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Seen one seen them all? More to genitalia than meets the eye

Guess what? It’s not so much size but the shape that matters. Ozchin

Why should male genitalia be so variable? This problem has puzzled evolutionary biologists for decades.

Even to the experts, it can be difficult to tell closely-related species apart just by looking at their physical appearance (or morphology).

Take even a quick glance at the shape of male genitalia in each species though and it becomes far easier to differentiate: different species have different genital morphology.

But why should male genitalia differ so greatly in size and shape?

Sexual selection

Evolutionary biologists have argued that “sexual selection” (when an individual has a reproductive advantage over its peers) may drive genital evolution in much the same way that it drives the evolution of exaggerated secondary sexual traits, such as the peacock’s train.

There are a number of different ways in which sexual selection can act:

  • Female choice of mating partners
  • Females deciding whether or not to accept and use sperm from their mating partners
  • Male-male competition, where males compete to mate with (and fertilise) females
  • Sexual conflicts when the interests of males and females differ, in regards to mating and fertilisation.

Consider the penis-equivalent of damselflies and dragonflies: it is equipped with structures that allow a male to remove sperm deposited by a female’s previous mate.

Then there are water striders in which males with long genitalia and short bodies are more successful in achieving genital contact than males with short genitalia and long bodies.

It is easy to see that the better-endowed male will achieve greater reproductive success, and his sons will inherit his sexual prowess. But this may not always be in the female’s best interests.

In seed beetles the penis is covered with aggressive spines that anchor the penis into the female reproductive tract. These spines ensure a higher degree of control for males over mating duration and paternity, but the damage inflicted on the female’s reproductive tract can reduce her lifespan.

(In case you are curious, penile spines were a feature of our early human ancestors. Indeed, we still retain the genes that encode penile spines although past selection has silenced them).

So what about female genitalia?

We might expect that female genitalia should also exhibit variation in size and shape, either because it allows a female to detect variation in male genital shape, or because it’s the way females evolve resistance to damaging male genitalia.

But so far, female genitalia have been much less studied.

If sexual selection drives the evolution of genitalia, then the evolution of male and female morphology should happen in concert, because the interaction between the sexes that culminates in successful reproduction – be it a “ballet” or a “war” – is based on the interaction of their genitalia.

Here at the Centre for Evolutionary Biology we have used the approach of experimental evolution on dung beetles to explore the concerted evolution of male and female genitalia.

What we found, and how we did it

We either enforced monogamy or allowed sexual selection to continue in replicated dung beetle populations. After four years (or 21 generations of dung beetle) we measured the changes in genital structures produced by the presence or absence of sexual selection.

In parallel, we inspected the genetic architecture underlying these genital traits. The results, published this week in Nature Communications, were very revealing: male and female genital morphology responded to sexual selection, and they did so in a way that reflects correlated evolution across the sexes.

Males from the sexually-selected lineages evolved a penis that was elongated relative to males in the monogamous lineages. Meanwhile, females from the sexually-selected lineages evolved smaller and harder to reach genital pits, structures that males need to gain anchorage in if they are to copulate successfully.

Furthermore, we were able to determine – for the first time in any species – the occurrence of sizeable genetic variation in female genital morphology.

Importantly, families of beetles with genes that resulted in sons having an elongated penis also had genes that resulted in daughters having smaller genital pits that are harder for the male to reach.

The close association between genes that determine the shape of male and female genital shape undoubtedly facilitate the concerted evolution we observed.

Our results provide the most complete data available for any species on the mechanisms – and evolutionary responses to – sexual selection that have long been argued to underlie the evolution of male genitalia.

They show that male genitalia evolve in much the same manner as the bright plumage coloration or elaborate acoustic signals that promote male reproductive success.

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