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Mating is a secretive affair for small male Loligo squid. Whereas their larger brethren try to woo females by showing off their changing colours and beating each other into submission, the smaller males do not stand a chance in this courtship game. Instead, they have to rely on stealth tactics. After a large ‘consort’ male successfully courts a female, he deposits sperm into her oviduct. A small ‘sneaker’ male then rushes towards the mating pair and quickly deposits his sperm onto the female's skin, aiming for a small receptacle near her mouth. The female expels the eggs from the oviduct, where most have been fertilised by the consort sperm, but as she deposits the eggs onto the seabed using the arm crown around the mouth, they are exposed to the sneaker sperm, resulting in external fertilisation of the remaining unfertilised eggs. How can this form of fertilisation be effective, given that there is little preventing the sneaker sperm from drifting off?

A team of researchers from various institutions in Japan, Germany and Italy have found at least part of the answer to this question, in a study recently published in Current Biology. When the team put sperm of consort and sneaker males into chambers and labelled each population with a different dye, they found that the sneaker sperm, but not the consort sperm, formed swarms by independently swimming towards each other. This behaviour has been seen in other animals, and will help the sperm to stay in the same spot. When the researchers then introduced a filter into the chamber that only allows small molecules to pass, they noticed that the sneaker sperm swarmed on either side of this barrier. As the cells cannot touch each other across the membrane, this suggests that the sperm are attracted by a molecule that they themselves produce. What molecule could this be?

After ruling out a number of chemoattractants, the authors found that a bubble of CO2 strongly attracted sneaker, but not consort, sperm. This was very interesting, as CO2 is a product of cellular respiration, and therefore it fits with the hypothesis that the sperm, itself, produces the attractant. In fact, when the team added inhibitors of a common sensor for CO2, carbonic anhydrase, to the chamber, the swarming behaviour of sneaker sperm was reduced.

However, both sneaker and consort sperm have this sensor, so why are only sneaker sperm sensitive to CO2? The authors noticed that when sneaker sperm came into contact with CO2 their intracellular pH dropped. In a series of molecular experiments they showed that it is precisely this acidification that underlies the swarming: when the intracellular pH drops, the sperm keep swimming in the same direction, but when it shoots up, they make a turn. This process results in a net movement towards the source of CO2. The consort sperm simply lack the molecular machinery that acidifies the intracellular milieu in response to CO2, and are therefore not sensitive to it.

This study elucidates how sperm has adapted to different mating behaviours through the process of evolution. It tells us that physiology adapts even within the same sex of the same species to ensure individuals can reproduce, so even the little guy has got a chance.

References

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