The tailored sperm cell

Abstract

Sperm are ubiquitous and yet unique. Genes involved in sexual reproduction are more divergent than most genes expressed in non-reproductive tissues. It has been argued that sperm have been altered during evolution more than any somatic cell. Profound variations are found at the level of morphology, motility, search strategy for the egg, and the underlying signalling mechanisms. Sperm evolutionary adaptation may have arisen from sperm competition (sperm from rival males compete within the female's body to fertilize eggs), cryptic female choice (the female's ability to choose among different stored sperm), social cues tuning sperm quality or from the site of fertilization (internal vs. external fertilization), to name a few. Unquestionably, sperm represent an invaluable source for the exploration of biological diversity at the level of signalling, motility, and evolution. Despite the richness in sperm variations, only a few model systems for signalling and motility have been studied in detail. Using fast kinetic techniques, electrophysiological recordings, and optogenetics, the molecular players and the sequence of signalling events of sperm from a few marine invertebrates, mammals, and fish are being elucidated. Furthermore, recent technological advances allow studying sperm motility with unprecedented precision; these studies provide new insights into flagellar motility and navigation in three dimensions (3D). The scope of this review is to highlight variations in motile sperm across species, and discuss the great promise that 3D imaging techniques offer into unravelling sperm mysteries.

Keywords: Chemotaxis; Flagellar beat; Klinotaxis; Sperm morphology; Steering.

Fig. 1

Exemplary variations in sperm design found in nature. a Sperm cell from the sea urchin Arbacia punctulata. The coarse overall morphology is found for many animal species. b The crawling sperm from the nematode Ascaris suum (picture courtesy of Dr. S. Sepsenwol). c The longest sperm known, from the fly Drosophila bifurca (picture courtesy of Dr. R. Dallai). Drosophila sperm with a shape similar to that of ball of wool is emanating from the last portion of the deferent duct. d–f sperm from different plants: Conocephalum conicum (d; biflagellated), Equisetum hyemale [e; with at least 80 flagella; (Renzaglia et al. 2002)], and Cycas revoluta (f; about 1000ths flagella). Reprinted with permission from (Renzaglia and Garbary 2001) and (Takaso et al. 2013). g, h Sperm can display profound variations in morphology even within the same class. Sperm from two passerine birds: the Eurasian bullfinch Pyrrhula pyrrhula (g) and the House sparrow Passer domesticus (h). Reprinted with permission from (Birkhead and Immler 2007)

Fig. 2

Exemplary axonemal structures found in sperm. a schematic diagram of a cross-section from a canonical 9 + 2 axonemal structure. View from the head towards the flagellar tip. Nine microtubule doublets (with subtubules A and B) are arranged cylindrically around an additional pair of microtubule singlets located at the centre. Two dynein arms (green) containing different subsets of dynein motors are attached to subtubule A and point towards the next B-tubule of the neighbour microtubule doublet in a clockwise direction (green). Dynein motors, fuelled by ATP, move adjacent microtubule doublets along the axis of the axoneme. Microtubule sliding is thought to be transformed into bending by mechanical constraints produced by their attachment to the basal body, nexin links (blue) (Lin et al. 2012), or clustering of motor activity (Movassagh et al. 2010). Radial spokes (red) connect the nine doublets in the periphery with the inner microtubule pair and associated filaments (grey). This complex is thought to orchestrate microtubule activity (Wargo and Smith 2003). b Flagellar cross-section from the sea urchin Arbacia punctulata with the canonical 9 + 2 structure. c Cross-section of the aberrant axoneme from the fly Sciara coprophila displaying its spiral shape. The axoneme is composed of 60–90 doublets, each one associated with a singlet or accessory microtubule. Subtubule A has two dynein arms (Jamieson et al. 1999). d Flagellar cross-section from the fly Drosophila bifurca. The axoneme and the two large mitochondrial derivatives can be seen. e Magnified detail from panel d displaying the characteristic 9 + 9 + 2 axoneme from insects. An accessory tubule (green) with its corresponding arms (red), a microtubule doublet (yellow), and the central pair (violet) have been labelled for clarity. Images are courtesy of Drs. S. Irsen (b) and R. Dallai (c–e)

Fig. 3

Recent advances in 3D sperm motility. a–c 3D reconstruction of the flagellum from malaria sperm. Flagella display a left (a) or right (b) handedness. The spatiotemporal map of chirality (c) shows propagating waves of alternate handedness across the flagellum. d 3D swimming path of a freely moving sperm cell from the sea urchin A. punctulata. Sperm swim along a helical path. From the motion of the sperm head, the flagellar beat plane can be inferred. Helix axis is shown in red. Two best-fitting planes along the path and the direction normal to them are shown in grey and blue, respectively. Time is color-coded along the path (see corresponding colorbar). e Swimming path of a sperm cell navigating in a chemical gradient. The axis of symmetry of the gradient is indicated by a grey line at the center. The cell approaches the gradient following a regular helical path (1). The helical axis bends smoothly during chemotaxis (2). Smooth helix alignment is interrupted by abrupt steering events (indicated by red cones). Strong alignment events occur when smooth alignment does not suffice to keep up-gradient swimming. f Rose plot of alignment events showing the changes in direction of the helical axis with respect to the parallel (${\mathrm{\nabla }}_{||}c$) and perpendicular (${\mathrm{\nabla }}_{\perp }c$) gradient components. Alignment of the helical axis is not random but scatters around the perpendicular gradient component, showing that the helical axis bends deterministically to align with the gradient direction

Fig. 4

Sperm vs. bacterial navigation paradigm. a, Bacteria like Escherichia coli, use a navigation strategy that is adapted for small cells with high rotational diffusion that randomizes swimming direction. The strategy followed consists into alternation between straight swimming (runs), and stochastic changes in direction (tumbles). For chemotaxis, the duration of runs is extended when swimming up the chemical gradient. The interval between runs is about 1 s, which is shorter than the time at which cell orientation is fully randomized by rotational diffusion (Berg 1993). b Large cells like sperm are less prone to rotational diffusion and thus have a longer swimming persistence, which allows for a deterministic search strategy. At rest, sea urchin sperm swim along circles (near a wall) or helical paths (in 3D). Both swimming paths are characterized by a periodic component. When immersed in a chemical gradient, the periodic component of swimming results in periodic stimulation of the cell. Periodic stimulus is translated into deterministic steering by simply producing a periodic modulation of the path curvature (in 2 and 3D) and path torsion (in 3D) (Alvarez et al. ; Jikeli et al. 2015). Chemical gradient is shown in shades of blue