Rapid genome shrinkage in a self-fertile nematode reveals sperm competition proteins

Abstract

To reveal impacts of sexual mode on genome content, we compared chromosome-scale assemblies of the outcrossing nematode Caenorhabditis nigoni to its self-fertile sibling species, C. briggsae. C. nigoni’s genome resembles outcrossing relatives, but encodes 31% more protein-coding genes than C. briggsae. C. nigoni genes lacking C. briggsae orthologs were disproportionately small and male-biased in expression. These include the male secreted short (mss) gene family, which encodes sperm surface glycoproteins conserved only in outcrossing species. Sperm from mss-null males of outcrossing C. remanei failed to compete with wild-type sperm, despite normal fertility in non-competitive mating. Restoring mss to C. briggsae males was sufficient to enhance sperm competitiveness. Thus, sex has a pervasive influence on genome content that can be used to identify sperm competition factors.

Genome structure predicts modular transcriptome responses to genetic and environmental conditions

“…We found that module M5 was unique in its sperm‐related gene enrichment. Its over‐representation of genes with phosphatase/kinase activity and glycogen metabolism, as well as rarity on the X chromosome and in operons, is consistent with studies in C. elegans (Albritton et al, ; Reinke & Cutter, ; Reinke et al, , ; Thomas et al, ; Wu, Go, & Samson, ; Yin et al, ). Sperm‐dependent fertility in C. briggsae appears to be especially sensitive to high temperature, with tropical and temperate genotypes differing in sensitivity (Poullet et al, ; Prasad et al, ).…”

“…Moreover, GO term enrichment in M5 indicates a prominent role of genes with phosphatase/kinase activity and glycogen metabolism (File ), including the orthologs of C. elegans gsp‐3/4 and aagr‐1 . Previous expression studies have reported male‐biased and sperm‐related genes to be enriched for genes with phosphatase/kinase GO terms (Reinke, Gil, Ward, & Kazmer, ; Thomas et al, ), and some glycoproteins play crucial roles in sperm competitiveness in C. briggsae (Yin et al, ). Sperm fertility is known to show temperature sensitivity differently between the AF16 and HK104 genotypes of C. briggsae (Poullet et al, ; Prasad et al, ).…”

Comparative genomics of 10 newCaenorhabditisspecies

“…A comparison of the genomes of the closely related sister taxa C. nigoni and C. briggsae revealed that the genome of C. briggsae has undergone extensive contraction after the evolution of hermaphroditism, which has largely been driven by loss of genes with male‐biased expression (Yin et al. ).…”

“…; Yin et al. ). C. briggsae appears to have undergone extensive genome contraction after the evolution of hermaphroditism compared to its gonochoristic sister C. nigoni .…”

“…; Yin et al. ). Comparisons between genomes of hermaphroditic species such as C. elegans and their outcrossing relatives have exposed the genomic consequences of a switch in reproductive mode from gonochorism to autogamous hermaphroditism, including changes in overall genome structure, gene structure, and protein‐coding gene content (Thomas et al.…”