A Novel Approach Identifying Hybrid Sterility QTL on the Autosomes of Drosophila simulans and D. mauritiana

Abstract

When species interbreed, the hybrid offspring that are produced are often sterile. If only one hybrid sex is sterile, it is almost always the heterogametic (XY or ZW) sex. Taking this trend into account, the predominant model used to explain the genetic basis of F1 sterility involves a deleterious interaction between recessive sex-linked loci from one species and dominant autosomal loci from the other species. This model is difficult to evaluate, however, as only a handful of loci influencing interspecies hybrid sterility have been identified, and their autosomal genetic interactors have remained elusive. One hindrance to their identification has been the overwhelming effect of the sex chromosome in mapping studies, which could ‘mask’ the ability to accurately map autosomal factors. Here, we use a novel approach employing attached-X chromosomes to create reciprocal backcross interspecies hybrid males that have a non-recombinant sex chromosome and recombinant autosomes. The heritable variation in phenotype is thus solely caused by differences in the autosomes, thereby allowing us to accurately identify the number and location of autosomal sterility loci. In one direction of backcross, all males were sterile, indicating that sterility could be entirely induced by the sex chromosome complement in these males. In the other direction, we identified nine quantitative trait loci that account for a surprisingly large amount (56%) of the autosome-induced phenotypic variance in sterility, with a large contribution of autosome-autosome epistatic interactions. These loci are capable of acting dominantly, and thus could contribute to F1 hybrid sterility.

Incompatibility between Nuclear and Mitochondrial Genomes Contributes to an Interspecies Reproductive Barrier

“…Although DM incompatibilities were originally linked to interactions between nuclear genes, miscommunication between nuclear and mitochondrial genomes has been implicated in yeast (Lee et al, 2008), drosophila and other insects (Dickman and Moehring, 2013; Foley et al, 2013), fish (Bolnick et al, 2008; Niehuis et al, 2008) and in primate xenomitochondrial cybrid cell lines (Bayona-Bafaluy et al, 2005). Previous studies in drosophila found male-specific infertility associated with mitochondrial polymorphism (Clancy et al, 2011; Innocenti et al, 2011).…”

Hybrid sterility and evolution in Hawaiian Drosophila: differential gene and allele-specific expression analysis of backcross males

“…Genetic models have been developed that indicate that this type of fitness reduction may require at least two genetic changes-one from each species-but can be much more complex and be the result of multiple gene interactions (Johnson, 2000;Coyne and Orr, 2004). Multiple studies of HMS in the well-studied allopatric species pair Drosophila mauritiana and Drosophila simulans showed interactions of at least three genes or more (Johnson, 2000), and the identification of over 100 genes contributing to HMS on the X chromosome (Wu et al, 1996), as well as many genes on the autosomes (Tao et al, 2003;Araripe et al, 2010;Dickman and Moehring, 2013).…”

Identification and genetic analysis of a pervasive ‘needle-eye’ sperm phenotype in Drosophila sterile hybrid males

“…Furthermore, combining X and Y chromosomes from different species has been shown to result in sterility, regardless of the autosomal complement (e.g. between D. simulans and D. mauritiana : [ 54 , 55 ], indicating that some aspect of heteromorphic chromosomes themselves may be responsible for F 1 sterility. Likewise, in mice, the pseudoautosomal region involved in pairing X and Y chromosomes is strongly associated with hybrid sterility when X and Y are from different species [ 56 ].…”