There, he monitors their progress for months: every week or so the watchful male calls to the female, who comes and deposits special nutritional eggs into the pool for the tadpoles to eat.

But in most cases, fathers are conspicuous by their absence – deserting the female as soon as they can.

Why so callous? To begin with, super-cheap sperm means the most successful males can potentially have unlimited offspring – if the species’ ecology allows it. This can even hold true for humans. The Sultan Moulay Ismail of Morocco, for example, may have had more than 1,000 children (compare that to the women’s record, a nevertheless astonishing 69).

But because it takes two to create a baby, the fact that some males can be extremely successful means that others get nothing (Ismail’s citadel must have been full of childless men). Today we think of ourselves as monogamous, but there are often still more childless men than women. For those male animals that are more successful, caring interferes with a winner’s strategy of pursuing mating. So in evolutionary terms males need a very, very good reason to care for offspring, or they will always do better seeking mates.

Dads defying the odds

Yet, in some species, males do all the care, with females contributing little apart from eggs. Although fairly common in egg-laying fish, male seahorses have taken it to extremes – they have a placenta and give birth to live young. Male rheas sit for weeks on a pile of up to 80 eggs, while male brushturkeys carefully tend piles of fermenting leaves so that the heat can incubate their eggs. In weird “sea spiders”, males tend eggs in all 1,300-odd species.

Male seahorses become pregnant, nourishing and protecting their fry until birth. Kevin Bryant/Flickr

Sometimes males have no choice but to care. Some males have to “mate-guard” females against rival males, right up until egg-laying – whereupon the female can run away leaving the male holding the babies. In others, like kiwis, females produce huge offspring and exhaust themselves, leaving males little option but to care. In Neanthes worms, before caring, the male resourcefully eats the female.

Occasionally, as in jacanas, males greatly outnumber females, who can therefore get away with dumping males with offspring. These males are unlikely to secure another mate, so their best option is to care.

But many of these “superdads” do some pretty cold calculus. Single dads are most likely to evolve where they still can mate while caring, and where care is cheap (like standing guard as opposed to feeding young). In territorial species like rheas and egg-laying fish, males with good territories guard clutches from many females. Or they make sure to seal the deal on their paternity. A male giant water bug typically carries only one female’s eggs on his back – but he makes the female mate several times while laying eggs.

In assassin bugs, males also accumulate eggs from many females, like rheas. But care is hungry work for these predators. They have a dark solution: to maintain body weight, they eat some of their own eggs.

Male scissortail sergeants eat their whole brood if it’s not big enough to bother caring for. Patrick Randall/Flickr

Male scissortail sergeant fish make an even more straightforward calculation. If the brood is too small, they cannibalise the entire brood and search for another mate. Makes sense – without a parent, the babies are doomed, so why waste them?

Humans: the verdict

Where do human fathers fit? They don’t habitually eat offspring, nor do they accumulate piles of babies from many women. As always, there is a lot of variation. Some are not involved, like the male chimpanzees to whom we are most closely related. But many enjoy a long and satisfying fatherhood, both teaching and learning from their children. These men may be more like wolf fathers – who provide food for their partner while she is pregnant and for their cubs once weaned; they also critically provide behavioural input in terms of play, and act as a role model. Most likely, this has evolved because such learning and experience are vital to offspring success in both species.

Grey wolf fathers are highly involved in parental care. Taral Jansen/Wikipedia

As a relatively new dad myself, this father’s day, I am thankful I belong to a species where fathers can make a valuable contribution to their offspring’s lives beyond mere genetics.

 

Secrets of the orchid mantis revealed – it doesn’t mimic an orchid after all

The orchid mantis, Hymenopus coronatus. Igor Siwanowicz
The orchid mantis, Hymenopus coronatus. Photo: Igor Siwanowicz

An article I originally wrote for The Conversation. Read the original article here.

In his 1879 account of wanderings in the Orient, the travel writer James Hingston describes how, in West Java, he was treated to a bizarre experience:

I am taken by my kind host around his garden, and shown, among other things, a flower, a red orchid, that catches and feeds upon live flies. It seized upon a butterfly while I was present, and enclosed it in its pretty but deadly leaves, as a spider would have enveloped it in network.

Orchid mantis: Hymenopus coronatus
frupus, CC BY-NC

What Hingston had seen was not a carnivorous orchid, as he thought. But the reality is no less weird or fascinating. He had seen – and been fooled by – an orchid mantis, Hymenopus coronatus, not a plant but an insect.

We have known about orchid mantises for more than 100 years. Famous naturalists such as Alfred Russell Wallace have speculated about their extraordinary appearance. Eschewing the drab green or brown of most mantises, the orchid mantis is resplendent in white and pink. The upper parts of its legs are greatly flattened and are heart-shaped, looking uncannily like petals. On a leaf it would be highly conspicuous – but when sitting on a flower, it is extremely hard to see. In photos, the mantis appears in or next to a flower, challenging the reader to spot it.

Hiding in plain sight?

On the face of it, this is a classic evolutionary story, and a cut-and-dried case: the mantis has evolved to mimic the flower as a form of crypsis – enabling it to hide among its petals, feeding upon insects that are attracted by the flower. Cryptic mimicry by predators is well known. For example, crab spiders camouflage themselves against a flower, and can change from yellow to white to match their host flower.

Crab spider (Misumena vatia) with wasp prey.
Olaf Leillinger/Wikimedia

The orchid mantis is something of a poster child for such cryptic mimicry. So obviously true is this evolutionary story that it is often discussed today as established fact.

No one seemed to have noticed that there has been no evidence to support this hypothesis. Orchid mantises are actually very rare in the field, so their behaviour is hardly known about, except in captivity. For example, nobody knows exactly which flower the mantis is supposed to mimic.

Now a set of new studies by James O’Hanlon and colleagues shows quite clearly that we’ve been getting it wrong all this time. While it is indeed a flower mimic – the first known animal to do this – the orchid mantis doesn’t hide in an orchid. It doesn’t hide at all. And to an insect, it doesn’t even look particularly like an orchid.

A deadly lure

O’Hanlon and colleagues set about systematically testing the ideas contained within the traditional view of the orchid mantis’ modus operandi. First, they tested whether mantises actually camouflage amongst flowers, or, alternatively, attract insects on their own. For a flower-seeking insect, as predicted, the mantis’ colour pattern is indistinguishable from most common flowers.

However, when paired alongside the most common flower in their habitat, insects approached mantises more often than flowers, showing that mantises are attractive to insects by themselves, rather than simply camouflaging among the flowers.

“We can clearly observe insects, like bees, diverging from their flight paths and flying right towards this deceptive predator,” O’Hanlon told me. “These beasties are marvellous for this kind of question, because we can observe a dynamic interaction between predators and prey.”

This phenomenon, known as aggressive mimicry, occurs in other animals. The Bolas spider releases chemicals that imitate sex pheromones released by female moths seeking a mate. Male moths, with their elaborately plumed antennae, can detect these pheromones from miles away, and are lured in to their death. Carnivorous Photuris firefly females can mimic the flash-responses of a different species of firefly, attracting amorous males who find themselves on the menu.

Next the researchers assessed where mantises chose to sit. Surprisingly mantises did not choose to hide among the flowers. They chose leaves just as often. Sitting near flowers did bring benefits, though, because insects were attracted to the general vicinity – the “magnet effect”.

Any old flower

When they compared the mantis’s shape and colour with flowers from an insect’s perspective, the predator did not resemble an orchid or indeed any particular species of flower, but rather a “generalised” flower. This fits with what we already know: some of the best mimics in nature are imperfect mimics with characteristics of several “model” species.

Placing experimental plastic models out in the field, the researchers found that mantis colour was much more important than shape in attracting insects. They believe that mantises may not actually precisely mimic a particular kind of flower. Instead they may exploit a loophole created by evolutionary efficiency savings within the insect brain.

Jumping to conclusions

As humans with giant, hyper-developed brains capable of abstract thought, we have the luxury of being able to make decisions using all the available information. After a few seconds of scrutiny, what initially looks like a flower because of its colour begins to look suspicious – and once we spy bug eyes and a vaguely insectoid outline, the game is up: it’s a mantis.

But a tiny insect zipping around on the move, with its compact brain, cannot afford such cognitive extravagance. It has a shortcut – a rule of thumb: anything matching colour X is a nectar-containing flower. More colour equals bigger flower, with potentially more nectar. No cross-checks, no two-step authentication. The mantis takes advantage of this shortcut by using “sensory exploitation”. It is a concentrated mass of the right colour – a supernormal stimulus. The insect classifies the mantis as a giant nectar-filled flower and approaches to investigate – to its doom.

“This work is terrific,” Martin Stevens of Exeter University, an expert on animal deception and mimicry, unconnected with the work, told me. “It’s wonderful to see something that Wallace and others discussed so long ago, finally tested experimentally.”

Colour me beautiful: an orchid mantis nymph devours its prey
Igor Siwanowicz

This is not the first species to lure in prey with sensory exploitation. The white crab spider reflects strongly in the UV, making it highly conspicuous to wandering insects. But the spider still “hides” on a flower. Surprisingly a flower with a crab spider is more attractive than one without: the crab spider mimics UV-reflective floral patterns that guide insects to nectar. But the orchid mantis is the first animal ever shown to mimic an entire flower, attracting insects on its own.

There is one remaining issue, though: if the mantis can attract insects by sensory exploitation alone, muses Stevens, then: “Why have body parts that look like petals? My guess is that the pollinators are initially attracted at a distance through sensory exploitation, but then more accurate mimicry kicks in at close range, when the insects can inspect the mantis more closely for what it is.”

Greg Holwell, who coauthored the study, told me: “What this work really emphasises is that working on a completely unstudied species can produce fascinating results. Getting out there and starting with some solid natural history helps to generate hypotheses that you can subsequently test with field experiments, and can lead to the discovery of completely novel phenomena.”

“While important discoveries are made from laboratory research on model species like fruit flies, every species has an exciting story to tell and can help shape our understanding of how the natural world works.”

Handcuffs, traps and spikes shed light on sex lives of insects

A male Mexican true bushcricket, left, grasps female with bear-trap genital claspers. Photo: L Barrientos-Lozano

(An article I originally wrote for The Conversation. Read the original article here).

Handcuffs, spikes and traps – you would think they were part of some bondage aficionado’s bedroom collection. But what are they doing in the insect world?

A new study I worked on sheds light on why some bushcrickets – usually gentle creatures – get pretty violent when it comes to sex, and in the process helps to settle a decades-old debate about their odd mating habits.

In just a few species of bushcrickets, scattered across the evolutionary tree, we found that males have evolved horrific-looking clasping devices near their genitals. They use them to hold females down for as long as possible after sex is done – that is, after they have transferred all their sperm. This results in long mating sessions, up to seven hours in some cases.

Bushcricket claspers are usually simple feelers that engage with pits on the female. But some species use spiked hooks to grab onto the female, often piercing her cuticle. Others have bear-traps, tongs that wrap around her, or even interlocking “handcuffs” that completely encircle her.

 

Male genital claspers from bushcrickets with relatively normal sex (left) and with protracted sex (right). In Anonconotus (top right) the spike pierces the female’s cuticle; in Phasmodes (bottom right) the interlocking claspers resemble ‘handcuffs’ and completely encircle the female. Photo: Karim Vahed

 

Females of these species are, perhaps understandably, not down with this. Although they themselves have not evolved any defensive tools, they actively resist by jumping, biting and kicking to dislodge the male – and with a degree of success, because species where females resist have less prolonged copulations than those where they do not.

Why would these males want to restrain their partners, when bushcricket mating is usually relatively peaceful? Female bushcrickets aren’t dangerous to males, unlike in some spiders where, before sex, males gas females or tie them up in silk to avoid being cannibalised. The answer takes us into one of evolution’s most important, but also most secretive, conflicts – the battle over what happens to sperm after mating – and also helps answer a longstanding question about some other odd sexual habits of bushcrickets.

Sperm in a bag

The act of mating itself is only the beginning of a struggle to determine which male actually gets to fertilise the female’s eggs. One in which females play just as active a part as males.

For example, female water striders have a submarine hatch covering their genitals, utterly preventing access. Unwanted males resort to “blackmailing” them into opening this hatch by threatening to attract predators. Other female insects have labyrinth-like vaginas with tortuous twists and blind endings. Some females even actively scoop sperm out of the male.

In most land animals, however, we never actually get to see what happens next, because sperm is placed deep inside the female. Often we have to make guesses about what male and females do with their genitalia, based on their shape. But bushcrickets are ideal study animals to look at the evolutionary fate of sperm.

Male bushcrickets transfer all their sperm in a bag, which then drip-feeds into the female after the male has left. But female bushcrickets can, if they want to, get rid of unwanted males’ sperm by simply removing (and usually eating) the sperm bag before the sperm is completely transferred. Males would naturally rather this didn’t happen, and try to stop it. And because this happens outside the female’s body, we have an opportunity to watch what is going on.

The food of love?

If giving females sperm in a drip-feed bag isn’t weird enough, male bushcrickets normally also produce a giant sticky blob of gel from their genitals, which females proceed to eat. This “nuptial gift” is enormously costly to produce, weighing up to 40% of the male’s body weight.

(To be fair, it could be substantially worse for the male – in sagebrush crickets, for instance, females suck the males’ blood during sex and in striped ground crickets they begin eating his legs.)

 

Female bushcricket, Poecilimon thessalicus, feeding on a huge nuptial gift given to her by the male. Photo: Gerlind Lehmann

For decades, scientists have debated what this huge nuptial gift, or “spermatophylax”, is for. Some think that the gift is a nutritious meal that helps the female make more, better babies with the male sperm – a win-win situation that is common in the insect world. Especially when food is scarce, females can use the gift as nutrition for making offspring.

But others think that the nuptial gift is also a device for manipulation – ensuring the female is distracted, so the sperm bag gets to drain as much sperm as possiblebefore she gets around to eating it. Gifts contain very poor nutrition – the equivalent of flavoured chewing gum – and are laced with substances that stimulate the female to feed and also make her less likely to mate again afterwards.

Why bushcrickets get kinky

Our new study looks at some of the more bizarre mating habits of 44 species of bushcrickets to work out why in some cases males have resorted to more aggressive practices.

In a scattering of bushcricket species, we found that, over evolutionary time, males have stopped bothering to produce the nuptial gift for females at all.

In every case where the nuptial gift has been lost, males have evolved to protract sex for long periods even after they have transferred their sperm bag, attempting to restrain the female using hooks, tongs or handcuffs while she desperately resists. In cases where males present females with a food gift, though, the decision appears to be more mutual: females do not typically resist sex, and the males’ genital claspers fit neatly into special grooves on the female with no evidence for conflict.

 

Mating pair of Meconema bushcrickets, female to the left, with male’s genital tongs highlighted in purple (and shown in inset). Photo: C. Roesti

Why do males of these species engage in such violent behaviour? We argue this almost certainly acts to prolong the drainage of sperm from the bag into the female for longer than she wants – the exact same function that had been proposed for the nuptial gift these species have lost. It is highly likely that this restraining behaviour is a substitute for the nuptial gift.

It’s what you do with it that counts

A great many studies of sexual conflict, especially spanning lots of species, focus on the form and complexity of male genital structures in particular – and there are certainly some corkers about.

But our study shows that sexual conflicts don’t necessarily lead to more complex male genital structures. For example, bushcricket male claspers already had simple hooked “teeth” – which usually engage peacefully with pits on the female. Some of our “stingy” males, though, used these same teeth in a different way – holding the female forcefully, piercing her cuticle. Without observing the behaviour, this difference wouldn’t have been obvious.

There is also currently a prevailing view that females are passive or possibly even willing recipients of male attempts to manipulate them. Female genital structures are often not as varied as those of males, and some have pointed to this fact as evidence that there really is no conflict going on. But our study clearly shows that, in this case, females actively and effectively resisted males using simple behaviour – jumping, biting and kicking – and not with specially evolved structures.

Whether you have gin-trap shaped genitals, a giant gift of jelly, or relatively normal-looking sexual apparatus, it is not what you have but what you do with it that counts.

Invertebrates inject a bit of romance during sex – by stabbing each other

Bedbug male stabbing a female during sex. Image: Wikimedia
Bedbug male stabbing a female during sex. Image: Wikimedia

(An article I originally wrote for The Conversation. Read the original article here).

It is fair to say we belong to a species obsessed by sex. We are among the only species to have sex for fun, not just for reproduction. For some other species, though, sex is far from fun. In fact, as two recent review papers show, it is a war zone, involving penis fencing and love darts.

In 1897, the Italian zoologist Constantino Ribaga discovered a strange organ in female bedbugs, halfway up the abdomen. He suggested they used it to produce sound, like cicadas. But something wasn’t right: in the bundle of cells underneath this organ he found large quantities of sperm.

The organ discovered by Ribaga, later dubbed a spermalege. Image: Rich Naylor

How did they get there? At the time, puzzled scientists concluded males must flood females with sperm, and the female digested the excess – as a “nuptial gift” – using this organ. But this theory was tenuous at best.

It wasn’t until 1913 that males were observed stabbing females through this organ with a horrifying syringe-like penis, then copulating with the wound. Sperm swim directly to the ovaries through the body cavity. This has been termed “traumatic insemination”.

In the first of the two papers, appearing in Biological Reviews, Rolanda Lange and colleagues at Tuebingen in Germany and Sheffield in the UK show that similar behaviour occurs across invertebrates.

In snails, which are hermaphrodites, amorous advances involve “traumatic secretion transfer”, blasting potential mates at close range with “love darts” covered in psychoactive mucus. Understandably, neither party is keen to play the female role, involving being shot. In sea slugs this results in “penis fencing” – each attempting to penis-stab the other. An inflicted wound inoculates the recipient with sperm.

A brown garden snail (Cantareus aspersus) impales its mate with a “love dart”. Image:Ronald Chase/Proceedings B

Why would a male want to impale the mother of his future children? In a paper in Annual Review of Entomology, Nik Tatarnic and colleagues from Sydney in Australia and Sheffield in the UK focus on arthropods. They explain that stabbing is, in evolutionary terms, a game-changing tactic for males.

To sire offspring obviously requires mating, but this is only a prelude. Much more crucial is fertilisation, and females understandably want to control when, where and by whom their eggs are fertilised.

In many cases females are highly successful at this – by, for example, using their reproductive tract as a powerful tool to screen out all but preferred males. Females often simply eject unattractive males’ sperm, or filter it out chemically, and sometimes can close their tract entirely. Female control is especially widespread in insects, where females store sperm in a sac – sometimes for years, opening it to fertilise eggs at their leisure.

 

The dragonfly penis is shaped like a spade for removing rivals’ sperm. Image: Jonathan Waage/Science

On the other hand, each male mating with a female would prefer his own sperm to fertilise the offspring. To achieve this, he must both overcome the female’s defences and beat her other mates – two neverending “arms races”.

Males can beat rivals to the first step – that is, mating – by impressing females through courtship. This may also win favour at the fertilisation phase. But males are more sneaky than that, with outlandish adaptations to ensure their sperm win the race, like plugging females up, or scooping out rival sperm. Our own human organ may indeed have a dual function as a “sperm scoop”.

 

Wood mouse sperm form a snake by hooking on to each other. Image: Harry Moore/ABC

Another solution is to try and directly overcome challenges posed by the females’ reproductive tract. Fruit fly males spike their sperm, drugging females into releasing more eggs, even though this shortens females’ lives. Wood mice females produce mucus that only strong-swimming sperm can cross. Ever resourceful, males’ sperm team up into long “snakes” that, together, altruistically push one lucky sperm through the mucus to success.

Stabbing for the win

 

Syringe-like bedbug paramere (penis), adapted for stabbing females. Image: Cassandra Willyard/lastwordonnothing.com

Penis-stabbing, though, shifts the goalposts entirely. By injecting sperm directly into females’ body fluid, male bedbugs bypass the female’s adaptations to control access to her eggs. The female is injured in the process, reducing her number of offspring. But in the cold language of statistics, this may be worth it for the male – a healthy female is no good if she doesn’t bear his offspring. Males can both prevent females from excluding their sperm and also from preferring other males.

 

The nightmarish embolus (penis-like organ) of a male Harpactea sadistica spider. Image: Milan Rezac/Science Blogs
 

This has been such a successful strategy for males that it has evolved repeatedly across the animal kingdom. Male Myzostoma worms secrete corrosive enzymes from their penis, dissolving a hole in the female’s skin into which they ejaculate. Male giant squid inject sperm packets into females’ arms – although occasionally they end up inseminating themselves, literally shooting themselves in the foot. In Harpactea sadisticaspiders, the male bites the female, then stabs her with needle-like genitals, ejaculating into the wound.

In some groups, like “bat bugs”, males spear females at random. In many others, though, females have evolved damage-limiting adaptations such as the bedbug “spermalege” (the organ discovered by Ribaga), offering an easy entry point to discourage indiscriminate stabbing. Some species have entire “paragenital systems” guiding sperm to their ovaries, while the regular reproductive apparatus shrivels from disuse.

 

Polistes wasp infected with a female Xenos twisted-wing parasite. Her brood canal pokes out for prospective mates, who, mysteriously, often ignore it and stab her instead. Image: Macro Photography/Aculeata Research

Males will often jump on and penis-stab anything that comes their way, even females of other species, often killing them in the process – a phenomenon that has driven some species to evolve apart. Male bedbugs regularly jump other males by mistake – which is such a problem that males in one species have evolved their own damage-control spermaleges.

In an arms race, though, neither side can win – each can only gain a temporary advantage – and, as expected, females are fighting back. Astonishingly, some female bedbugs have evolved modified spermaleges that mimic those of males, to reduce harassment. Others have evolved ways of digesting the injected sperm and using it to repair their wounds, minimising the damage.

The course of true love never did run smooth. For males and females locked in an arms race, though, it could be said to run in circles – vicious ones at that. And all to inject a little bit of romance.

Even among ants, size matters more than shape

(An article I originally wrote for The Conversation with some beautiful photos by Alex Wild (www.alexanderwild.com). Read the original article).

Myrmecocystus workers: living larders. Alex Wild (www.alexanderwild.com)

Worker ants are a funny old bunch, of many shapes and sizes. But they tend to get bigger and smaller much more often than evolving entirely new shapes, according to a new study.

While most animals juggle survival with having babies, a worker ant is not constrained by also having to be a functioning mum. She can safely leave that job to the queen ant, because the queen produces the worker’s siblings, who all share her genes and thus pass on her DNA.

Although specially adapted for a life of labour, worker ants nevertheless still come in many different forms. Not constrained by the need to produce offspring, and given the many tasks workers perform, one might imagine this could lead to the evolution of some extremely strangely shaped insects.

At a cursory glance, this seems to be true in spades. Take, for instance, the turtle ant Cephalotes that nests in tree cavities. It has a dedicated caste of soldiers who are supposed to block entrances, and this they achieve by using heads that have evolved to look like manhole covers.

Cephalotes workers: heads shaped like manhole covers. Alex Wild (www.alexanderwild.com)

Or consider the honeypot ants (shown in the lead photograph), Myrmecocystus, who have abdomens that are giant distended living vats of honey.

There are also Camponotus workers that “explode” on contact with enemies, showering them with glue from a massively overdeveloped gland in their head.

Camponotus worker explodes in an enemy’s face. Mark Moffett (www.doctorbugs.com) / Minden Pictures / FLPA

These remarkable examples, however, might just be exceptions. Most worker ants have more mundane-looking features that set them apart, mostly mere variation in size. It is rare for ants to have more than one specialised kind of worker. Even the most complex societies of ants, like leafcutter ants, have at most three truly distinct kinds of workers, and these tend to vary only in size.

This discrepancy intrigued Marcio Pie and Marcel Tschá, from the Federal University of Paraná ‎in Brazil, who have just published a study in PeerJ to find out if size actually varies more than shape. To do this, they took thousands of measurements from technical photographs of worker ants on AntBase, a repository of ant pictures and data.

And indeed it seems, at least among the workers of some 100 ant species they measured, that size was actually much more variable than shape (“shape” being measurements that don’t simply all vary in concert with each other across species).

This fact makes evolution in worker ants less special than we might expect – because variation in size is also how many other groups of animals vary most in their evolutionary history. Despite the many weird and wonderful forms of ants we know exist, it seems worker ants are no different from the rest of us when it comes to how morphology evolves.

In many cases workers of different species differ mainly in size, not shape. Here an Argentine ant (Linepithema, left) attacks a fire ant (Solenopsis). Alex Wild (www.alexanderwild.com)

So why does size vary so much? One theory is that size represents a “genetic line of least resistance” – ie size seems to be easy to evolve.

In the multilayered webs of interacting genes making up something as complex as an ant, not all genetic combinations exist. Some are more frequent than others. In wild populations, patterns of genetic variation are not random, but fall along well-defined axes that act as channels guiding the way the physical form can evolve. Typically, the most important is a “bigger-smaller” axis. Also, hormones control growth, and can act on many body parts at once. Genetic mutations that change hormone levels can result in big changes in size.

In a slightly more complex twist, some features grow disproportionately as animals get bigger. Just as in Alice in Wonderland, as ants become really small, tiny objects like sand grains become enormous. Under these conditions, long legs for running become less important and stubby legs are an advantage. Thus, legs are proportionally shorter in smaller ants.

And why is it that ant shapes vary so little? One theory holds that what workers lack in specialised forms, they make up for in flexible behaviour, which allows workers to respond to unpredictable environments. Ants are able to reallocate whole sections of the workforce at a moment’s notice when the need arises. For example, African driver ants (Dorylus) form living bridges when on the move, red ants (Myrmica) become undertakers and fire ants (Solenopsis) form living waterproof rafts to see the whole colony through a flood.

Fire ants form living rafts

Another possibility hinges on the fact that ant workers are still technically capable of having offspring, and occasionally try to do so (although their offspring are all male, and are often eaten by other workers). This may mean their forms are still constrained by the need to reproduce, however meagre a brood they end up producing.

Nevertheless, in some cases, specialised ecology has selected for specialised workers. And, in keeping with this, Pie and Tschá did find a few cases of rapid shape evolution in isolated lineages, for example in fungus-farming ants (like leafcutter ants).

Leafcutter ants, Atta cephalotes. Alex Wild (www.alexanderwild.com)

Shape evolution had also accelerated in another group containing weirdos such as Calyptomyrmex, some of whose members have mysterious spatula-shaped hairs covering their bodies – nobody knows what for.

Calyptomyrmex: covered in mysterious oddly shaped hairs. Alex Wild (www.alexanderwild.com)

The obvious next question is – does slow shape evolution go hand in hand with flexible, jack-of-all-trades workers like fire ants? Conversely, do we see the fastest shape evolution in lineages where different kinds of workers have specialised, inflexible jobs, like turtle ants? Perhaps studying some more ant pictures might answer those questions.