Check Mate

Gryllodes sigillatus mating
A female decorated cricket, with spermatophore attached, dismounts male

Think of a duck. Chances are, you’re picturing a mallard – and, if you weren’t, you probably are now. Imagine the male with his striking green-blue head, and the comparatively drab, mottled brown female. If you are a regular reader of science blogs, or simply a fan of waterbird genitalia, your mind may wander to his 20cm-long explosive corkscrew penis, or her cavernous vagina, riddled with dead ends and hairpin bends.

The father of modern taxonomy himself, Carl Linnaeus – admittedly, without having gained privy to these reproductive organs – first classified the male and female mallards mistakenly as separate species. We accept these differences readily nowadays, but how and why have they occurred? Even stranger, why should any species evolve such elaborate reproductive organs?

The answer stems from ‘gametes’, or reproductive cells. Males are defined by carrying sperm, millions of pared-down parcels transporting genetic cargo at high speed. Meanwhile, females harbour relatively few eggs, sluggish monoliths packed with nutrients and protection, waiting patiently for one battling sperm to fuse the genetic information and produce a new organism.

This imbalance in the resources ploughed into gametes results in conflicting desires in the sexes. A male could incur little cost by mating with as many females as possible, increasing the probability of his genes passing to the next generation. His female counterpart, having invested so much in her eggs, gains more from exercising restraint to ensure her offspring are of the highest possible genetic quality.

By what means, then, can a female determine her perfect match? Darwin outlined such characteristics in his 1871 book ‘Selection in Relation to Sex’:

“…the greater size, strength, and pugnacity of the male, his weapons of offence or means of defence against rivals, his gaudy colouring and various ornaments, his power of song, and other such characters.”

This system can be as straightforward as the bull elephant seal using his great strength to drive rivals from a harem of females. Other traits proved far more puzzling – Darwin’s frustration in the years prior to this publication is summarised in an 1860 letter containing the epithet:

“The sight of a feather in a peacock’s tail, whenever I gaze at it, makes me sick!”

One theory is that such traits indicate genetic quality by acting like handicaps. Bright colours, displays and songs attract predators, while a cumbersome tail hinders a quick getaway. A male may be indicating, “Hey, if I have such a big handicap and I’m still here, doesn’t that show you how great I am? You should probably have my babies.”

What happens, then, to those that cannot compete at the highest level – should they simply give up? No, instead they engage in some downright sneaky behaviour, such as yellow dung flies waiting at the edge of a dung heap, ready to pounce on unsuspecting females travelling to meet Mr. Right atop a delicious pile of excrement. On the Hawaiian island of Kauai, Professor Marlene Zuk discovered that the mate attraction ‘song’ of the field cricket – produced by males rubbing their wings together – had enabled an invading parasitic fly to target the species ruthlessly. Rather than face extinction, however, this cricket population rapidly evolved to favour a mutation that removed rough edges from the wings. These smooth, silent crickets possess no real powers of attraction, instead surrounding the remaining chirpers in the hope of engaging a prowling female. While she would prefer a personal serenade from her potential mate, waiting too long exposes her to greater danger – or the risk of being ‘left on the shelf’. There is such a thing as being too choosy, after all.

Another tactic is to offer a ‘nuptial gift’, which can be an edible treat that the male produces himself. This has led to the synthesis of offerings that lower the female’s desire to remate before his sperm have completed fertilisation. ‘Aggressive sperm’ may outcompete or kill off rival gametes, while a dragonfly penis can scoop out existing seminal fluid. The bumblebee, meanwhile, breaks off its penis in the queen to form a ‘vaginal plug’ – an extreme case of putting all your eggs in one basket, if that’s not too confusing an analogy given the topic at hand.

It would be foolish to presume, however, that females have been standing by idly in evolutionary terms. Insects such as water striders and seaweed flies are locked in a race whereby females evolve anti-grasping functions just as the males develop claspers. Indeed, the mallard’s complex vagina has evolved as a defence mechanism. As the female is victim to frequent attempts at forced copulation, this not only helps to prevent entry, but also diverts unwanted sperm away from those precious eggs.

This arms race has raged ever since sex first evolved. As long as males and females continue searching for the tiniest advantage over one another, the battle of the sexes shows no sign of slowing down.

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