On the Origin of Orifices: Ears

Ears aren’t the most beautiful part of the human body. Even if you’re lucky enough not to have a pair that stick out at 90 degrees or spontaneously sprout tufts of hair, many people still feel that the only way to improve their appearance is to punch holes in them and add shiny bits of metal. 

Still, those flappy bits of cartilage should not write off the amazing structures that are hidden inside our skulls. The mammalian ear is very sophisticated:  sound collected by the outer ear is channelled into the middle ear, where it is amplified by the ear drums. The sound then passes via a group of small bones into the fluid-filled cochlea of the inner ear, which is lined with sensitive hair cells. When these are disturbed by sound waves, they move and fire nerves at their bases, sending off information to be processed by the brain. Other structures in the inner ear also help us with balance (though they still haven’t evolved to cope with fairground rides and student drinking games).

But this complexity has not always been there. How did we end up with holes in the sides of our heads, anyway? And where did all those complicated bits inside come from? Well, listen carefully. Or read carefully. Eyes are probably the more useful organ for understanding this post: let your ears relax for a bit and put on some pretty music. That’s right.

You might notice that you can’t point out the ears on a fish: the inner ear is the only part of the trio found in most modern fishes- reflecting the situation in early vertebrates.

'I never wanted your stoopid ears anyway.'

 Sound travels well in water, but as fish have a similar density to water, their entire bodies and their surroundings are equally affected by sound waves, making them very difficult to detect. Tiny hair cells like those in our cochlea are found down either side of fishy bodies and within the inner ear, and first appeared at least 440 million years ago. However, without altering the relative speed of sound waves, these hairs would not have been any good for sound detection. Modern fishes have got around this using a collection of very dense otolith bones in their inner ears. Sound waves move these bones more slowly than the rest of the fish’s body, causing the inner ear’s sensory hairs to distort and fire their nerves. Some species can improve their sensitivity further by connecting their ears to their swim bladders, which are filled with gas and thus slow down the sound waves that pass through them, allowing detection.

Now, you might remember from a few posts ago that early vertebrates started doing interesting things with the structure of their gills. The first pair of gill bars changed to form the jaw, and the second became the jaw-supporting hyomandibular bone; but such a major alteration in the gills’ internal anatomy was bound to affect its other features, too.  And it did: the first pair of gill openings that once served to flush used water out into the environment became squashed and shrunken, going from large, muscular flaps to a small, pretty useless hole leading into the mouth on either side of the head, called the spiracle. Useless yet harmless structures like this tend to have one of two fates in evolution. They either slowly disappear over evolutionary time- like a hamster’s tail- or undergo chance modifications that make them worth keeping around after all. We might never have known the spiracle had ever existed if it hadn’t been recruited for a new role in our ancestors!

Some fish probably started using the spiracle as a novel way of sucking in water to breathe, as an alternative to the mouth when at rest. Modern sharks have developed a similar “breathing hole” that they use when chilling on the sea floor, to avoid sucking gravel into their delicate gill system (ouch). Fossilised fishy ancestors of the first tetrapods (all four-limbed vertebrates, from frogs to humans to whales) show an enlarged spiracle for this purpose, allowed by the shrinkage of the hyomandibular bone. This bone later went on to shrink even more, becoming the stapes (or “stirrup”) of the middle ear in tetrapods. Here, it took on the function of relaying vibrations from the (also new) eardrum to the liquidy depths of the middle ear, making them louder in the process. This new structure was necessary when our ancestors came onto land, and found themselves deaf: sound has a harder time travelling through air, and the weedy little vibrations on land just weren’t enough to be picked up by their inner ears without amplification. So the spiracle switched roles once again, and became a sound-window to the outside world.

I propose an underwater kingdom for the elderly!

This bony amplification system has been honed even further in the mammals, and again, its evolution was tightly linked to that of the jaw. Reptiles and amphibians have multiple bones joined together to make up their lower jaws: the dentary, the quadrate and the articular. But this is rather like making a scissor blade out of three separate pieces glued together instead of a single block of metal: it’s never going to be quite as strong. In search of a more powerful bite, the ancestors of mammals evolved a larger dentary bone, which eventually became the sole bone of the lower jaw. Reduced in size and now a little bit useless, the quadrate and articular could easily have disappeared altogether- but like the spiracle, they were saved by recruitment into the ear system, where they teamed up with the stirrup bone. The transition can be seen in fossils of the lineage that led to mammals: at some stages, the quadrate bone appears to have had a dual function, remaining as part of the jaw whilst transmitting vibrations to the inner ear. In their present form, we generally know the articular and quadrate bones as the anvil and the hammer due to their shapes- slightly catchier titles, really. They may seem to have been demoted a little, having gone from being some fairly significant chunks of bone to being the smallest in the (human) body. However, they play an important role in broadening the range of pitches that mammals can detect- allowing whales and bats to use sonar, and humans to appreciate opera and car alarms. Not a bad new job, really. 

So learn to love your ears, because scientists certainly do! The evolution of many aspects of hearing has been mercifully easy to study compared to the other senses, simply because so many bones are involved- and bones are much more likely to turn up in the fossil record than, say, eyeballs. Given that the jaw and the ear are so closely linked, it shouldn't be too difficult to come up with a clever bit of backchat to anyone who admonishes you for using your mouth more than your ears, but I'll let you figure that one out. That’s enough ears for now: in the next Origin of Orifices, we’re taking a trip to the other end of the digestive system. No giggling!

Image credits: Clownfish- http://www.flickr.com/photos/tambako/4188752328/
Old lady: http://www.flickr.com/photos/louisa_catlover/5581012353/

Double lives: the evolution of insect metamorphosis

I found these the other day. Cute or what?!

True, most people prefer the adult version- particularly if turns out to be a butterfly. Caterpillars almost seem like different species when they grow up- their bodies change beyond recognition, as do their lifestyles. This type of life cycle is called holometabolism, in which a soft-bodied eating-machine of a larva forms a pupa at the end of its growth. Here, it undergoes a staggering transformation to become an adult: a change commonly known as metamorphosis. All “Very Hungry Caterpillar” so far. But butterflies and moths shouldn’t get all the limelight. In fact, the larvae in my photo above aren’t caterpillars at all: they’re young Hazel Sawflies, relatives of bees, wasps and ants. About 80% of all insect species are thought to adopt this life cycle, including the aforementioned bees and their relatives, beetles, and flies.

Most of the remaining insect species have a much OLDER method of growing up: the young insects basically resemble small versions of their parents, with hard exoskeletons and, frequently, similar lifestyles to the adult. These youngsters are often known as “nymphs”. Like holometabolous insects, they shed their skins as they grow, separating their youth into multiple “instars”. When they moult out of their skins for the final time, they emerge as adults: the only major features gained in this final transformation are wings and functional genitalia. Grasshoppers, true bugs and dragonflies are good examples of this fast-track hemimetabolous lifestyle.

I've spent a lot of time cooing over insects in my last few posts. N'AWWW!

For a long time, it was assumed that the larvae of holometabolous insects were equivalent to hemimetabolous nymphs, and had simply become highly specialised over evolutionary time. Genetics tell us that all holometabolous insects had a common ancestor: i.e. this lifestyle has only evolved from hemimetabolism ONCE. But how and why they evolved so many differences- the soft body, the complicated pupal stage- was a bit of a mystery. It’s hard to imagine a fully-formed nymph, just a few simple developmental steps away from being a functional adult, being selected to gradually become more and more like a soft sack of guts. Eventually, the differences between baby and adult would be so great that only liquidising the larva in a stationary, vulnerable pupa could produce the necessary change to its body: it just makes growing up complicated! And how did they insert this new life-stage into their development from nowhere?

Then, in 1999, Truman and Riddiford cracked the metamorphosis puzzle. They noticed that in hemimetabolous insects, there was actually ANOTHER, very short, developmental stage in between the embryo in the egg and the nymph! Before moulting into a true nymph, this “pronymph” has a soft body, no wing buds, unusual bodily proportions and an underdeveloped sensory system: features also seen in holometabolous larvae. Is this, in fact, the stage that gave rise to caterpillars and maggots? But the pronymph cannot feed, as its mouthparts are also soft: what pressures could possibly have led to the extension of this brief, rather vulnerable phase?

Truman and Riddiford ask us to imagine a mutant hemimetabolous insect that starts leaving a small pocket of yolk inside its eggs: something that modern butterflies and moths also do. This food source is wasted upon an embryo that cannot feed, but if a pronymph were to develop the ability to eat the yolk whilst in the egg, it would have a great advantage- a pre-hatch snack to prepare it for the challenges of the outside world! Early development of nymphal features like hard mouthparts can be induced by playing around with the hormones of modern pronymphs in the egg, showing us a possible mechanism for this anomaly.

 Like many modern insects, this ancestral insect may have laid its eggs in the soil or in some other secluded environment, away from danger. Therefore, the pronymphs may have had to burrow out of their birthplace before their first moult into a nymph. But the feeding pronymph would have seen things a little differently:  there was food here! Perhaps it was decaying wood under the bark where it hatched (which many young beetles feed on today), or plant roots in the soil. Either way, it was inaccessible to other members of its species: adults and nymphs rarely found themselves in this environment, and other pronymphs were simply unable to eat it. So as well as a head-start from their eggy breakfast, mutant pronymphs also got a boost from helping themselves to some abundant food source for which there was no competition. The advantages of exploiting this resource may have been so great that in future generations, it was better to put off becoming a true nymph, and hold on to pronymph characteristics even after moulting. Gradually, the pronymph stage would have become more and more extensive, and more and more specialised for eating the new food source. This meant the normal nymphal development had to be compressed into a much shorter, more intense period. That’s right- the pupa. This putative sequence of events is much more elegant- we no longer have to explain how nymphs regressed from mini-adults to bizarre eating machines, or how the pupal stage arose de novo. As in countless cases, evolution has tweaked with already-existing material rather than starting from scratch, eventually changing  some features of the organism beyond recognition.

Today, holometabolous insects continue to reap the benefits of their dramatic coming-of-age. Adults and larvae live such different lifestyles that they don’t compete for food and space- leading to a higher population- and a single species can become perfectly adapted to multiple ecological niches. In fact, the latter point could even explain why holometabolous insects are so diverse: living in two different environments might mean encountering twice the amount of environmental change over time. Adaptation to this change, or innovations that allow a new niche to be taken on by one life-stage, means more chance of a new species arising. Some non-metamorphic species- like dragonflies, whose larvae live underwater- have managed some level of ecological separation, but it’s nothing compared to the bizarre rift between the amorphous maggot and its highly-structured parent.

So, next time we ponder over the huge differences that make caterpillars and butterflies seem like entirely separate species, we should remember:  that’s kind of the whole point!

Image credits: Grasshopper nymph by Obsidian Soul (Own work) [CC-BY-SA-3.0 (http://creativecommons.org/licenses/by-sa/3.0) or GFDL (http://www.gnu.org/copyleft/fdl.html)], via Wikimedia Commons

Wanted: nanny. Must be willing to be eaten alive.

Walking the dog the other day, I chanced upon something interesting going on in the path verge. At first, it was the black clusters covering the plant that drew my eye- on closer inspection, aphids. They were not alone- stepping between them were two spindly, fly-like insects that were several times the aphids’ size, but still very small. The aphids seemed agitated by their presence, flicking up their abdomens when one passed close, and it soon became clear why. Every now and then, one of the larger insects would curl its abdomen underneath its body, and dab the tip against one of the aphids: it was laying eggs on them. They were female wasps- not the big, sugar-guzzling yellow and black stingers that have holidaymakers in a state of constant paranoia at this time of year, but members of several related groups that are collectively known as parasitoid wasps. 

You get the idea.

This term covers a broad but very specialised range of insects that provide generously for their larvae… by giving them a live meal. Victims are usually other insects, and they’re not treated with much respect: the eggs deposited on them by the adult female hatch into ravenous young, which devour the host at just the right rate to keep it ticking over until they’re finished with it. There are all sorts of grim but fascinating ways in which the larvae of different species get the most out of their host, with examples of brainwashing, mutation and virus warfare, but the main distinction between a parasitic and a parasitoid lifestyle is that in the latter, the host usually winds up dead. 

It’s worth remembering that as grisly and intriguing as the larval lifestyle is, they couldn’t do it without their mum’s hard work. How does a tiny female wasp track down a suitable host that will take care of her babies until they are grown? (Now there’s a good plot twist for Mary Poppins…) How did my two wasps know that the aphids were there, both ending up on a single plant amongst thousands of others in the area? I won’t keep you in suspense- they used their brains.

Now, insects aren’t exactly famous for being intelligent. Nobody has ever uttered the words “ as wise as a mosquito” (as a compliment, anyway), and anyone who’s seen a bee repeatedly ramming itself against a pane of glass won’t have much respect for their intellect. To be honest, plentiful brain power and learning ability just aren't necessary for most insects: they get through their short lifespans just fine on innate behavioural responses to environmental cues, investing their energy in reproduction rather than IQ. But for some insects, the environment can be quite unstable, and so a rigid response to a certain stimulus might vary quite widely in its effectiveness. 

Parasitoid wasps have just this problem. Different species have a range of hosts that their larvae can survive on: some specialise on just one host, others have hundreds of options. Many host species are herbivorous, and so the volatile distress signals released by damaged plants can be a useful cue for the wasps to follow to find their quarry. Unfortunately, many hosts also have a varied diet, and so always following the same plant species’ signal might yield disappointing results. With the abundances of different hosts and their distributions changing within seasons and between different years, wasps are faced with a dilemma. An innate response to a cue that is successful for one generation may be totally useless to the next generation, depending on where the best food supply is: the changes are much too fast and unpredictable for evolution to synchronise alterations in wasp behaviour with the environment. So the parasitoids have a trick up their sleeves, allowing them to fine-tune their behaviour to suit the current conditions- they LEARN.

In general, the system works like this. Wasps are born with a set of scents that they are programmed to respond to, by following them to their source. If a female wasp finds a suitable host at the end of a certain trail, she remembers her success, and becomes more likely to follow similar scents in future. This process- called associative learning- allows some adaptation to the present environment, but it’s risky: what if her success was only down to chance? It’s a bit like if you once saw a hospital next to a church, and decided that the best way to find a hospital elsewhere in future was to look out for a church spire. You'd be in trouble, basically. So parasitoids have tweaked this basic learning response, and we can get a good idea of how and why by doing comparative studies on closely-related wasp species that face different ecological challenges…

Cotesia glomerata and its close relative, Cotesia rubecala, spend their childhoods inside juicy caterpillars: largely within two species that may be familiar to anyone with a garden or allotment. C.glomerata favours the caterpillars of the Large White: those big, funky-looking grey, black and yellow things that selflessly eat cabbages so that human children don’t have to. C. rubecala has a taste for Small Whites, which are (shockingly) smaller and a more straightforward green colour, but similarly enthusiastic about their five-a-day. Chances are, if you search enough domesticated brassica leaves you’re bound to find at least one of these species crawling around- but in a wild setting, the search is not so straightforward.

See, the lifestyles of the caterpillars are actually quite different, and this has influenced the searching behaviour of their parasitoids. Large White caterpillars have a fairly predictable distribution: they have a small range of plant species that they like to eat, and tend to hang out in big gangs. In fact, a female C.glomerata coming across a bunch of these has hit the reproduction jackpot: she may be able to deposit most of her lifetime supply of eggs on a single colony, and so needs to make relatively few successful forays to fulfil her mission. This means that even if she commits a fairly unreliable scent cue to memory, it’s unlikely to be disastrous, as she’s already secured the future of many of her offspring. So she can afford to be a little careless: usually, only one successful encounter is needed for the guiding scent to be encrypted in the wasp’s long-term memory. This ensures that if she comes across a similar scent again- no matter how far in the future- she’ll be in with a chance of boosting her reproductive success even further.

Small White caterpillars, on the other hand, take a bit more work to track down. Mother butterflies lay just one egg per plant: as our second wasp species C.rubecala also lays one egg per host, it must make far more hunts than its cousin to maximise its reproduction. Even more frustratingly, Small Whites are much less picky about the plants that they lay on, so there are a whole range of potential cues that a wasp must look out for. Committing one to memory too quickly could be disastrous for a female: a single successful search is unlikely to provide reliable evidence for where more caterpillars might be found, and so she could end up wasting her time and energy looking on the wrong foodplants. Furthermore, committing things to long-term memory is actually quite costly for insects.  Unlike shorter-term memory, it requires new proteins to be set up in the neural system, which takes energy. Over the course of a lifetime, brainy can be a bad thing: some experiments show fruit flies that have been working their long-term memories are less resilient to environmental challenges like dessication, and are thus more likely to die early. So to avoid these costs to its health, and sidestep ruining its reproductive success, C. rubecala is much more cautious about forming long-term memories. Until a single cue has resulted in about three successful searches, it will not encrypt it into its long-term memory, storing it using less resilient- but much cheaper- options until then.

Not all wasps use smells to hunt down their hosts: Hyposter horticola has a very different strategy that uses visual cues, but plenty of brain power, too. This species also likes caterpillars, but there’s just one problem: the wasp needs to lay its eggs when the caterpillar is fully developed, but has not yet hatched from the egg. This is a tiny window- just a few hours- and so a wasp that searches randomly with scent cues is unlikely to have much luck. Instead, the parasitoids operate in quite a sinister way to make sure they get their timing right. When the female finds a clutch of eggs, she’ll memorise its location using visual landmarks. She will then frequently visit her hosts-to-be over the next few days to check up on how they’re coming along- presumably standing over them rubbing her hands together and cackling lullabies to the embryonic caterpillars. These regular visits also help to refresh her short-term memory about the location of the eggs, allowing her to monitor several clutches at once. 

It seems a little labour-intensive: why not stick a scent marker on the eggs and follow it back later, freeing up more time to hunt down extra hosts? Unfortunately, butterfly eggs are a much-sought resource in the meadows where Hyposter makes a living, and females are constantly competing to infect a limited number of clutches. Scent-marking the prize would be like erecting a neon sign inviting everyone to join in the macabre baby shower- much better to use natural clues, and keep them to yourself! This system is so effective, and competition so rife, that in many meadows every single egg cluster is parasitized. Luckily for the caterpillars (and in the long term, the wasps), only a third of the eggs in each clutch tend to be infected, though it is not certain why. These tight numbers mean that in any year, the local wasp population is usually exactly one third of that of the butterfly- creating some odd-looking population graphs that look nothing like the classic model of predator-prey fluctuations. Finally, other female wasps get put off laying in the same clutch by a scent mark left by the “winner”- so sibling caterpillars always have sibling parasites inside them. How cute!

As we can see, learning is a costly tool to maintain (kids- add this one to the homework excuses phrasebook). But in the right situations, the benefits of learning can outweigh the cost of investment: whether it’s outwitting predators, prey or competitors, keeping up with ecological flux or interacting with other members of a social group, complex, changeable conditions often require more than simple hardwired reactions from animals if they are to succeed. Now, if an insect the size of a pinhead can use its brain to succeed… where am I going wrong?