A closer look at sex

Damian Smith asks if a closer look at the sex lives of fruit flies can reveal some dark details about our evolutionary past?

Linked paper: Sexual conflict over remating interval is modulated by the sex peptide pathway. Damian T. Smith, Naomi V. E. Clarke, James M. Boone, Claudia Fricke, Tracey Chapman 2017 Proceedings B doi: 10.1098/rspb.2016.2394

First up, check out this animation we made about our research. Read on for more.

When most people think about sex, they think about the harmonious pairing of momentary bliss between two individuals. And in the animal world, they usually think of a flashy male vying for the attention of the best female so they can rear healthy offspring together. But when you look a little (a lot) closer, things are definitely not what they seem. Yes, males try and attract females, and yes females are (usually) fussy about which male they mate with, but the reality of the situation involves a lot more conflict between males and females than first meets the eye.

Sexual conflict

There is conflict because females want their offspring to be fathered by the best possible male, whereas males want the females offspring to be fathered by them, not someone else. This causes females to shop around and mate with multiple males. Generally, it’s pretty hard for males to fake how good they are, because what females are looking for is usually truly costly to males (showy males will get spotted by predators or use most of their energy showing off rather than foraging). Males have evolved ingenious ways to make sure they father the offspring.

This is a fruit fly up close. I will forgive you if you think they are a little cute 😉

Possibly the best way to ensure you are the father is to make sure the female doesn’t mate to another male. You could sit around and “protect” her from other males like in the golden dung fly  (yes, its yellow) and dragonflies, or you could block up her reproductive organs by leaving a plug behind like in bees, or if you are extremely committed, you could snap off your penis and leave that behind during mating to plug up the hole, like these spiders do (although it doesn’t seem to help). But if you wanted to get sneaky, you could use some chemical warfare to stop her remating. That’s what the fruit flies does. The males use proteins attached to their sperm that break off when inside the female. Helpfully, it is called “sex peptide” and it binds to neurons in the female to change her behaviour so she rejects other males when they try and mate with her.

So now we know that males are trying to prevent females from mating again, and we know that a male protein is responsible for achieving that in fruit flies. Being scientists, we decided to find out what would happen if we switched off the protein. We asked Naomi Clarke, a third year student, to run this project for us. Having never worked on fruit flies before, Naomi had the tough task of completing an overambitious project. I showed her the ropes, and we quickly got on with putting hundreds of flies in tubes and watched them mate.

This video is of us setting up a big experiment. The whole teams gets involved so we can get lots done. Those tubes in the background each have a male and female fly in them, and we record when they mate.

The gritty details

We expect conflict in a situation where males and females want different lengths of time between matings to maximise their offspring production. So we compared offspring numbers from females that could and could not respond to sex peptide and whether the offspring belonged to the first or second male she mated with. We borrowed some flies from Nilay Yapici and her colleagues (check out their paper here) where they had taken the receptor for sex peptide out of the females (genetics is awesome).

We then mated each female to two males, with different lengths of time between the matings. Timing is everything here, but not all the players in the situation will necessarily have the same priorities. Just imagine, if you were the first male a female mated with, you probably want her to not remate for a long time, so that she can produce offspring with your sperm. However, the second male probably wants to mate sooner than that so that he can produce some offspring before the female gets too old.

When females were able to respond to sex peptide, the female, first male and second male she mated with all differed in the optimum time to remate in terms of number of offspring produced (textbook conflict). However, when we took away the ability of females to respond to sex peptide then everyone benefits from (and produces the most offspring) when there is the same interval between matings (peace on earth). This means that this one protein is responsible for a major source of conflict between males and females. i.e. when they mate.

The interesting results bit

summary eternal triangle figure.png

This figure shows how many offspring the first male (top left), second male (top right) and female (bottom) have when the females mates to two males, with a different length of time between the matings. The grey bars show the number for when females have the receptor for sex peptide (SPR+) and the white bars when the female does not have the receptor for sex peptide (SPR0) and the error bars are standard errors. I have added red arrows to show the maximum offspring production when the female can respond to sex peptide, and a faded red and blue arrow for when she can’t. This is to show that the maximum offspring production differs for each individual when females respond to sex peptide, but everyone benefits from the same interval between matings when females can’t respond to sex peptide.

Glow in the dark sperm

As an added extra we used fruit flies with fluorescent sperm to see what the sperm of the two males was doing, and if it was responsible for these differences in male offspring production (check out the video below of them swimming around in the female reproductive organs). Perhaps sex peptide plays a role in throwing out previous mates sperm from the female for example. At this stage Naomi worked in a dark room with a microscope for weeks at a time so she could see the fluorescence better. It turns out sex peptide doesn’t really make much difference to the sperm numbers of the two males, and it isn’t the number of sperm that counts in this situation, which is a bit of a shame given the cool glowing sperm and the work involved to count them. But what it does mean is that the efficiency of sperm use by the female changed if she could respond to the sex peptide from the males, because sperm numbers did not differ, indicating it was how she used them that mattered. During the analysis stage, we thought for a long time there wasn’t much information to be gathered from this part of the project. A very vitamin D deficient Naomi wasn’t happy about that.

Something unexpected

One final thing we saw was unexpected, and pretty cool. When the female had mated twice, she produced offspring much faster than when she had only mated once. Quite odd. This happened a bit when females could not react to sex peptide, but happen loads more when she could, but only if she mated again really soon after the first mating. This means that sex peptide helped the second male hijack any effect on producing offspring caused by the first male.

So we have a male protein that tries to stop females remating so that he gets all the offspring. When she does mate again, this protein is also important for determining when the three individuals (first male, second male and female) benefit most from female remating. Without it, they all agree when it best for the female to mate again, but if it is there (which is the normal state), they disagree on when the female should mate, which introduces conflict into the situation.

Interesting because….

All this may sound small and unimportant, but remember this: every animal you have ever heard of (including you) is only here today because of sex. Most species (including us) have females that mate with more than one male. In most of these (including you) males have mechanisms to try and make sure the male fathers the offspring. So these processes are important for a huge number of species. In evolutionary terms, conflict is super cool. If there is conflict, organisms adapt to get the upper hand. Then there are counter adaptations, just like in a military arms race. This process is potentially never ending, and can drive evolution forever, and has almost certainly played a huge part in the life around us today.

About the author

14103013_933528736630_7539182535544892687_oDamian Smith is an evolutionary biologist interested in how conflict between male and females has driven evolution to produce the life we see around us today. He mainly focuses on how males use proteins that they transfer to female with their sperm to influence female behaviour. For more information  about this work Damian can be contacted at Damian.Smith@uea.ac.uk.