Abstract
Sex determination is a fundamentally important and highly diversified biological process, yet the mechanisms behind the origin of this diversity are mostly unknown. Here we suggest that the evolution of sex determination systems can be driven by a chromosomal inversion. We show that an XY system evolved recently in particular nine-spined stickleback (Pungitius pungitius) populations, which arose from ancient hybridization between two divergent lineages. Our phylogenetic and genetic mapping analyses indicate that the XY system is formed in a large inversion that is associated with hybrid sterility between the divergent lineages. We suggest that a new male-determining gene evolved in the inversion in response to selection against impaired male fertility in a hybridized population. Given that inversions are often associated with hybrid incompatibility in animals and plants, they might frequently contribute to the diversification of sex determination systems.
Highlights
Sex determination is a fundamentally important and highly diversified biological process, yet the mechanisms behind the origin of this diversity are mostly unknown
These chromosomes correspond to linkage group (LG) 12, which consists of chromosome (Chr) 12 and a part of Chr[7] in the three-spined stickleback (Gasterosteus aculeatus)[18], and the sex-determining gene is located in the G. aculeatus Chr[12] region[18,19], which is not involved in sex determination in G. aculeatus[20] or in the brook (Culaea inconstans) or four-spined stickleback (Apeltes quadracus)[15], phylogenetically close relatives of Pungitius[21]
Based on a global phylogenetic analysis of 25 Pungitius populations using 46 autosomal short tandem repeat (STR) loci and mitochondrial cytochrome b sequences, we identified nine highly divergent lineages, corresponding to P. tymensis (PT), Japanese Omono (JO), Japanese freshwater (JF), Japanese brackish-water (JB), western European (WE), eastern European (EE), eastern North American (EA), central North American (CA), and P. laevis (PL) lineages (Fig. 1, Supplementary Table 1, and Supplementary Data 1)
Summary
Sex determination is a fundamentally important and highly diversified biological process, yet the mechanisms behind the origin of this diversity are mostly unknown. Extensive theoretical studies have proposed several hypothetical models for the evolution of sex determination systems, such as genetic drift[4], pleiotropic benefits[4,5], sex ratio selection[6,7,8], and sexual antagonism[9,10,11]. Most of these models emphasize the importance of natural selection on fitness differences that are directly caused by, or indirectly associated with, a novel locus as a driving force promoting transitions in sex determination systems[12,13]. We suggest that a new XY sex determination system has evolved in response to selection for hybrid incompatibility caused by the chromosomal inversion
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