Academic journal article Genetics

Reproductive Isolation in Hybrid Mice Due to Spermatogenesis Defects at Three Meiotic Stages

Academic journal article Genetics

Reproductive Isolation in Hybrid Mice Due to Spermatogenesis Defects at Three Meiotic Stages

Article excerpt

ABSTRACT

Early in the process of speciation, reproductive failures occur in hybrid animals between genetically diverged populations. The sterile hybrid animals are often males in mammals and they exhibit spermatogenic disruptions, resulting in decreased number and/or malformation of mature sperms. Despite the generality of this phenomenon, comparative study of phenotypes in hybrid males from various crosses has not been done, and therefore the comprehensive genetic basis of the disruption is still elusive. In this study, we characterized the spermatogenic phenotype especially during meiosis in four different cases of reproductive isolation: B6-ChrXMSM, PGN-ChrXMSM, (B6 3 Mus musculus musculus-NJL/Ms) F1, and (B6 3 Mus spretus) F1. The first two are consomic strains, both bearing the X chromosome of M. m. molossinus; in B6-ChrXMSM, the genetic background is the laboratory strain C57BL/6J (predominantly M. m. domesticus), while in PGN-ChrXMSM the background is the PGN2/Ms strain purely derived from wild M. m. domesticus. The last two cases are F1 hybrids between mouse subspecies or species. Each of the hybrid males exhibited cell-cycle arrest and/or apoptosis at either one or two of three distinct meiotic stages: premeiotic stage, zygotene-to-pachytene stage of prophase I, and metaphase I. This study shows that the sterility in hybrid males is caused by spermatogenic disruptions at multiple stages, suggesting that the responsible genes function in different cellular processes. Furthermore, the stages with disruptions are not correlated with the genetic distance between the respective parental strains.

WHEN animals from genetically diverged populations hybridize, complete or partial sterility is often observed in the F1 hybrids or in their descendants. This phenomenon belonging to postzygotic reproductive isolation accelerates irreversible genetic divergence by preventing free gene flow across the two diverging populations, and thereby plays a pivotal role in speciation. Sexual dimorphism is a general feature of reproductive isolation (Wu and Davis 1993; Laurie 1997; Orr 1997; Kulathinal and Singh 2008). In mammals, impairment is much more severe in males than in females, and in general the heterogametic sex is more sensitive to interspecific and intersubspecific genetic incompatibility. This phenomenon is well known as Haldane's rule (Haldane 1922; Laurie 1997; Orr 1997).

In many animals, the reproductive isolation is caused by spermatogenic disruptions characterized by reduced number of germ cells and small testis size. These animals include Drosophila (Joly et al. 1997), stickleback fish Pungitius (Takahashi et al. 2005), caviomorph rodent Thrichomys (Borodin et al. 2006), house musk shrew Suncus (Borodin et al. 1998), wallaby Petrogale (Close et al. 1996), and genus Mus (Forejt and Iványi 1974; Matsuda et al. 1992; Hale et al. 1993; Yoshiki et al. 1993; Kaku et al. 1995; Gregorova' and Forejt 2000; Elliott et al. 2001, 2004; Good et al. 2008). Although reproductive isolation by spermatogenic impairment is a well-known phenomenon, its underlying genetic mechanism and molecular basis have remained elusive. The Dobzhansky-Muller model, which infers that hybrid sterility or inviability is caused by deleterious epistatic interactions between nuclear genes derived from their respective parent species or subspecies (Dobzhansky 1936;Muller 1942), is widely accepted in animals and plants and is also applicable to the sterility of hybrid animals in F2 or backcross generations, so-called hybrid breakdown, in which the genes causing postzygotic reproductive isolation are partially recessive (Orr 2005).

The genetic incompatibility between house mouse subspecies is an ideal animal model for studying the early stage of speciation. Two subspecies of mouse, Mus musculus domesticus and M. m. musculus, diverged from their common ancestor 0.3-1.0 MYA (Yonekawa et al. 1980; Moriwaki 1994; Bonhomme and Gue'net 1996; Boursot et al. …

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