Trials of a sperm
Nicola Hemmings examines the numerous factors that influence a sperm's chances of fertilising an egg
The Biologist 62(4) p18-21
A sperm's journey from insemination to fertilisation can be likened to running a marathon. In order to win, runners must possess the perfect suite of morphological, physiological and genetic traits, and most runners simply don't have what it takes.
Sperm are no different. Of the hundreds of millions of sperm typically inseminated, only a tiny fraction – fewer than 0.001% in mammals and birds – make it anywhere near the egg. In fact, a sperm's task is akin to running several consecutive marathons across treacherous terrain with a few battlefields thrown in for good measure.
The female reproductive tract is a remarkably hostile environment for sperm. On entrance, they are treated as foreign bodies by the immune system and face aggressive attack. The female then proceeds to whittle down the surviving few, preventing too many sperm reaching the ovum – which can jeopardise development – while simultaneously ensuring those that do make it are fit for task. On their journey to the egg, sperm must therefore overcome a barrage of physical and chemical obstacles. Most of them die trying.
Secrets of success
Sperm are unrivalled among animal cells in their morphological diversity. From the corkscrew form of passerine bird sperm to the 6cm long flagella of Drosophila bifurca sperm[1], shape and size have obvious implications for sperm function. However, this extreme variation makes it difficult to identify a universal set of vital statistics for winning sperm. Is it possible to define a general recipe for success?
There is one clear rule: sperm must be free from abnormalities, deformities and damage (see above) in order to progress even a short distance through the female tract[2,3,4]. However, once the dross is eliminated and only morphologically 'normal' sperm remain, the link between morphology and success is rather unclear.
Theoretically, sperm that are equipped with a large midpiece (the powerhouse of the sperm) and/or flagellum (the motor) should have more energy and propulsion, aiding their progression through the female tract.
In reality, though, this isn't always the case. In certain mammals, fishes and birds, swimming speed increases with sperm length. Yet, in others, swimming speed doesn't appear to be influenced by sperm length at all5. Long sperm have even been found to be slower than short sperm in two (very different) species – the fruit fly Drosophila melanogaster[6] and the emu Dromaius novaehollandiae[7]. Therefore, a concept of the 'best' sperm morphology remains elusive.
Speed and staying power
Sperm morphology and motility are closely linked. Considering the effect of speed and endurance on sperm success may therefore help us understand some of the counterintuitive relationships described above.
In general, successful sperm are fast sperm. Sperm that fertilise eggs tend to be those that are able to traverse the female reproductive tract quickest and reach the egg first[8]. Recently, Bennison et al. (2014)[9] found a clear relationship between sperm morphology, swimming speed and fertilisation success: within a single species, the zebra finch (Taeniopygia guttata), longer sperm (a) swim faster, (b) reach the ovum in higher numbers under direct competition with short sperm and (c) are more likely to fertilise eggs.
This series of knock-on effects makes logical sense, but speed can also have its downsides. The faster you swim, the sooner you run out of energy and ultimately die[10]. If sperm need to stay alive and viable for extended periods of time, a slow and steady approach could prevail[11]. This is more likely to be the case for externally fertilising animals, such as broadcast spawning aquatic species whose sperm may have to search far and wide for eggs.
Suitability
With males under strong selection to produce super sperm, females could simply sit back and provide the arena for sperm competition. This passive approach would promote competition between sperm, allowing only successful competitors to fertilise eggs. It's not a bad strategy – 'good genes', coding for competitive sperm, may then be passed on to the female's offspring, ultimately enhancing their future reproductive success.
However, the 'best' sperm should not only be able to win in sperm competition, but it should also carry a set of genes that are compatible with those of the female. The level of genetic compatibility between males and females is known to influence sperm success, and this is often mediated by the female herself. For example, when female field crickets (Teleogryllus oceanicus) were inseminated by related and unrelated males, sperm from the unrelated males were preferentially used by the female for fertilisation[12]. This makes good reproductive sense – related individuals tend to have a similar genetic makeup. By differentially using sperm from unrelated males, females enhance the genetic variability of their offspring and avoid inbreeding depression.
There is an array of mechanisms by which females can implement their preferences post copulation, from differential sperm storage and ejection[13] to direct assessment of sperm pronuclei inside the ovum[14]. Differential sperm use by females has been termed 'cryptic female choice'[15], because the choices are made inside the female reproductive tract and hidden from the male, giving females at least some control over the outcome of sperm competition.
A recipe book
Cryptic female choice has important consequences for the vital statistics of successful sperm. Once inside the reproductive tract, interactions with the female epithelial tissue, ovarian fluids and even the egg can dramatically influence sperm performance.
While certain thresholds of form and function may be required for sperm to make it to the egg, successful fertilisation can ultimately depend on the suitability of genes carried by the sperm. Females differ, making it impossible to identify a one size fits all rule[6]. Indeed, we should expect sperms' competitive success to vary depending on the female.
If one thing is for sure, it is that identifying a universal recipe for successful sperm is unrealistic. However, this doesn't mean the secrets of successful sperm must remain a mystery.
Recently, there have been a number of elegant sperm competition studies that have explicitly tested the fertilisation value of multiple sperm traits, simultaneously and under different contexts[16,17,9]. By comparing and contrasting these studies, we can begin to explain the various conflicting patterns that have been linked to sperm success.
Instead of universal rules, we should be aiming to write an entire recipe book for winning sperm, taking into account the highly varied environments in which they will be operating. In my opinion, this is a far more ambitious and exciting goal for future studies of sperm selection.
Dr Nicola Hemmings is a postdoctoral research associate at the University of Sheffield. She is currently working on the mechanisms of sperm transport and sperm selection in birds.
References
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