Cellular geometry controls the efficiency of motile sperm aggregates

Abstract

<jats:p>Sperm that swim collectively to the fertilization site have been observed across several vertebrate and invertebrate species, with groups ranging in size from sperm pairs to massive aggregates containing hundreds of cells. Although the molecular mechanisms that regulate sperm–sperm adhesion are still unclear, aggregation can enhance sperm motility and thus offer a fertilization advantage. Here, we report a thorough computational investigation on the role of cellular geometry in the performance of sperm aggregates. The sperm head is modelled as a persistent random walker characterized by a non-trivial three-dimensional shape and equipped with an adhesive region where cell–cell binding occurs. By considering both, a simple parametric head shape and a computer reconstruction of a real head shape based on morphometric data, we demonstrate that the geometry of the head and the structure of the adhesive region crucially affects both the stability and motility of the aggregates. Our analysis further suggests that the apical hook commonly found in the sperm of muroid rodents might serve to shield portions of the adhesive region and promote efficient alignment of the velocities of the interacting cells.</jats:p>

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

“…Using an integrative methodical and analytical approach that combines traditional morphometry and machine learning, we characterized sperm head shape variation and investigated its role in collective motility in the Peromyscus lineage. Our results support the theoretical predictions that sperm with a smaller head aspect ratio (i.e., relatively wider head), are more likely to aggregate and to form larger aggregates when they do [34,36]. Moreover, we find that variation in sperm head dimensions across these captive species is consistent with previously recorded morphological diversity observed from museum samples [35], supporting the use of high-throughput morphometric methods.…”

“…A prediction that follows this hypothesis is that species that produce sperm aggregates should have sperm with shorter flagella, but we found no evidence for this prediction in Peromyscus, nor was it observed in diving beetles [29]. Furthermore, sperm aggregates that conjoin in a head-to-head orientation, such as in Peromyscus, are wider, not longer, than a single cell, which will differentially impact the additive force from the cells and their motility [34,37]. Given the diverse mechanisms by which sperm conjugates form in other taxonomic groups [26,27], including in other rodents in which sperm form 'trains' by latching onto (which was not certified by peer review) is the author/funder.…”

“…found that in all but one species, over 90% of the sperm swam as solitary cells, despite the presence of the apical hook [31]. Together these studies serve to illustrate that the impact of the apical hook may be minimal or secondary to other morphological features or the shape of the sperm head in facilitating sperm aggregation [34].…”

“…Moreover, across the genus, all sperm are released as single cells, but some species produce sperm that loosely adhere to one another at their head region, forming sperm aggregates that vary in size [36,37] and in the relatedness of cells that associate with one another [30]. Theoretical models predict that the two-dimensional aspect ratio [36] and three-dimensional shape [34] of sperm heads in the deer mouse (Peromyscus maniculatus) facilitate their aggregation. Here we test this prediction across Peromyscus species by characterizing the complex and potentially subtle variation in sperm head shape from high resolution images, which we analyze using a combination of manual and automatic morphometric methods, and the size and proportion of aggregated sperm cells using live cell optical imaging.…”

Changes in group size during resource shifts reveal drivers of sociality across the tree of life

“…Improving our understanding of which benefits underlie sociality among extant species will allow us to test whether some benefits tend to drive the evolution of sociality, with other benefits accruing secondarily. In addition, this framework could be applied at the sub-organismal level, potentially explaining the group sizes of cellular aggregations such as sperm cells 144, 145 , erythrocytes and platelets 146–148 , and some immune cells 149–151 . Taking a high-level view of sociality across the tree of life, while abstracting away many of the finer details, may therefore be a powerful approach towards a deeper understanding of one of the major evolutionary transitions.…”