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Male Frog Extracts and Fertilises Eggs From Dead Female

For a small Amazonian frog called Rhinella proboscidea, death is no impediment to sex. The males form huge mating balls in which dozens of individuals compete to fertilise a female. These competitions are so intense, and the combined males so heavy, that the poor female sometimes drowns in the struggle.

But for the males, that’s not a deal-breaker. Thiago Izzo from Brazil’s National Institute of Amazonian Research has found that the males can force the eggs from the bodies of the deceased female, and fertilise them. It’s a unique strategy and one that effectively involves sexual reproduction with a dead partner. Izzo calls “functional necrophilia”.

R.proboscidea is a small frog that looks like a dead leaf, right down to its pointed snout, its brown colour and the central white ‘vein’ running down its back. But its camouflage breaks down when it’s time to mate. Hundreds of males gather at breeding sites for just two to three days and when any female shows up, there’s intense competition for her attention. This strategy is called “explosive breeding” and it’s as violent as it sounds. Males wrestle for mating rights, and will try to displace any rivals that have actually found a female. The result is a large mating ball with a female at its bottom. She often drowns.

In the deadpan style of academics, Izzo writes that “such occurrences are obviously detrimental to females”. You don’t say.

He has seen the aftermath of the carnage first-hand, having found several explosive breeding sites in Brazil’s Adolfo Ducke Forest Reserve between 2001 and 2005. The first time, he found around 100 males and 20 dead females. The second time: 50 males and 5 dead females. But when Izzo dissected the females, he couldn’t find any eggs inside them. Where had they gone?

Izzo found the answer when he saw a male grasping the body of a dead female and rhythmically squeezing the sides of her belly. Out popped her eggs, like beads on a jelly-coated string.

The male on top squeezes eggs out of the dead female below. From Izzo et al, 2013. Journal of Natural History
The male on top squeezes eggs out of the dead female below. From Izzo et al, 2013. Journal of Natural History

Izzo saw the same behaviour again and again. On one occasion, the male pushed his dead partner around the pond, “apparently to avoid other males”. The eggs that emerge are quickly fertilised—Izzo kept an eye on them and saw that they eventually developed into embryos.

There have been many other cases of animals having sex with the dead, including several frogs and an ameiva lizard that tried to mate with a road-killed female. On Scott’s Antarctic expedition of 1910-1913, George Murray Levick saw a male Adelie penguin trying to have sex with a dead female, an act of “astonishing depravity” that he removed from his paper on the penguin’s behaviour.

And of course, there’s the now legendary case of homosexual necrophilia between two mallards—one living and one dead by window. That incident led to an IgNobel award for its discoverer, the inauguration of Dead Duck Day, and an academic paper with the keywords: “homosexuality, necrophilia, non-consensual copulation, mallard”.

All of these incidents were regarded as mistakes, but the behaviour of R.proboscidea is anything but. Izzo expects that other explosive breeders—and there are many frogs that do this—might also rely on functional necrophilia.

This behaviour clearly benefits the male. He doesn’t waste the huge amount of energy that he just spent on wrestling with other suitors. It would be a wasted effort, in any case—R.proboscidea males outnumber the females by ten to one, so the odds of finding and mating with another partner are pretty low. But he doesn’t have to. He can still foster a new generation of frogs.

There might even be some benefits for the female. She too gets a post-mortem chance of passing her genes to future frogs despite the unfortunate side effect of, er, being drowned by a ball of violent males. Silver lining!

Reference: Izzo, Rodrigues, Menin, Lima & Magnusson. 2013. Functional necrophilia: a profitable anuran reproductive strategy? Journal of Natural History http://dx.doi.org/10.1080/00222933.2012.724720

Hat tip to Olivia Solon for alerting me to this story

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How the rhino beetle got its horn (and why it cannot lie)

The male Japanese rhino beetle wields a huge forked horn on his head. It looks like a jousting weapon, and the male uses it to pry and flip other males off a branch. But it’s also a billboard, a prominent and completely honest advertisement for the male’s quality.

The horns are extremely variable. Small males have pathetic nubbins on their heads, while big ones have unfeasibly large prongs that can grow to two-thirds of their body length. Doug Emlen from the University of Montana has found that the growth of the horns is intimately tied into molecules that reflect how well-nourished the beetles are. Not only that, but the horn is more sensitive to these molecules than any other body part. Well-fed beetles may have larger wings and bodies than poorly-fed ones, but they have much larger horns.

This ornament can’t be faked. It is impossible for a weak beetle to feign rude health by growing a larger horn, so females can rely on the size of the horns to judge a potential partner’s health. And with a body part that conspicuous, they don’t have to look very hard.

The growth of the horns depends on insulin and related molecules called insulin-like growth factors (IGFs). Most people know insulin as the substance that some diabetics have to take, but it and the IGFs are also major players in animal development. Their levels change depending on nutrition, stress and infections, and they control how fast different tissues can grow. They fine-tune the size of an animals’ body so that it’s appropriately sized for the environmental challenges it will face. If there’s plenty of food around, a bigger body will do well, and insulin and IGFs ensure that one is produced.

If every body part was equally responsive to insulin and IGFs, then every bit of an animal would grow at the same size. A big individual would just be a scaled-up version of a small one. But this doesn’t always happen. Some body parts ignore the signals and are much the same size in every individual – the genitals of many insects are a good example. Others, like the rhino beetle’s borns, are hypersensitive and grow huge, out of all proportion to the rest of their bearer’s anatomy.

Emlen studied the beetles’ horns by interfering with their insulin receptors, the molecules that insulin docks with. Without these receptors, insulin becomes a messages without a listener – it has no influence. Emlen silenced the receptors when the beetles were finishing up their larval careers, and ready to transform into adults. At this point, their body size is roughly set, but their adult body parts, like horns, wings and genitals, were still getting bigger.

The loss of insulin signals didn’t affect the beetles’ genitals – they were the same size as those of normal insects. It did, however, make their wings around 2 percent smaller. And it made their horns a whopping 16 percent smaller. This means that the horns are 8 times more sensitive to insulin than wings (which are representative of most other body parts).

Insulin and IGF help to set the size of many other exaggerated animal ornaments, including the antlers of red and fallow deer, the horns of dung beetles, and the giant claws of some crustaceans. You can understand why. These hormones have been coupling the growth of animals to environmental conditions for half a billion years. They form a widespread system, and an easy one to tweak. If a body part becomes subtly more sensitive to these signals, then – Bam! – it’s free to outpace the rest of the body in size.

Here’s the important thing: a change like that would necessarily produce body parts that honestly indicate their owner’s quality. Weak, starving individuals can’t produce big ornaments, because the size of those ornaments is tied to their insulin levels and their insulin levels are tied to their nutritional state. They can’t fake their way to showiness.

This is a subtly different explanation to the one that’s often put forward to explain the evolution of flashy animal ornaments – the handicap principle. It states that low-quality individuals can’t bear the cost of, say, a long tail or a magnificent set of antlers. They would be too conspicuous or heavy. They need strength and health to pull off. Cheats couldn’t bear the burden.

You can understand how the handicap principle would work for a signal that’s already exaggerated, but obviously, those signals didn’t start off that way. They would have had much humbler and smaller origins, when the costs of bearing them would have been low. So, at this early stage of evolution, why didn’t weak individuals cheat by producing larger ornaments?

Emlen’s rhino beetles provide an answer. The signals can’t be faked not because they’re a drain, but because they’re intimately tied into an individual’s physical condition. It’s not that cheaters can’t carry the burden of big ornaments. It’s that cheaters can’t exist.

Reference: Emlen, Warren, Johns, Dworkin & Lavine. 2012. A Mechanism of Extreme Growth and Reliable Signaling in Sexually Selected Ornaments and Weapons. Science http://dx.doi.org/10.1126/science.1224286

More on extreme body parts:

From 250 million years of repression, a wonderland of hats

Giant squid, what big eyes you have. All the better to spot sperm whales with, my dear.

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The rubbish sperm of the naked mole rat

The naked mole rat must be one of the strangest mammals in existence. They live in underground colonies like those of ants and bees, with a fertile queen lording over sterile workers. They feel no pain in their skin, they live unusually long lives, they can cope with chokingly low levels of oxygen, and they seem to be immune to cancer. Their sight is poor, they can’t control their body temperature very well, and their teeth jut out beyond their lips. And they look like wrinkled sausages.

Now, just when you thought they couldn’t get any weirder, we can add another bizarre trait to the naked mole rat’s extensive list: they have really rubbish sperm.


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Hummingbirds dive to sing with their tails

Many birds sing to woo females, but some hummingbirds go to great lengths to do so. They climb to between 5 and 40 metres before plummeting past perched females in death-defying dives. They pull up at the last minute, spread their tail feathers and produce a loud chirpy song. The song comes not from the birds’ mouths, but from their tails. The splayed tail feathers vibrate as air rushes past them, causing them to flutter.

Flutter sounds colloquial and innocuous, but it can be deadly. It’s what happens when air, moving at just the right speed, zooms past objects with just the right stiffness, setting up large and potentially disastrous vibrations. Flutter brought down the passenger plane Braniff Airways Flight 542, killing everyone on board. Flutter wrecked the Tahoma Narrows Bridge, causing it to warp and twist like a piece of rope. But flutter also ensures that male hummingbirds get some action.


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Hermaphrodite insects fertilise daughters with parasitic sperm

The life of the cottony cushion scale insect reads like something from the most ridiculous of tabloid newspapers. Dad leaves parasitic body parts in his own daughter, which produce sperm that fertilise her eggs. He is both father and grandfather to his own grandchildren.

On top of that, these insects are mostly hermaphrodites. With the exception of the odd pure male, almost every individual is both male and female. They reproduce by having sex with themselves, fertilising their own eggs with their own sperm. And this means that scale insects can be father, mother, grandfather and grandmother to all of their grandchildren. Good luck drawing that family tree.

Scale insects are small animals that suck on plant sap for a living. Encased in bizarre waxy shells, most people wouldn’t even recognise them as insects – the cottony cushion scale, for example, looks like a dollop of shaving foam. It and two of its close relatives are the only known hermaphrodites out of several millions of insect species.

In most hermaphroditic animals, an individual grows up and develops the organs that make both sperm and eggs. But that’s not the case for the cottony cushion scale. When it mates with itself, it fertilises its own egg with its own sperm. Then, after the point of conception, yet more sperm invades the embryo. This “infectious tissue” creates sperm-producing organs inside the daughter* and the resulting sperm eventually fertilises the daughter’s eggs. (A note on terminology: obviously, each insect is hermaphrodite but they’re referred to as “daughters” because they have the body of a female. The rare pure males look very different.)


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Why sons inherit their mother’s curse

No expecting mother would ever wish harm to befall her children. Unfortunately, she may have no choice in the matter. Due to the rules of genetics, mums always run the risk of passing a “mother’s curse” onto their sons, but not their daughters.

The curse is an ancient one, the result of events that happened billions of years ago. At a time when all life consisted of single microscopic cells, one of these swallowed another. Normally, the engulfed cell would be digested, but not this time – this time, the two cells formed an alliance. The swallowed cell transferred many of its genes to its host, keeping only those involved in providing energy. It evolved into a mitochondrion – a tiny, efficient battery that would power its host, giving it the energy to become more complex. This alliance is the foundation of all complex life on the planet. All animals, plants, fungi and algae run on mitochondria power.

This means that all animals really have two genomes – their main nuclear one, and a far smaller secondary one in their mitochondria. The two sets of genes work together, each controlling the activity of the other. But they are inherited differently. The nuclear genome is a mash-up of genes from both parents, but the mitochondrial one only comes from mum. And this asymmetry is the reason for the mother’s curse.


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Male water striders summon predators to blackmail females into having sex


If you want to see some sex, violence and blackmail, don’t bother with soap operas – try looking at the surface of your local lake or stream. There, you’ll find small insects called water striders (or pond skaters), skimming across the water on outstretched legs. These legs can pick up the vibrations of prey, predators and mates, but they can also produce vibrations by tapping the water surface. And males use this ability to blackmail their way into sex. It’s a drama of sexual tension played out across the surface tension.

Water strider sex begins unceremoniously: the male mounts the female without any courtship rituals or foreplay. She may resist but if she does, he starts to actively strum the water surface with his legs. Each vibration risks attracting the attention of a hungry predator, like a fish or backswimmer (above). And because the female is underneath, she will bear the brunt of any assault. By creating dangerous vibes, the male intimidates the female into submitting to his advances. Faint heart, it is said, never did win fair lady.


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Pocket Science – T.rex the nose-loving tyrant leech king, why losers ejaculate more, and how cuttlefish could “see” with their skin

Not Exactly Pocket Science is a set of shorter write-ups on new stories with, where possible, links to more detailed takes elsewhere. It is meant to complement the usual fare of detailed pieces that are typical for this blog.

Tyrant leech king – a new T.rex found in the nose of a Peruvian girl

Tyrant_leech_kingThree years ago, a nine-year-old girl was admitted to La Merced hospital in Peru with a headache that had lasted for two weeks and a strange “sliding sensation” in her nose. Her parents quickly discovered the source of the problem – a sizeable black worm lodged up her right nostril. They quickly sought medical help and it came in the form of Dr Renzo Arauco-Brown, who “with some effort” removed a seven-centimetre leech from the girl’s nose. Brown sent the animal to leech guru Mark Siddall from the American Museum of Natural History, who immediately recognised it as a new species. Uniquely among leeches, the bloodsucker had a single jaw (most have three) but it was lined with eight enormous sharp teeth. For this reason, the Siddall gave it the fanciful name of Tyrannobdella rex, or “tyrant leech king”. A new T.rex had arrived.

It turns out that T.rex has a history of feeding on humans. After describing the new species, Siddall found two other specimens. Both had been removed from the nostrils of young boys in 1997. Like the most recent case, these children had also been bathing in local lakes and streams, which is almost certainly how they picked up their tyrant vampire.

While most leeches are found on the skin, Tyrannobdella is a member of the praobdellid group, which have a disturbing propensity for entering human orifices. They have specialised at feeding on mucous membranes, such as those found in the nose, eye, vagina, anus and urethra (don’t click on these links if you’re squeamish). These bloodsuckers can stay inside for days or weeks on end. They lead to a condition called “orificial hirudiniasis” and they could be potentially life-threatening, especially if secondary infections kick in. It’s likely that many more members of this group are awaiting discovery, although finding them may be a tricky business. As Siddall slyly writes, “Our standard methods of attracting leeches to our exposed selves may prove awkward given their established propensity for particular anatomical feeding sites.”

Reference: PLoS ONE http://dx.doi.org/10.1371/journal.pone.0010057

Why losers ejaculate more

Flour_beetleNot every male is a fighter and, as a result, many don’t become lovers either. But for these losers, there’s another option for passing on their genes to the next generation – make sure that you ejaculate copiously when you get the chance.

The male flour beetle has to battle other males over the right to mate with a female. Kensuke Okada from Okayama University found that males who lose these fights become less aggressive and avoid fighting again. However, they make up for avoiding combat by doubling the amount of sperm they produce when they ejaculate. This extra investment is a temporary one; after five days, things were back to normal.

These results show that males can fine-tune their sexual strategies according to the competition they face. Males who triumphed in combat didn’t feel the need to produce more sperm. They are strong enough to guard females they mate with and can stop other males from displacing his sperm with their own. Losers have to move about into new territories and when they do get to mate, they run the risk that a stronger male will just flush their sperm out with his own afterwards. For those who lose physical fights, contributing to the next generation means winning the sperm wars, and doing that means producing more sperm.

Reference: Biology Letters http://dx.doi.org/10.1098/rsbl.2010.0225

More on sperm competition: sperm wars of ants and bees, glowing sperm races, spiky penises, traumatic insemination and frigid echidnas

Could cuttlefish “see” with their skin?

CuttlefishCuttlefish and their cephalopod relatives, squid and octopuses, are capable of nature’s most spectacular acts of camouflage. They can change the colour of their skin on a whim, send moving waves of stripes down their body, and send messages to one another in shifting hues. This ability is even more incredible when you consider that, according to all evidence to date, cuttlefish are colour-blind. If they can’t actually see colour, how can they mimic it so accurately?

Now, cephalopod specialists Lydia Mäthger and Roger Hanlon have made an intriguing discovery that could potentially answer this question. They found that a gene called opsin is active all over a cuttlefish’s skin; opsin proteins are sensitive to light and an essential part of the visual system. It’s possible that these animals can sense light using their entire skin, and that their colour-changing skill is based on this distributed “sight”.

The idea isn’t without precedent. Some squid have organs on their skin that double as an extra pair of “eyes”. But so far, Mäthger and Hanlon’s idea is still a hypothesis. The skin opsins may have no significance at all and the duo has some work ahead to them to show that they actually play an important role. For a start, there’s some evidence that opsin-like genes are active in the skin of humans, and we certainly can’t change colour without a significant amount of make-up. And the opsins in a cuttlefish’s fin, underside and retina are all the same, so it’s unlikely that they could discriminate between different colours.

However, Mäthger and Hanlon suggest that the opsins may be useful in matching brightness and contrast. They could also interact with chromatophores – the tiny, expandable sacs of pigment that underlie a cuttlefish’s colour-changing ability. Chromatophores come in different colours and they could act as filters for the opsins. Light passing through these sacs could provide information on different wavelengths of light coming in from the environment.

Reference: Biology Letters http://dx.doi.org/10.1098/rsbl.2010.0223

More on cephalopods: the squid with living, seeing flashlights, coconut-armoured octopuses, the mimic octopus, clever cuttlefish, and the secret signals of squid

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Pocket science – sperm races and poison-stealing voles

Not Exactly Pocket Science is a set of shorter write-ups on new stories with, where possible, links to more detailed takes elsewhere. It is meant to complement the usual fare of detailed pieces that are typical for this blog.

Live broadcasts of sperm races

Last week, I blogged about the sperm wars of ants and bees. Even after males have mated with a queen, their semen contains chemicals that have evolved to incapacitate the sperm of their rivals. But there’s more than one way of winning the sperm wars. Some insects do it through sheer numbers.

Mollie Manier managed to set up live broadcasts of the sperm wars. She engineered male flies whose sperm was loaded with proteins that glow either red or green. By following these glows with a special microscope, Manier captured astounding and beautiful videos of the sperm racing around the female’s genital tract at high speed, like miniature formula-one cars.

When fruit flies mate, the female stores the male’s sperm in a special pouch. Because of this, the last male to mate with her gets an advantage because his sperm can flush out those of earlier suitors. To facilitate this, males ejaculate far more sperm than is actually necessary to fill the female’s stores. That gives them the best chance of ousting as many rival cells as possible. But unlike the battles of ants and bees, the sperm of fruit flies don’t actually harm those of rivals. Once the number of racers has been set, it’s a fair fight.

Reference: Science http://dx.doi.org/10.1126/science.1187096

More from Jef Akst at The Scientist

Poisonous fungi unwittingly betray plants to voles

Meet the Southern vole – it looks unassuming but this little critter might just have a penchant for stealing biological weapons. As the vole eats grass, it sometimes gets mouthfuls of a fungus called Neotyphodium, which lives inside the stems. The fungus produces chemicals that poison plant-eaters trying to munch its home. Related species, like the field vole, lose weight and die earlier when they eat these poisons, but Susanna Saari found that the Southern voles seem to be immune. When they eat infected ryegrass, they’re perfectly healthy and neither their body weight nor their numbers fall.

If anything, they actually seem to benefit from the poisons, becoming less likely to fall prey to their greatest enemy, the least weasel. The reason for this protection is still unclear. Many animals steal biological weapons: the sea slug Glaucus protects itself with stinging cells taken from the jellyfish it eats; the tiger keelback snake eat toads to steal their poison; the hooded pitohui nicks poisons from beetles. But Saari thinks that the voles are different. Lleast weasels, which hunt by smell, couldn’t distinguish between the urine of voles that had fed on infected or uninfected grass. When the voles faced a weasel, those that were full of fungi were actually less active but despite this tendency to freeze, they were less likely to be captured by weasels. Perhaps by freezing in the face of danger rather than fleeing, they somehow protected themselves.

Meanwhile, the discovery could recast the relationship between the fungus and the grass. Neotyphodium infects 20-30% of all grass species and the two are typically viewed as accomplices, whose interests are aligned. The fungus doesn’t harm the health of the grass, and its toxins deter grazers. But if the fungus’s poisons are actually a boon to some grass-eaters, its presence might actually harm the grass by drawing hungry voles. In that case, the fungus would be less a beneficial tenant than a resident parasite.

Reference: PLoS ONE http://dx.doi.org/10.1371/journal.pone.0009845

And finally…

The biggest story of the last week was undoubtedly the tale of X-Woman’s Fingerbone. Unfortunately, the timing of the story coincided with the move to Discover and other things, which meant no time to cover the story in the depth that it clearly required. But that’s no big loss – there’ s little chance that anyone could have produced coverage as thorough and lucid as my co-blogger(!) Carl Zimmer. Go read his take.


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Sperm war – the sperm of ants and bees do battle inside the queens

One night of passion and you’re filled with a lifetime full of sperm with no need to ever mate again. As sex lives go, it doesn’t sound very appealing, but it’s what many ants, bees, wasps and termites experience. The queens of these social insects mate in a single “nuptial flight” that lasts for a few hours or days. They store the sperm from their suitors and use it to slowly fertilise their eggs over the rest of their lives. Males have this one and only shot at joining the Mile High Club and they compete fiercely for their chance to inseminate the queen. But even for the victors, the war isn’t over. Inside the queen’s body, their sperm continue the battle.

If the queen mates with several males during her maiden flight, the sperm of each individual find themselves swimming among competitors, and that can’t be tolerated. Susanne den Boer from the University of Copenhagen has found that these insects have evolved seminal fluids that can incapacitate the sperm of rivals while leaving their own guys unharmed. And in some species, like leafcutter ants, the queen steps into the fray herself, secreting chemicals that pacify the warring sperm and ease their competition.

The amazing thing about this chemical warfare is that it has evolved independently several times. Social insects evolved from ancestors that observed strictly monogamous relationships. Even now, the queens from many species mate with just one male during their entire lives. With just one set of sperm in their bodies, they have no problem with sperm conflict. The trouble starts when species start mating with several males during their nuptial flights, as honeybees, social wasps, leafcutter ants, army ants, and others do today.