Evolution of sperm competition: Natural variation and genetic determinants of Caenorhabditis elegans sperm size

Abstract

Sperm morphology is critical for sperm competition and thus for reproductive fitness. In the male-hermaphrodite nematode Caenorhabditis elegans, sperm size is a key feature of sperm competitive ability. Yet despite extensive research, the molecular mechanisms regulating C. elegans sperm size and the genetic basis underlying its natural variation remain unknown. Examining 97 genetically distinct C. elegans strains, we observe significant heritable variation in male sperm size but genome-wide association mapping did not yield any QTL (Quantitative Trait Loci). While we confirm larger male sperm to consistently outcompete smaller hermaphrodite sperm, we find natural variation in male sperm size to poorly predict male fertility and competitive ability. In addition, although hermaphrodite sperm size also shows significant natural variation, male and hermaphrodite sperm size do not correlate, implying a sex-specific genetic regulation of sperm size. To elucidate the molecular basis of intraspecific sperm size variation, we focused on recently diverged laboratory strains, which evolved extreme sperm size differences. Using mutants and quantitative complementation tests, we demonstrate that variation in the gene nurf-1 - previously shown to underlie the evolution of improved hermaphrodite reproduction - also explains the evolution of reduced male sperm size. This result illustrates how adaptive changes in C. elegans hermaphrodite function can cause the deterioration of a male-specific fitness trait due to a sexually antagonistic variant, representing an example of intralocus sexual conflict with resolution at the molecular level. Our results further provide first insights into the genetic determinants of C. elegans sperm size, pointing at an involvement of the NURF chromatin remodelling complex.\n\n\n\nO_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=166 SRC=\"FIGDIR/small/501486v1_ufig1.gif\" ALT=\"Figure 1\">\nView larger version (166K):\norg.highwire.dtl.DTLVardef@1ff917org.highwire.dtl.DTLVardef@11a5e4corg.highwire.dtl.DTLVardef@250996org.highwire.dtl.DTLVardef@1989580_HPS_FORMAT_FIGEXP M_FIG C_FIG