Evolution of the spermatozoon in muroid rodents

Abstract

In the rodent superfamily Muroidea, a model for the evolution of sperm form has been proposed in which it is suggested that a hook-shaped sperm head and long tail evolved from a more simple, nonhooked head and short tail in several different subfamilies. To test this model the shape of the sperm head, with particular emphasis on its apical region, and length of sperm tail were matched to a recent phylogeny based on the nucleotide sequence of several protein-coding nuclear genes from 3 families and 10 subfamilies of muroid rodents. Data from the two other myomorph superfamilies, the Dipodoidea and kangaroo rats in the Geomyoidea, were used for an outgroup comparison. In most species in all 10 muroid subfamilies, apart from in the Murinae, the sperm head has a long rostral hook largely composed of acrosomal material, although its length and cross-sectional shape vary across the various subfamilies. Nevertheless, in a few species of various lineages a very different sperm morphology occurs in which an apical hook is lacking. In the outgroups the three species of dipodid rodents have a sperm head that lacks a hook, whereas in the heteromyids an acrosome-containing apical hook is present. It is concluded that, as the hook-shaped sperm head and long sperm tail occur across the muroid subfamilies, as well as in the heteromyid rodents, it is likely to be the ancestral condition within each of the subfamilies with the various forms of nonhooked sperm heads, that are sometimes associated with short tails, being highly derived states. These findings thus argue against a repeated evolution in various muroid lineages of a complex, hook-shaped sperm head and long sperm tail from a more simple, nonhooked sperm head and short tail. An alternative proposal for the evolution of sperm form within the Muroidea is presented in the light of these data.

Loss of Zona Pellucida Binding Proteins in the Acrosomal Matrix Disrupts Acrosome Biogenesis and Sperm Morphogenesis

“…In contrast, loss of ZPBP2 results in decreased fecundity and subtle sperm head deformities that correspond to the discrete localization of ZPBP2 along the rostral ridge of spermatozoa. Since several muroid rodents (in superfamily Muroidea) with a variety of less prominent apical hook and nonhooked sperm heads exist in nature (6,7), the morphological changes of Zpbp2-null sperm are unlikely to be prohibitive to their fertilization potentials, thus suggesting that the reduced zona penetration is responsible for the decreased fecundity. In double-knockout mice, the effects of disrupted ZPBP1 preclude any appreciation of independent ZPBP2 function.…”

Changes in the curvature of sperm apical hooks in murine rodents

“…species where the male is not capable of guarding the female after copulation, it is advantageous to have cooperating sperm with long apical hooks that form trains. These species also have longer sperm tails (Breed 2005) and relatively larger testes (Roldan et al 1992;Breed & Taylor 2000). The movement of tails in the train is coordinated.…”

“…If the apical hook represents an ancestral trait in the murine rodents and its absence has been derived (Breed 2004(Breed , 2005, the sperm morphology and the associated mating systems may have followed different trends. The first is the tendency to monoandry (monogamy), i.e.…”

“…Positive correlation between relative testes weight and the sperm tail length has been associated with the phylogenetic relationship of individual species (Breed 2005;Breed & Taylor 2000;Roldan et al 1992). In some genera (groups), considerable interspecies differences in the relative testes weight and sperm size (tail length) have been found in phylogenetically closely related species (Breed & Taylor 2000).…”

Sperm morphology of the eurasian beaver, Castor fiber: An example of a species of rodent with highly derived and pleiomorphic sperm populations

“…However, in the rodent Superfamily Muroidea, which includes the common laboratory rats and mice in the Family Muridae, most species have a sperm head that is hook-shaped with a highly complex and asymmetrical acrosome and an elaborate cytoskeletal rostral projection, a perforatorium, and a long sperm tail attached to the lower concave surface of the sperm head (Retzius, 1909;Friend, 1936;Clermont et al, 1955;Bishop and Austin, 1957;Bishop and Walton, 1960;Lalli and Clermont, 1981;Breed, 2005). There are nevertheless a few species within this superfamily that have a highly derived sperm head shape that lacks an apical hook and in which the sperm tail is generally much shorter (Friend, 1936;Breed, 2004Breed, , 2005, with such divergent sperm morphology generally occurring in species that have relatively small testes.…”