Magnified spermatozoa of Tribolium castaneum flour beetles. Competition between sperm of different males within a female reproductive tract, leading to selection of compatible sperm, could explain why promiscuous inbred females have higher fitness than females that were mated to single males.
Credit: Łukasz Michalczyk
A mating pair of Tribolium castaneum flour beetles. By mating with multiple males, inbred females can rescue their reproductive fitness.
Credit: Łukasz Michalczyk
CAMBRIDGE: Female promiscuity is higher in inbred populations, where taking multiple partners allows them to maximise their reproductive success, scientists have found.
Research published last week in Science uses the red flour beetle (Tribolium castaneum) to demonstrate the effects of genetic bottlenecks on mating patterns.
It shows that inbreeding promotes polyandry, a mating pattern in which females mate with several males, and may provide an explanation for the evolution of this strategy despite its negative costs.
"Most species on our planet reproduce sexually and most of these have a polyandrous mating pattern," explained evolutionary biologist and lead researcher Matthew Gage from the University of East Anglia in the UK.
"We provide a solution to why this common but somewhat paradoxical female mating pattern can evolve as a means to avoid reproducing with incompatible males."
Possible polyandry pay off
The optimal reproductive strategy for females of any species is to mate with only the most genetically compatible available male - the one that will ensure the strongest offspring.
Mating with many males, as in polyandry, can reduce reproductive success; high frequency mating can cause trauma, exhaustion or even death. But in some situations, this risk may pay off.
One example of this is when a population is highly inbred. This reduces genetic compatibility and reproductive success because there is less variation in the population's genes. This increases the risk that offspring inherit traits that reduce their survival.
Some species have evolved mechanisms to avoid inbreeding. Female field crickets, for example, use a post-mating selection mechanism to take up more sperm from an unrelated male over that of a brother, even if they mate with both.
Inbreeding promotes polyandry
Gage and his colleagues set out to discover whether similar mechanisms could lead to polyandry once inbreeding has already occurred.
The group created a population of inbred beetles and assessed the mating behaviour of the females against an outbred control population.
They looked at their reproductive success, measured as the number of surviving offspring each produced, and their motivation to mate.
Reproductive success of females in the inbred population increased when they were allowed to breed with five males rather than one. Outbred controls were equally successful in both cases.
"Because inbred and outbred males have identical fertility," explained Gage, "the result tells us that females in inbred populations used promiscuity to either avoid fertilisation by genetically incompatible sperm, or promote fertilisation by more compatible sperm."
Inbred females more frisky
The researchers also found that females from an inbred population were more motivated to mate than outbred controls when presented sequentially with ten different males.
"Females from previously-bottlenecked populations were quicker to mate with each new male, mated more frequently, mated for longer, and spent more total time actually mating," explains Gage.
This demonstrates that inbreeding promotes polyandry, providing an explanation for why this mating pattern may have evolved despite the costs.
Compelling evidence
Gage points out that their model system is exaggerated to allow easier measurements, and that the situation in a natural environment may be more complex.
"Evolution is likely to work on more subtle benefits and costs over hundreds of thousands of generations. There might still be sufficient genetic compatibility benefits to be gained through some promiscuity even under non-inbred conditions."
However, Jonathan Evans, an expert in sexual selection at the Centre for Evolutionary Biology at the University of Western Australia, thinks this study goes further than any other in understanding the evolution of polyandry.
"Until now, there has been very little evidence that variation in female re-mating behaviour has a heritable basis, much less that such genetic variation can respond to selection," he said.
"[This study] provides really compelling evidence that female behaviour can evolve adaptively to exploit post-copulatory mechanisms of incompatibility avoidance."
