Growing up, an animal's environment can influence its personality. But researchers also want to know whether the parents’ environment can influence the personalities of their offspring too. Recent work by Juliette Tariel and colleagues from the Université Claude Bernard in Lyon, France, suggests that this is the case for the offspring of freshwater snails (Physa acuta). An animal's response to predators is just one behaviour that could be affected by the parents’ environment. So Tariel and colleagues wanted to see how snails would respond to a predator, and whether the youngsters’ responses to a predator varied – from relaxed to terrified – if their parents were familiar with the predator's smell.

The researchers took adult snails from the river Rhône in Lyon back to the lab. They then put the snails into plastic containers filled with either freshwater or water mixed with the smell of the snail's predator – crayfish – and allowed the snails to breed. Finally, the team left some of the offspring in their original watery homes or transferred them to a container with the opposite-scented environment, predicting that offspring of parents familiar with the crayfish scent would respond faster to the predator and that there would be more variation in their individual responses. To test this, the researchers put an adult snail into a container filled with crayfish water and counted how many seconds it took for the snail to escape and crawl out of the water.

Surprisingly, Tariel and colleagues found that the parents’ environments didn't affect the variation in behaviour of their offspring. All of the youngsters whose parents that had lived with the stink of predators escaped within similar time frames.

In contrast, growing up with the smell of fear did affect the youngsters’ behaviour. Individual snails often responded differently from their brothers and sisters; there was much more variation in their behaviour. The difference in the baby snails’ responses might be due to differences in how they use energy while developing. For example, some snails may invest energy into growing thicker shells for defence rather than building muscle for a sprint escape.

Another surprise was that the snails produced by parents that bred in the crayfish-ridden water tended to escape more slowly when presented with a predatory crayfish; if they tried to escape at all. The snails’ slow escape might be because the snails are familiar with the odour of crayfish. The scent of crayfish usually warns snails when a predator is at large, but if the snails constantly smell crayfish without encountering the genuine threat, they could well stop responding to the scent as they appear to have nothing to fear.

While this is the opposite of the researchers’ original prediction, the discovery that crayfish odour carried less dread for the offspring of parents living with the scent of fear suggests that the environment of parents can affect how their babies respond to changes in their own environments. In the case of these freshwater snails, where their parents grew up could be a matter of life and death, if the youngsters have lost their edge and don't know when to make a speedy getaway.

How do developmental and parental exposures to predation affect personality and immediate behavioural plasticity in the snail Physa acuta?
Proc. R. Soc. B
. doi:10.1098/rspb.2020.1761