How the sperm lost its tail: the evolution of aflagellate sperm

Abstract

The typical sperm is comprised of a head, midpiece and flagellum. Around this theme there is an enormous diversity of form--giant sperm, multi-flagellate sperm and also sperm that lack flagella entirely. Explaining this diversity in sperm morphology is a challenging question that evolutionary biologists have only recently engaged in. Nonetheless, one of the selective forces identified as being an important factor in the evolution of sperm form is sperm competition, which occurs when the sperm of two or more males compete to fertilize a female's ova. In species with a truly monandrous mating system, the absence of sperm competition means that the selection pressure on males to produce motile sperm may be relaxed. Potentially aflagellate sperm are less costly to produce, both in terms of energy and time. Thus, selection may therefore favour the loss of the sperm flagellum and any other motile mechanisms in monandrous taxa. A review of the literature revealed that 36 taxonomic groups, from red algae to fish, were found independently to have evolved aflagellate sperm. I review what is known about the mating systems of each of these taxa and their nearest sister taxa. A sister-group analysis using this information provided weak evidence suggesting that the evolution of aflagellate sperm could be linked to the removal of selective pressures generated by sperm competition.

Evolution and spermatogenesis

“…Loosening of the selective pressure by sperm competition does not necessarily equal monogamy (Morrow 2004). Other mechanisms of reducing or removing sperm competition could include self-fertilization, as has been shown for the hermaphroditic form of Dicemydae; or population dynamics-in the sea spiders Pycnogonum littorale, the male to female ratio has shifted, thus limiting the number of available males.…”

“…As adults only live for one day, there might simply not be enough time for female to remate, and thus reduced opportunity for sperm competition. Based on currently collected data, it appears that aflagellate spermatozoa have evolved independently at least 36 times across a wide range of taxa (Morrow 2004). In 19 of these cases, loss of flagellae correlates with loss of motility; however, in at least 10 of these examples an alternative mechanism has been employed and the sperm retains motility.…”

Hydrodynamics of the double-wave structure of insect spermatozoa flagella

“…Although the structure of many different spermatozoa has been examined, the rapid and divergent evolution in sperm morphology is not well understood [5,9]. Hydrodynamic considerations of the relationship between flagellar morphology and functional parameters such as the swimming speed may provide useful information for explaining the evolutionary divergence.…”

Mechanisms Underlying the Sperm Quality Advantage in Drosophila Melanogaster

“…Also, experiments controlling the number of sperm inseminated into females have found repeatable and/or heritable differences among males in ejaculate performance or the outcome of sperm competition (Martin et al 1974;Dziuk 1996;Birkhead et al 1999;Froman et al 2002). Sperm cells are the most diverse cell type known, exhibiting rapid and dramatic evolutionary divergence in form (Sivinski 1984;Baccetti 1986;Jamieson 1991;Pitnick et al 1995aPitnick et al , 2003Jamieson et al 1999;Morrow 2004), as expected of traits subject to intense sexual selection (Eberhard 1985;Andersson 1994). Although the evolution of sperm quality traits by postcopulatory sexual selection has been suggested numerous times (Roldan 1991;Roldan et al 1992;Gomendio and Roldan 1993;Eberhard 1996;Birkhead and Pizzari 2002;Pizzari and Birkhead 2002;Snook 2005), the adaptive significance of nearly all variation in sperm form is unknown.…”