Rival competition makes ant sperm better swimmers

Ant sperm recognize rival sperm and become more mobile, faster and straighter swimmers as a result, according to a study published in the open access journal BMC Evolutionary Biology. The study looked at the factors that modify sperm behavior when there is competition with sperm from other males in a social insect which only mates on a single day during its lifetime.

Researchers at the University of Copenhagen, Denmark found that mixing ejaculates from different male ants in vitro increased the number of mobile sperm by 50% compared to control samples which had been mixed with a saline solution. Sperm mixed with rival ejaculates were also more than 20% faster and swam in straighter lines compared to controls.

Dr Joanito Liberti, the first author of the study said: "Ants are peculiar in that all their sexual activity is carried out during a single mating event early in adult life. When ant queens mate with multiple males their sperm have a single time-window to compete with rival ejaculates for storage in the reproductive organs of the queens. We discovered a fine-tuned mechanism of sperm motility that appears to be regulated by reproductive secretions from both male and queen ants. The findings suggest that sperm are able to assess the level of sperm competition and adjust their level of movement (motility), and thus energy expenditure, accordingly."

In a series of follow up experiments, the authors found that the increase in sperm motility when mixing ejaculates was induced by the seminal fluid of rival males, not by their sperm, and that a similar increase could also be induced by mixing sperm with the reproductive tract fluid of queens. This fluid is made in the spermatheca, the female organ that receives and stores sperm. The increases in sperm motility that followed contact with fluids of other males or sexual partners went well beyond increases in motility that were observed when sperm were mixed with own seminal fluid. The proportion of mobile sperm, their swimming speed and linearity were 40%, 15% and 8% higher when exposed to rival seminal fluid or queen secretions than when exposed to own seminal fluid.

Professor Jacobus Boomsma, senior author of the study said: "Previous studies by our group showed a decrease in sperm survival after exposure to seminal fluid from rival males in the same leaf-cutting ant species that our current study is about. So we would have expected similar negative effects of rival seminal fluid on sperm motility, but we found the opposite result. Our observation that rival male seminal fluid enhances sperm motility more than own seminal fluid does, suggests that sperm have evolved a self-non-self-recognition mechanism to regulate motility."

The finding that changes in sperm motility, swimming speed and linearity are less pronounced in the presence of own seminal fluid also suggests that enhanced mobility is costly to ant males, for example because it may place sperm under oxidative stress, according to the authors. This, in turn, may impact the long-term viability of the sperm when they are stored within the female reproductive tract. As females store and use sperm to fertilize eggs over many years, sperm viability over time is important to both males and females. Whether increased motility really is associated with higher oxidative stress needs to be investigated in future experiments.

The authors extracted sperm from male Acromyrex echinatior leaf-cutting ants collected in Gamboa, Panama between 2002 and 2014 and mixed the sperm either with a saline solution, with own seminal fluid, with rival seminal fluid, or with both own and rival seminal fluid. They then used microscopy techniques to measure the rate of movement, the speed and the directionality of the sperm as they swam. In further experiments the authors also exposed sperm to fluids from the female reproductive tract, in combination with own, rival or no seminal fluid. The authors caution that their aim was not to replicate the natural environment that sperm encounter after insemination. Rather, they studied the sex-specific factors that modify sperm competition and sperm storage in a social insect whose females may live for decades but complete their life-time mating activity on a single day early in adult life when they disperse to found new colonies.

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