The promiscuous sex lives of bush-crickets: Females prefer one night stands and avoid mating with the same male

In Victorian times, it seems that most scientists, including Darwin, assumed that females of all species mated with just one male. Over the last few decades, however, it has become increasingly clear that this is far from the truth. Advances in techniques such as DNA fingerprinting have revealed that polyandry (females mating with more than one male) is widespread in the animal kingdom - even in many species which appear to be monogamous. There are still relatively few studies that have been able to measure the true extent to which females mate with different males, as opposed to re-mate with the same male, in the wild, however.

Multiple mating by females is obviously not in the interests of the male. The existence of this mating strategy in females has resulted in a wide range of evolutionary counter-adaptations in males. These are particularly diverse in the insect world and include chastity-belt-like mating plugs, which can prevent females from re-mating, guarding females from rival males, and the transfer of hormone-like substances that switch off the female's sexual receptivity.

But when it comes to choosing a mating partner, it seems that it's the female dark bush-crickets who are in control.

Through new research, carried out by myself and a team of researchers at University of St Andrews' Centre for Biological Diversity, we have discovered that female bush-crickets are tactical in choosing who they mate with; although they mate multiple times, they appear to strategically avoid having sex with the same male.

This is the first study that has been able to determine, for females that had mated in the wild, not only how many different males they had mated with, but also how many times they have mated with each male. Our study has also allowed us to work out which male's sperm each female used to fertilise her eggs and the factors affecting this, such as the relative position of sperm in the female's reproductive tract. Due to the difficulty of distinguishing sperm from different males within the female's sperm stores, very few previous studies have been able to quantify the effect of the relative position of sperm on male fertilisation success.

How was the study carried out?

In a bid to find out more about the mating patterns of dark bush-crickets, we collected 36 females at the end of their mating season from a densely-populated hedgerow in Devon before taking them back to the laboratory at the University of Derby. There, we maintained the females in captivity and allowed them to lay eggs for two weeks.

We were able to examine the extent to which females mated with the same or with different males for each mating due to a unique aspect of bush-cricket biology: each time a female bush-cricket mates, the male's ejaculate is stored in a separate container within her sperm storage organ. Within this area, the female stores sperm from every male she has ever mated with during her lifetime.

So, by using a species of cricket in which sperm from different matings occur in discreet packages within the female, we were able to examine not only whether each mating was with a new or a previous partner, but also the influence of the position and number of sperm deposited on male fertilisation success in females that had mated in natural field conditions.

We extracted DNA from the sperm in each of the separate packages within the female's sperm stores and matched this with DNA extracted from the female's eggs. This allowed us to work out how many different males the females mated with and which of the sperm were used to fertilise the eggs.

What did the study find?

Our study, which was recently published online in the journal Molecular Ecology, revealed that female bush-crickets appear to adopt a deliberate multiple mating strategy.

Only six of the 36 female bush-crickets we examined had mated with the same male more than once - meaning that over 80% of the female crickets mated with a different male each time. We also found that each cricket had up to six different partners. These results back up previous laboratory studies which have shown that female crickets prefer novel partners, and even mark their mates with their own unique scent so that they can avoid re-mating with them.

It is likely that female dark bush-crickets avoid mating with the same male because this strategy improves their fitness. Previous laboratory studies of crickets and a range of other animals have shown that mating with multiple partners (as opposed to re-mating with the same partner) can increase the hatching success of the female's eggs and even be associated with an increase in the survival of her offspring. These effects are thought to result from females having a greater chance of mating with males with better, or more compatible, genes (akin to not putting all their eggs in one basket).

Our study also found that sperm package size and placement influence fertilisation success in the bush-cricket: larger sperm packages and those from the female's most recent mate fertilised a greater proportion of eggs. As might be expected, we also found that a higher number of competing males reduced the chances of siring offspring for each male, confirming that from the male's perspective, polyandry is not a good thing.

Dr Karim Vahed talks about the research

The research paper was written by Karim Vahed, University of Derby; Mike Ritchie, University of St Andrews; Darren Parker, University of St Andrews' School of Biology; Julia Zaborowska, University of St Andrews' School of Biology.

View full research paper