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The social shape of sperm: Using an integrative machine-learning approach to examine sperm ultrastructure and collective motility

Kristin A. Hook, Qixin Yang, Leonard Campanello, Wolfgang Losert, Heidi S. Fisher

Preprint posted on 7 December 2020 https://www.biorxiv.org/content/10.1101/2020.12.05.413120v1

Article now published in Proceedings of the Royal Society B: Biological Sciences at http://dx.doi.org/10.1098/rspb.2021.1553

The hidden life of sperm: link between ultrastructure and collective behaviour

Selected by Mariana De Niz

Categories: cell biology

Background

Sperm cells have undergone extensive evolutionary modifications, and are one of the most morphologically diverse cell types in nature. They also display great variation especially among mammals, where sperm cells have significant modifications in their compartmentalized design, particularly the size and shape of the head. Identifying and quantifying informative morphological features in sperm cells, and their functional significance, has been an ongoing challenge across taxa. Some hypotheses on the functions and morphology (size and shape) of the sperm head include relevance in hydrodynamics, swimming performance, and collective behaviour. A remarkable yet relatively rare behavioural variation predicted to be associated to the head shape, includes the formation of collective groups that swim together, for motility or transport, through the female reproductive tract. In mice of the genus Peromyscus, a large natural variation of sperm traits is observed, thus offering a unique opportunity to influence of the sperm head shape on aggregating behaviour. In their work, Hook et al (1) use machine learning and traditional morphometric approaches to investigate if and how the Peromyscus sperm head shape associates with collective sperm behaviour.

Figure 1. Morphological features of Peromyscus sperm, including representative sperm heads for each species, and features measured in the manual sperm head analysis. (From Ref. 1).

Key findings and developments

Sperm head morphology across focal species of Peromyscus. The authors began by determining morphological and behavioural traits of sperm (including numbers of cells and aggregates) obtained via manual measurements among P. maniculatus, P. eremicus, P. polionotus, P. gossypinus, P californicus and P. leucopus. They found that sperm heads are significantly different among the focal species of Peromyscus, despite their close evolutionary relationships. The most important morphological features identified automatically and manually were the head width, the head aspect ratio, and the head area.

Association between sperm aggregation and sperm head shape.

Using a fully-connected neural network, the authors found that among all the combinations of inputs, the network with head width and head area as the sole input, provided the best performance to predict sperm aggregation size. Within the inter-species analysis, and controlling for phylogenetic relatedness, the authors found that the elongation of the sperm head significantly associates with collective sperm movements observed in vitro. Species whose sperm feature relatively wider heads aggregate more often and form larger groups. These associations were however, not observed for head length, head area, midpiece length, flagella length, or head-to-flagella ratio. These findings support the theoretical prediction that an adhesive region around the equatorial region of the sperm head mediates these unique interactions.

What I like about this preprint

I have a deep interest in flagellates and their dynamic features both on their own, collective, and within fluids. I find the fundamental question being addressed in this work, of great interest.

References

  1. Hook, et al, The social shape of sperm: Using an integrative machine-learning approach to examine sperm ultrastructure and collective motility, bioRxiv, 2020.

 

Posted on: 22 December 2020

doi: https://doi.org/10.1242/prelights.26603

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Author's response

Heidi Fisher shared

Open questions

1.In your work you chose members of the Peromyscus genus, and you mention that aggregation is very rare in other mammalian species. Why do you think aggregation happens in the rare occasions that it does, in other mammalian species?

Yes, we know it occurs in a number of different species, including woodmice, lab mice and lab rats, but also in guinea pigs, opossums, echidna, etc. However, it is not necessarily beneficial in all these species. For example, in lab mice, sperm will form clumps in certain environments but it significantly reduces their motility. Peromyscus maniculatus, the deer mouse, is particularly interesting because not only do sperm form aggregates that improve their swimming velocity, but they also do so selectively – they preferentially group with sperm from the same male over sperm from a rival, even if that rival is their own brother (Fisher & Hoesktra 2010, Nature).

 

2.If you analysed collective behaviours under flow, would the associations you found in your work here, differ?

That’s a great question and one we have not tackled yet, but are eager to try. My expectation is that the species that produce sperm that swim faster as aggregates in highly viscous environments are the same ones that would swim faster under flow, but at this point, it is just a guess.

 

3.Did sperm density and space constraints influence their probability of aggregating?

Density is absolutely important, and we took a lot of time to control for it in our experiments (and again statistically in our analysis). It makes sense that if there are more cells nearby, then there is greater opportunity for sperm to bump into another and form a group, and we see evidence of this in the lab. In terms of space influencing aggregation, to a certain extent that is important, but the cells are so small in comparison to the chamber slides we use in the experiments that it is not an issue here.

 

4.Is it possible to study sperm behaviour in a natural fluid and a natural organ (ie, either within the male reproductive system, or upon entry into the female reproductive system), under physiological speed and pressure, to observe whether differences exist between species, and how sperm motility and collective behaviours are influenced by these environments?

Yes and no. Within the male reproductive system, no, because in Peromyscus, sperm form groups after they are released into the female tract. However, this not the case for all mammals that produce sperm aggregates; in the echidna and the opossum, for example, sperm groups and pairs assemble prior to ejaculation. Other researchers have imaged sperm groups within the female reproductive tract in lab mice. It is a big challenge but their elegant experiments gave an important and unique insight into how they groups move in a biologically relevant context (https://www.biorxiv.org/content/10.1101/2020.10.18.344275v1.article-metrics). In lab mice, however, sperm do not selectively form groups the same way that deer mice sperm do, so it would be especially exciting to repeat these experiments in Peromyscus.

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