Marine fish spermatozoa: racing ephemeral swimmers

Abstract

After a long period of spermatogenesis (several weeks to months), marine fish spermatozoa are delivered at male spawning in seawater (SW) at the same time as ova. In some fish species, as the ova micropyle closes quickly after release, these minute unicells, the spermatozoa, have to accomplish their task of reaching the micropyle within a very brief period (several seconds to minutes), for delivery of the haploid male genetic information to the ova. To achieve this goal, their high-performance motile equipment, the flagellum, must fully activate immediately on contact with the SW and then propel the sperm cell at an unusually high initial velocity. The cost of such 'hyperactivity' is a very rapid consumption of intracellular ATP that outstrips the supply. The spermatozoa become rapidly exhausted because mitochondria cannot compensate for this very fast flagellar energy consumption. Therefore, any spermatozoon ends up with two possibilities: either becoming exhausted and immotile or reaching the egg micropyle within its very short period of forward motility (in the range of tens of seconds) before micropyle closure in relation to both contact of SWand cortical reaction. The aim of the present review is to present step by step the successive events occurring in marine fish spermatozoa from activation until their full arrest of motility. The present knowledge of activation mechanisms is summarized, as well as a description of the motility parameters characterizing the motility period. As a complement, in vitro results on axonemal motility obtained after demembranation of flagella bring further understanding. The description of the sperm energetic content (ATP and other high energy compounds) and its evolution during the swimming period is also discussed. A general model aiming to explain all the successive cellular events occurring immediately after the activation is presented. This model is proposed as a guideline for understanding the events governing the sperm lifespan in the marine fish species that reproduce through external fertilization.

Vitrification Technique - New Possibilities for Male Gamete Low-Temperature Storage

“…During spermatogenesis, sperm cells are prepared for accomplishing their fertilizing task for which they need to fully exploit their swimming ability immediately and as fast as possible in order to encounter the egg. The initial velocity is very high at activation, but motility duration lasts for periods ranging only 40 s to 20 min as an energetic consequence of the high velocity (Cosson et al 2008). As possible to see the fish spermatozoa are much different from mammalian one.…”

“…The fish sperm cells are homogenous; all spermatozoa can be activated at the same time and then swim with very similar characteristics at a certain time point post-activation. In many fish species, the flagellum is 50-60 mm long with a ribbon shape (presence of fins) instead of cylindrical; thus, the flagellum appears brighter by dark-field microscopy, allowing clear visualization of wave shapes (Cosson et al 2008). Just for knowledge, the head of investigated us rainbow trout spermatozoa is ovoid-shaped, measuring about 3 x 1.3 µm in diameter and possess any acrosome.…”

Aquaporin3 is a sperm water channel essential for postcopulatory sperm osmoadaptation and migration

“…Studies in fish indicated that environmental osmotic changes trigger sperm motility [1,2]. Interestingly, in most mammalian species examined, the sperm journey from the male to female reproductive tract also experiences a natural osmotic decrease [3,4], implicating that an osmotic stress response upon ejaculation is evolutionarily conserved for normal sperm function.…”

Biophysics of Fish Sperm Flagellar Movement: Present Knowledge and Original Directions

“…Sperm velocity represents a global combination of several parameters such as head dimension (diameter of head), beat frequency, length of flagellum and physical parameters of wave propagation like wave length and amplitude [43], which contributes differentially to energetic exhaustion. Velocities of spermatozoa are greatest immediately after activation [4], for example, in halibut 150-180 μm/s [81,82], in fugu 160 μm/s [83], in cod 65-100 μm/s [84] or 130 μm/s [64], in hake 130 μm/s [64,85], in tuna 215-230 μm/s [86], in turbot 220 μm/s [70,87] and in sea bass 120 μm/s (straight line velocity) [69,88]. High initial velocity leads to shortened total duration of motility, because fish spermatozoa mostly rely on their preaccumulated energy store for operating their propulsive motors [4,9].…”

“…Sperm migrating in high viscosity fluids commonly exhibits larger numbers of waves though of lower amplitudes [86,107]. Thus, an increase in viscosity by addition of viscous compounds in the swimming medium actually leads to a lowering of propulsive velocity of the sperm [86].…”