Abstract
BackgroundReproductive isolation is a defining characteristic of populations that represent unique biological species, yet we know very little about the gene expression basis for reproductive isolation. The advent of powerful molecular biology tools provides the ability to identify genes involved in reproductive isolation and focuses attention on the molecular mechanisms that separate biological species. Herein we quantify the sterility pattern of hybrid males in African Clawed Frogs (Xenopus) and apply microarray analysis of the expression pattern found in testes to identify genes that are misexpressed in hybrid males relative to their two parental species (Xenopus laevis and X. muelleri).Methodology/Principal FindingsPhenotypic characteristics of spermatogenesis in sterile male hybrids (X. laevis x X. muelleri) were examined using a novel sperm assay that allowed quantification of live, dead, and undifferentiated sperm cells, the number of motile vs. immotile sperm, and sperm morphology. Hybrids exhibited a dramatically lower abundance of mature sperm relative to the parental species. Hybrid spermatozoa were larger in size and accompanied by numerous undifferentiated sperm cells. Microarray analysis of gene expression in testes was combined with a correction for sequence divergence derived from genomic hybridizations to identify candidate genes involved in the sterility phenotype. Analysis of the transcriptome revealed a striking asymmetric pattern of misexpression. There were only about 140 genes misexpressed in hybrids compared to X. laevis but nearly 4,000 genes misexpressed in hybrids compared to X. muelleri.Conclusions/SignificanceOur results provide an important correlation between phenotypic characteristics of sperm and gene expression in sterile hybrid males. The broad pattern of gene misexpression suggests intriguing mechanisms creating the dominance pattern of the X. laevis genome in hybrids. These findings significantly contribute to growing evidence for allelic dominance in hybrids and have implications for the mechanism of species differentiation at the transcriptome level.
Highlights
Biological species remain cohesive by a lack of gene flow between interspecific populations and the mechanisms that maintain this pattern are manifest by various forms of reproductive isolation
If hybrid male Xenopus are sterile due to phenotypic defects associated with spermatogenesis, we predict that characteristics of sperm quality should be different in hybrids compared to the parental species
We tested this hypothesis by injecting males with human chorionic gonadotropin hormone to assay the effect of hormone induced stimulation on spermatogenesis in hybrids and the two parental species and compared sperm characteristics of these injected males with uninjected sexually mature males
Summary
Biological species remain cohesive by a lack of gene flow between interspecific populations and the mechanisms that maintain this pattern are manifest by various forms of reproductive isolation. Much work, using mainly forward genetic approaches, has focused on the genetic basis of postzygotic reproductive isolation and Haldane’s rule These studies have provided support for both dominance effects and faster male evolution as the main mechanisms generating Haldane’s rule; only recently have studies focused on gene expression as related to sterile hybrids and this opens a new avenue towards understanding the proximate causes of reproductive isolation [2,3,4,5,6,7,8,9,10,11,12]. The broad pattern of gene misexpression suggests intriguing mechanisms creating the dominance pattern of the X. laevis genome in hybrids These findings significantly contribute to growing evidence for allelic dominance in hybrids and have implications for the mechanism of species differentiation at the transcriptome level
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