Hybrid Breakdown Caused by Substitution of the X Chromosome Between Two Mouse Subspecies

Abstract

Hybrid breakdown is a type of reproductive failure that appears after the F2 generation of crosses between different species or subspecies. It is caused by incompatibility between interacting genes. Genetic analysis of hybrid breakdown, particularly in higher animals, has been hampered by its complex nature (i.e., it involves more than two genes, and the phenotype is recessive). We studied hybrid breakdown using a new consomic strain, C57BL/6J-XMSM, in which the X chromosome of C57BL/6J (derived mostly from Mus musculus domesticus) is substituted by the X chromosome of the MSM/Ms strain (M. m. molossinus). Males of this consomic strain are sterile, whereas F1 hybrids between C57BL/6J and MSM/Ms are completely fertile. The C57BL/6J-XMSM males showed reduced testis weight with variable defects in spermatogenesis and abnormal sperm head morphology. We conducted quantitative trait locus (QTL) analysis for these traits to map the X-linked genetic factors responsible for the sterility. This analysis successfully detected at least three distinct loci for the sperm head morphology and one for the testis weight. This study revealed that incompatibility of interactions of X-linked gene(s) with autosomal and/or Y-linked gene(s) causes the hybrid breakdown between the genetically distant C57BL/6J and MSM/Ms strains.

Investigating the Impact of a Curse: Diseases, Population Isolation, Evolution and the Mother’s Curse

“…Hybridization is characterized as the inbreeding between genetically divergent populations or species that many times results in different types of failure in reproduction [ 101 , 102 ]. Reduced fertility can be observed in F 1 hybrids, or reduced viability and fitness are present only in F 2 or later generation hybrids leading to the hybrid breakdown [ 102 ]. Hybrids have been studied for many years and Darwin’s observation on hybrid sterility is remarkable [ 103 , 104 ].…”

Hybrid breakdown in male reproduction between recently diverged Drosophila melanogaster populations has a complex and variable genetic architecture

“…In such cases alleles involved in an incompatibility may or may not be fixed within a population ( Turelli & Orr, 2000 ), and if they are recessive, isolation will typically only manifest in second generation or later hybrids of sexually reproducing diploids. Reproductive isolation of this kind is often termed “hybrid breakdown” and is a specific category of intrinsic postzygotic reproductive isolation ( Oka et al, 2003 ).…”

“…Investigation of hybrid breakdown and later generation BDMIs has received some attention in recent speciation literature, and is often pursued between closely related species (e.g., Breeuwer & Werren, 1995 ; Matsubara, 2020 ; Morgan et al, 2020 ; Oka et al, 2003 ; Renaut & Bernatchez, 2011 ). Examples of within-species models of reproductive isolation are more limited ( Koski et al, 2022 ; Pritchard & Edmands, 2013 ; Stelkens et al, 2015 ; White et al, 2012 ), yet in these few studies the existence of moderately strong isolating barriers among populations has been evidenced.…”