Sperm Competition in Mammals

The Microscopic War Inside Promiscuous Females

You’re surely familiar with the term ‘sexual selection’, especially if you binge-watched every David Attenborough documentary like I did, on repeat. Sexual selection is responsible for some of the most remarkable features seen in the animal kingdom – the majestic antlers of deer, the radiant colors of the birds-of-paradise, the huge nose of the proboscis monkey, the magnificent tail of the peacock or the violently blue scrotum of the vervet monkey...

These features signal a male’s quality – bright colors are expensive to make, and they require good health. Also, anything absurdly large and conspicuous doesn’t only attract mates, but also predators. If the carrier of such features lives long enough to reach maturity (i.e. it doesn’t get eaten despite being handicapped by them) and mate, it’s more than obvious that a female should want her offspring to carry his genes - if the father succeeded in life, his sexy sons will as well.

Naturally, sexual selection leads to contests. Males will either get into fights to gain access to females, or it's the females who will choose who they mate with, so males will perform sexy dance-offs or present their vocal repertoire and try to out-perform their rivals. Females then decide who's good enough to win the prize - fathering the next generation.

You’d think that that’s where the story ends - the couple gets to mate and everyone can live in peace until the next mating season, right? Not quite.

For many species, the contest continues on a microscopic level, inside the female, post-copulation. You'd be naive to believe that most species are monogamous. The opposite is true. A 2013 study found that only 9% of 2543 mammalian species are socially monogamous (and that's more than a third of all mammalian species on Earth), but even socially monogamous species aren't necessarily genetically monogamous - females will often mate with a neighbor or two nonetheless.

It's no surprise, then, that sperm of various males often meet inside a female's reproductive tract. They compete over fertilizing the female's egg(s), and that's what we call sperm competition. Let me introduce you to the theory of this microscopic war, but be warned – it’ll get kinky.

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If you're unfamiliar with the terminology used in this article, please check the vocabulary below!

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How to React to Sperm Competition

Picture it as a lottery or raffle – the more tickets you have, the greater your chance of winning! Sperm competition caused the evolution of many more physiological and behavioral adaptations, such as mate guarding, repeated copulations or repeated ejaculations, shorter intervals between ejaculations, plus also some freaky stuff that you’ll find below. These adaptations evolved to outnumber rivals in sperm count (scramble type sperm competition) or to make further copulations with a given female impossible (interference type sperm competition).

There are two models that aim to explain how males react to sperm competition:

Sperm competition risk (SCR). In this model, there are two males and the prediction is that as the risk of competition increases (i.e. the chance that the rival male will meddle with the other male’s prospective mates increases) sperm investment also increases. This means that the male whose SCR gets from 0 to 1 will have sex more frequently, reduce the time between each copulation as well as between each ejaculation. Apart from the straightforward effect – sowing more seed – this can also cause the elimination of a rival’s sperm or reduce the females’ sexual receptivity.

Sperm competition intensity (SCI). If females, by default, mate with more than one male, males will reduce their sperm investment with growing SCI (i.e. with a growing number of rivals) and increase sperm investment with decreasing SCI (i.e. when the number of rivals is low). There’s already a high competition risk in this model (females are expected to mate with numerous males), so if males invest their sperm wisely, they’ll save enough to mate with a bunch of them, increasing the chances that at least one of them will carry their child.

As goes with many models, these have also been challenged by growing experimental evidence: DelBarco-Trillo and Ferkin, for example, found that males can behave in three ways if the SCI increases:

1. They do what the model predicts.
2. They do the exact opposite.
3. They invest a similar amount of sperm during each copulation no matter what.

Yes, it gets confusing. Life is diverse in many aspects and so are the adaptations to various situations, so let’s look at some examples. This time I’ll focus on mammals, who differ from other animals with sperm competition in that mammalian females don’t store sperm in their reproductive tract for long periods of time like birds or insects do.

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Randy Sheep

Male Soay sheep (Ovis aries) engage in fights where the size of their horns determines dominance, while females are highly promiscuous. Males with larger horns (i.e. consorts) get better access to females and are better at guarding them, which increases their mating success. Preston et al. (2003) proved that this is not so simple. It’s not the size of their horns that ultimately determines mating success. Instead, it’s the size of their testicles.

Consorts with larger testicles mate more often than do consorts with smaller ones, and a large part of consorts (22% in their study) doesn’t mate at all. Sheep don’t form harems, so the fact that a great number of females in a population are estrous synchronously makes it really hard for the consorts to keep an eye on every one of them - the randy weaker males have a chance to score. When this happens (SCI grows), testicle size (and, thus, sperm count) becomes more important in determining mating success than the size of their horns, because mate-guarding is now out of question.

So, then, if the number of receptive females is low enough for males to monopolize them, it’s profitable for males to grow larger and stronger and thus more capable of guarding them actively. This leads to sexual size dimorphism, but seems like it only works in mammals that have evolved external weapons, such as antlers or horns, but not in species that don’t have them, e.g. lemurs which do not exhibit sexual size dimorphism.

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Interference Type Sperm Competition

Dunham and Rudolf (2009) argue that copulatory plugs are effective in species with a short behavioral estrus, since the plugs last between 17 and 72 hours. The first male to mate with a given females plugs her reproductive tract and by the time the plug disintegrates, she’s no longer advertising her sexual receptivity. Such species should be more effective in finding a mate, since they're pressured by time, and should have well-developed accessory glands and proteins that partake on the making of copulatory plugs.

The existence of penile spikes, too, can be explained by passive mate-guarding – they’re found in species that utilize copulatory plugs and used as un-plugging devices. Alternatively, they can be used to scrape off the sperm of the early birds that already mated with the female in question or prolong the refraction period between copulations in females of a species that doesn’t have copulatory plugs.

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Scramble Type Sperm Competition

It is now clear that sperm competition leads to an increase in sperm numbers, but does it also affect sperm size? Sure, you can store more sperm if it’s smaller, but larger sperm does something better – it swims faster.

That’s exactly what Gomedio and Roldan (1991) found in rodents and primates. Apart from that, they found that sperm size could be adaptive in the context of sperm competition and that testis size is a reliable predictor of SCR. In species where females mate with many males, males produce longer sperm than the males of species in which females mate with only one male.

Twenty years later, Tourmente et al. conducted a research based on samples from 226 eutherian mammals. They, too, concluded that sperm size (together with sperm-head length) and testis size are reliable predictors of sperm competition success. An increase in relative testis size (and, thus, in sperm production) is a universal response to the degree of sperm competition, since many taxa rely on sperm quantity to successfully fertilize a female.

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Sperm Trains and Hooks

Sperm competition does not only affect sperm size and number - it can also lead to fascinating morphological adaptations, such as apical hooks in rodents.

It’s very important that all three features that the green-beard gene codes for work well, because if they don’t, rivals would help each other to reach the egg so the whole thing would miss 👏 the 👏 point 👏.

A comparative study based on muroid mice (Muroidea) found that mice with larger testes have sperm with more curved apical hooks, confirming that the hooks are adaptive in the context of sperm competition. Not all mice, however, use apical hooks to form sperm trains.

If house mouse (Mus musculus) sperm form trains, it’s probably just by accident – they swim slower than single sperm. Firman and Simmons (2009) found that, instead, the hooks could help them save energy. The timeframe between copulation and ovulation in house mice can be up to 8 hours long and if you’re a tiny sperm floating around for hours waiting to be able fulfil your mission, you’ll probably get dead tired. The lifespan of sperm is positively correlated with estrus length and Firman and Simmons further developed this statement by stating finding that estrus length together with body length and testis size are positively correlated with the degree of apical hook curvature, as the number of copulations increases with estrus length and sperm competition is therefore more intensive. Surely, if there’s more competition, you better sharpen your hook! A team of Czech scientists also found that variation in apical hook length decreases with increasing sperm competition, suggesting a stabilizing selection.

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Suicidal Reproduction

The final phenomenon I think is worth mentioning when we discuss sperm competition in mammals is semelparity – synchronized suicidal reproduction. It’s a life history strategy that maximizes reproduction so much that semelparous males die after their first reproductive event - they’re programmed to die after a single mating season. If we want truly explicit examples of semelparous mammals, we must visit Australia or Papua New Guinea.

There are at least 3 genera of dasyurid (Dasyuridae) marsupials the males of which all die after their first reproductive event because of a corticosteroid feedback loop - Antechinus, Dasykaluta and Phascogale.

Similarly to the sheep I mentioned earlier, these monestrous (not to be confused with monstrous) dasyurids have synchronous estrus – males are unable to monopolize females because the entire population is sexually receptive at the same time. This intensifies male competition at the expense of post-mating survival. Species in which males synchronously die after mating have larger testis size than males of species that also have low post-mating survival, but without the synchronous immune collapse, again supporting the notion that semelparity gives these genera an advantage in sperm competition. Suicidal reproduction is adaptive even though it causes death.

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The Microscopic Fight for Paternity

There are fascinating events occurring beyond what we can see with the naked eye. Sperm competition often resembles a microscopic war. Sometimes it’s the females who suffer, e.g. by getting their reproductive tract plugged or by losing on their attractiveness, in other cases it’s the males who pay the ultimate price to ensure paternity – death. We can be thankful that our ancestors took a more peaceful evolutionary path to the kind of sex we can all enjoy today by ditching the genes that coded for the production of penile spikes. Yup, we almost had them, too.

VOCABULARY

Common name:	Soay sheep
Scientific name:	Ovis aries
Phylum:	Chordata
Class:	Mammalia
Order:	Artiodactyla
Family:	Bovidae
Scientific reading:

Common name:	Loris
Subfamily:	Lorinae
Phylum:	Chordata
Class:	Mammalia
Order:	Primates
Family:	Lorisidae
Scientific reading:

Common name:	Guinea pig
Scientific name:	Cavia porcellus
Phylum:	Chordata
Class:	Mammalia
Order:	Rodentia
Family:	Caviidae
Scientific reading:

Common name:	Wood mouse
Scientific name:	Apodemus sylvaticus
Phylum:	Chordata
Class:	Mammalia
Order:	Rodentia
Family:	Muridae
IUCN status:	Least concern
Population trend:	Stable
Scientific reading:

Common name:	House omuse
Scientific name:	Mus musculus
Phylum:	Chordata
Class:	Mammalia
Order:	Rodentia
Family:	Muridae
IUCN status:	Least concern
Population trend:	Stable
Scientific reading:

Common name:	Broad-footed marsupial mouse
Genus:	Antechinus
Phylum:	Chordata
Class:	Mammalia
Order:	Dasyuromorphia
Family:	Dasyuridae
Scientific reading:

Common name:	Kaluta
Genus:	Dasykaluta
Phylum:	Chordata
Class:	Mammalia
Order:	Dasyuromorphia
Family:	Dasyuridae
Scientific reading:

Genus:	Phascogale
Phylum:	Chordata
Class:	Mammalia
Order:	Dasyuromorphia
Family:	Dasyuridae
Scientific reading: