Promiscuity Breeds Efficiency: Mouse Mating Systems Affect Sperm Sprints

Sperm is constant joke-fodder. From the opening credits of the movie "Look Who's Talking" to various Shakespeare passages, we humans never seem to tire of laughing at hordes of competitive little sperm powering past each other in the race towards their final destination. They're unbelievably tiny, simple entities, and yet the outcome of their performance is huge. Or perhaps we just stay fascinated by the dramatic fact that all of our lives began when one of those little guys won a race that has been going on since deep time. Aside from all of the off-color jokes and cartoons, though, research into what makes sperm successful is highly relevant to several areas of human medicine as well as reproductive science involving livestock and other species.

The idea that fertilization involves an “every man for himself” race between sperm is not necessarily accurate, however, especially for monogamous species in which a female only has one mate at a time. After all, a male organism will successfully reproduce himself if any one of his multitudes of sperm successfully reach an egg. Some mammals even have sperm with physical features that allow them to literally hook themselves together and travel in packs, combining the power of their flagella to surge along towards the finish line.

For example, behold, the sperm of the humble Peromyscus, a New World rodent genus that includes familiar species such as the deer mouse (P. maniculatus) and the Oldfield or beach mouse (P. polionotus). Peromyscus sperm actually include huge hook-type structures, which they use to latch onto each other and race towards their destinies in groups, peloton-style.


(From Fisher et al. 2014)

We know that species with more intense male-male competition experience higher degrees of sperm competition (this explains much of the difference in testes:body size ratios between different mammals). Mouse species within the genus Peromyscus exhibit a spectrum of mating systems, making this genus an especially interesting group for investigating effect of sperm aggregation on performance. For example, the deer mouse (P. maniculatus) is highly promiscuous: mating is essentially a free-for-all in this species. Both males and females have multiple partners within very brief periods of time, and multiple-paternity litters are common. On the other hand, the beach mouse (P. polionotus) is extremely monogamous. Their fidelity has even been confirmed by genetic testing (in contrast to many species that are socially “monogamous” and pair-bonded but still sneak around on the side).


Deer mouse (P. maniculatus)


Beach mouse (P. polionotus)

Despite their divergent mating systems, deer mice and beach mice have nearly identical sperm: it has characteristic hook-type structure on the head, which they use to link together into the aggregations mentioned above. This appears to work the same way in both species, and the sperm look extremely similar . . . and yet they experience highly disparate competitive environments.

A sperm from an individual male deer mouse will probably be in a much more dire situation as it races to outpace sperm from the female's other recent partners. The sperm from a monogamous beach mouse should, in theory, be able to “take it easier,” because all of the other sperm in the fertilization race come from the same individual. How do these behavioral differences at the organismal level affect the sperms' behavior and performance, and what does this teach us about sperm competition and/or cooperation?

A new study in the Proceedings of the Royal Society B addresses just these questions (Fisher et al. 2014). A group of researchers, led by Harvard University’s Dr. L. Mahadevan and Dr. Hopi Hoekstra, used mathematical models to predict how forming aggregations improves sperm performance: what is the optimal aggregation size, and how much of a performance boost (measured by average velocity--VSL--of sperm) does such an arrangement provide? They then used advanced imaging technology to test the model predictions and compare deer and beach mouse sperm performance.

The findings were fascinating: the models predicted that an aggregation of exactly seven sperm will achieve the best VSL. In other words, VSL performance increased as the number of sperm in a group increased from a singleton to an aggregation of seven, but additional sperm beyond the seventh caused decreases in VSL. Lucky seven wins. It is noteworthy that the optimal aggregation size didn’t achieve the highest VSL due to faster speeds, but because the physics of how the sperm link together seem to allow a group of seven to take the most direct (linear) path towards their target. In other words, it is linearity, rather than speed, that helps sperm to maximize their velocity.

(From Fisher et al. 2014)

(From Fisher et al. 2014)

(From Fisher et al. 2014)

(Click to embiggen for clarity; From Fisher et al. 2014)

So that's what the math tells us. But how do the model predictions hold up when we observe sperm behavior from real animals? The researchers tested this by examining sperm from both deer mice and beach mice, to observe both VSL and aggregation behavior.

The authors note that although there were individual differences within species (i.e., some males just have faster sperm than their conspecific brethren; every species has its studs), sperm group size still influenced VSL in both mouse species after individual differences were accounted for. In other words: the optimal aggregation size is the same for both species despite their differences in mating behavior. Physics is physics, after all, so it makes sense that similarly formed sperm would form aggregations with similar attributes for optimal performance.

There is a twist, however. Despite the fact that mice of both species achieve optimal sperm VSL when their sperm forms aggregations of seven, beach mice (the monogamous species) show significantly more variation in sperm group size than the promiscuous deer mice. Likewise, deer mice have sperm that travels much more linearly—ie, more efficiently—than the sperm of beach mice, probably because the beach mouse sperm fails to form optimal aggregations as often.


(From Fisher et al. 2014)

(Click to embiggen for clarity; From Fisher et al. 2014)

The take-home message of this study is incredibly interesting: Behavior at the organismal level significantly affects gamete behavior even in species that have virtually identical sperm. Beach mouse sperm and deer mouse sperm have the same optimal performance parameters, and yet the beach mouse sperm, facing less intense competition, just doesn't seem to be pressured enough to conform to those optimal conditions. Deer mouse sperm, on the other hand, is in a more “do or die” type scenario, and is much more likely to form highly competitive and efficient sperm aggregations. Despite being extremely similar in shape, this study demonstrates that sperm behavior at the cellular level reflects the competitive environment created by behavior at the organismal level.  Cool stuff, no?

The present study is extremely valuable for highlighting how basic physics and geometry interact with cellular morphology and organismal behavior to influence sperm behavior and/or success. In addition, it is an example of how quantitative models can be used to test predictions about evolution and selective processes in nature. It will be fascinating to see how hypotheses about competition at the gene level, rather than the individual level, can be worked into studies like this in the future.

Why should we care about all of this, as non-members of the esteemed Peromyscus group? Infertility issues as well as the need for effective contraception are both important and emotional topics for many people, as well as being lucrative parts of the health industry. Insights into the behavior of sperm are therefore of extreme interest to medical researchers and other stakeholders. Data on how species mating systems affect gamete behavior could also be useful for breeding programs for both domesticated and wild animals (the value/efficiency of captive breeding program for species conservation of mammals is a debate for another time and place, however). Clearly, this is a line of research with a wide variety of applications, and it will be interesting to follow similar experiments with other sets of mammalian species.
H. S. Fisher, L. Giomi, H. E. Hoekstra, & L. Mahadevan (2014). The dynamics of sperm cooperation in a competitive environment Proceedings of the Royal Society B arXiv: 1407.0666v1


Image credits

Phelps sperm cartoon

Peromyscus maniculatus

Peromyscus polionotus

Figures are all from Fisher et al. (2014)

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