Sunday Spinelessness – Throwing pesky males off the scent

By David Winter 19/09/2010

We often think about evolution as a competition, but it’s not always clear who the competitors are. While popular accounts of evolution often talk about species competing for survival, Darwin saw evolutionary change as the result of individual’s struggle for existence and Richard Dawkins recast individuals as proxies in a battle between genes. A new paper from Kerstin Johannesson and her colleagues at the University of Gothenburg highlights another ongoing competition which explains a good deal of biology: the battle of the sexes.

In sexually reproducing species, the costs of making the next generation often fall unevenly on males and females. Take the rough periwinkle, Littorina saxatilis for an example.

Periwinkles are snails that live in the harsh zone between the sea and the shore on rocky beaches. Life in the inter-tidal means a periwinkle can expect to spent some if its day underwater, some high and dry, and be buffeted by waves the rest of the time. Female L. saxatilis have tweaked the typical marine snail lifecycle in response to their harsh habitats. Instead of laying a lot of eggs which hatch as tiny swimming plankton, L. saxatilis females retain a relatively few eggs within their shells. Safely stowed by their mothers, the young snails can develop to such a size that they are able to look after themselves once they hatch. Which is all well and good, but the maternal care displayed by these periwinkles means males have very different interests than females when it comes to mating. From a male’s point of view more is always better, since every mating will increase the number of offspring he will sire. For females it’s a different story, they can only retain so many eggs so only need so many matings to maximise the number of offspring they will produce.

In my little sketch of this sexual conflict I’ve suggested females actually decrease the number of offspring they produce with each mating after some optimal point. That’s with good reason, as mating almost always comes at some cost. The examples from species with sexual conflicts can be gruesome; male bedbugs exclusively inseminate females by puncturing their abdomen with a hypodermic penis, some male water striders will attract the attention of predators unitl would-be mates yield to their advances, and ducks, well, Carl Zimmer has said enough about the ducks. There doesn’t seem to be anything quite as unsavoury going on with these snails, but Joannesson and colleagues were able to show mating still comes at a cost. Inter-tidal creatures are always at risk of being washed off their rocks. Enough rough periwinkle lives have been lost to the waves that all around the world L. saxatilis populations have evolved into two distinct morphological types, a form with a large muscular foot capable of tightly gripping rocks dominates low on the shore while a less muscular form lives higher on the beach. Since a mating couple presents twice as much surface area to an incoming wave, you might expect mating increases the chance a periwinkle gets swept from the rocks. To test this idea researchers got crafty. Literally. They broke out the hot glue guns and stuck empty shells on to females and saw what happened. They showed that periwinkles sporting an extra shell were more likely to fall off a platform dragged underwater in a laboratory tank and less likely to survive in the wild.

L. saxatilis populations are often very dense (around 200 snails per square metre in this study) so females don’t have to go out of their way to provision their eggs with sperm and, given the cost of mating, it’s in their interest to dissuade males as much as possible. So how do they do it? In general, snails seek out other snails by following chemical cues in the trail of mucous they leave behind them. Periwinkles males in particular have been shown to follow female trails when they are on the lookout for a mate, so there must be some clue in the mucous that marks it as belonging to a female. To see how L. saxatilis males do at finding females the researchers collected populations of this species, and three other periwinkle species that live in much sparser populations on Swedish beaches. They then filmed these captive snails moving about in the laboratory and totaled up this distance each male covered in following female and male trails. By comparing L. saxatilis males’ tracking ability with males from these other species the researchers could isolate the effects of the sexual conflict in L. saxatalis . These other species have sparser populations and different mating systems, which mean females are less likely to achieve the optimal number of matings and sexual conflict is less likely to arise. Here’s what they found.

Each point in these charts is the result recorded from one male, the position of the point depends on this distance he covered following male trails (the y- or vertical axis) and the distance covered following female trails (the x- or horizontal axis). So, in the first chart the majority of males spend the majority of their time following female trails and one crawled to the beat of his own drum and followed male trails to the tune of 400 millimetres without showing the slightest interest in females at all. The same overall patter, males following female trails significantly more often than male trails, is repeated in each of the other species (charts ‘a’ through ‘c’) but not in L. saxatilis. Male L. saxatilis don’t seem to be able to pick male and female trails, even when a different population was subjected to the test (so it’s not a local effect in the Swedish snails) and when they were given an hour to get sniffing. So what’s going on? Are females deliberately putting pesky males of their scent, or do males in such a densely packed species just not have to bother with tracking females? As the authors point out, the latter seems unlikely since the males’ inability to pick female trails leads to an unusually large number of male-male couplings in the wild. Time spent tracking and mounting a male is time that could be spent in search of a female. So, even in a dense population, it’s in a males’ interest to be able to tell the difference between male and female trails. To put it to the test, the researchers ran one more test. This time the L. saxatilis males were observed among females from another species (the flat periwinkle L . fabalis). In this test, even with the species gap, the L. saxatilis males have no trouble picking out females:

So, given the chance, L. saxatilis males can find female trails but it seems female L. saxatilis aren’t giving them the chance. By smelling like males these females reduce the burden of unwanted matings and frequently set males up on accidental male-male couplings

Johannesson, K., Saltin, S., Duranovic, I., Havenhand, J., & Jonsson, P. (2010). Indiscriminate Males: Mating Behaviour of a Marine Snail Compromised by a Sexual Conflict? PLoS ONE, 5 (8) DOI: 10.1371/journal.pone.0012005