Abstract
Systematic characterization of ẖybrid incompatibility (HI) between related species remains the key to understanding speciation. The genetic basis of HI has been intensively studied in Drosophila species, but remains largely unknown in other species, including nematodes, which is mainly due to the lack of a sister species with which C. elegans can mate and produce viable progeny. The recent discovery of a C. briggsae sister species, C. nigoni, has opened up the possibility of dissecting the genetic basis of HI in nematode species. However, the paucity of dominant and visible marker prevents the efficient mapping of HI loci between the two species. To elucidate the genetic basis of speciation in nematode species, we first generated 96 chromosomally integrated GFP markers in the C. briggsae genome and mapped them into the defined locations by PCR and Next-Generation Sequencing (NGS). Aided by the marker, we backcrossed the GFP-associated C. briggsae genomic fragments into C. nigoni for at least 15 generations and produced 111 independent introgressions. The introgression fragments cover most of the C. briggsae genome. We finally dissected the patterns of HI by scoring the embryonic lethality, larval arrest, sex ratio and male sterility for each introgression line, through which we identified pervasive HI loci and produced a genome-wide landscape of HI between the two nematode species, the first of its type for any non-Drosophila species. The HI data not only provided insights into the genetic basis of speciation, but also established a framework for the possible cloning of HI loci between the two nematode species. Furthermore, the data on hybrids confirmed Haldane’s rule and suggested the presence of a large X effect in terms of fertility between the two species. Importantly, this work opens a new avenue for studying speciation genetics between nematode species and allows parallel comparison of the HI with that in Drosophila and other species.
Highlights
It is well known that many closely related species are able to mate with each other, but their hybrid progeny frequently die, become sterile or develop abnormally
To empower the use of this species pair in Hybrid incompatibility (HI) studies, we first created a collection of fluorescent markers over the C. briggsae genome to facilitate the directional introduction of the marker-associated C. briggsae genomic fragments into the C. nigoni background
The study provides an invaluable resource for the molecular cloning of HI loci between C. briggsae and C. nigoni, and permits comparative analysis of speciation genetics between nematode and other species
Summary
It is well known that many closely related species are able to mate with each other, but their hybrid progeny frequently die, become sterile or develop abnormally. If the allele that causes HI is recessive, the heterogametic hybrid progeny will manifest its full effects due to hemizygosity, whereas the homogametic hybrid progeny will not show such effects due to the compensation by a second copy of a wild-type allele This explanation, dubbed the dominance theory [7], has gained support from genetic studies of HI in both animal and plant species. The second factor is that, hybrid male sterile loci may accumulate faster than hybrid inviable or female sterile loci, because male-specific genes are thought to evolve faster as a consequence of sexual selection This idea is referred to as the fast-male theory [8]. The second empirical rule proposed to explain HI is called the large X effect, which states that the substitution of X chromosomal fragments produces more severe HI than the similar
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