Integration of Male Mating and Feeding Behaviors inCaenorhabditis elegans

Abstract

The Caenorhabditis elegans male must integrate various environmental cues to ensure proper execution of mating. One step of male mating, the insertion of the male copulatory spicules into its mate, requires UNC-103 ERG (ether-a-go-go-related gene)-like K ϩ channels. unc-103(lf) alleles cause males to protract their spicules spontaneously in the absence of mating cues. To identify proteins that work with UNC-103, we suppressed unc-103(lf) and isolated lev-11(rg1). LEV-11 (tropomyosin) regulates the spicules directly by controlling the male sex muscles and indirectly by controlling the pharyngeal muscles. lev-11-mediated suppression requires the pharyngeal NSM neurosecretory motor neurons; ablating these neurons in lev-11(rg1); unc-103(lf) males restores spontaneous spicule protraction. Additionally, unc-103-induced spicule protraction can be suppressed by reducing a pharyngeal-specific troponin T. These observations demonstrate that non-genitalia cells involved in feeding also mediate male sexual behaviors.

Cell Excitability Necessary for Male Mating Behavior inCaenorhabditis elegansIs Coordinated by Interactions Between Big Current and Ether-A-Go-Go Family K+ Channels

“…In C. elegans, EAG and BK channels also interact to downregulate sex muscle excitability when the young adult males undergo a period of starvation, presumably to direct the males' behavior from copulation and toward food acquisition (Gruninger et al 2006;LeBoeuf et al 2011). We previously reported that EAG K + channels play a prominent role during food deprivation (LeBoeuf et al 2007(LeBoeuf et al , 2011; here, we show that BK channels are also important.…”

“…In previous work, we demonstrated that starvation can suppress the excitability of the mating circuit in ERG-like K + channel/unc-103 mutants through enhanced compensation by EAG/egl-2 function (Gruninger et al 2006;LeBoeuf et al 2007LeBoeuf et al , 2011). Since we established that there is a genetic interaction between slo-1, egl-2, and unc-103, we asked whether food-deprived BK channel/slo-1 mutant males, like unc-103(0) animals, had a reduced frequency of the Prc phenotype via enhanced egl-2 compensation.…”

“…We starved males by picking them at the late L4 stage and placed them on NGM plates lacking their food source, E. coli OP50. Males develop normally under these starvation conditions (Gruninger et al 2006). After 18-22 hr, we scored whether the starved males displayed the spontaneous spicule protraction phenotype.…”

Diversity in Mating Behavior of Hermaphroditic and Male–Female Caenorhabditis Nematodes

“…Previous studies have shown that N2 C. elegans males insert their spicules into older, rather than younger, genetically paralyzed hermaphrodites (Garcia et al 2001;Garcia and Sternberg 2003;Gruninger et al 2006). However, the mutations that produce paralysis in hermaphrodites could additionally cause defective vulval musculature that disrupts the males' ability to insert their spicules.…”

FMRFamide-Like Neuropeptides and Mechanosensory Touch Receptor Neurons Regulate Male Sexual Turning Behavior inCaenorhabditis elegans

“…In wild-type males, a stereotypic behavioral sequence includes response to hermaphrodite contact (requiring male-specific ray neurons), backing along the mate's body, turning at the mate's head or tail (requiring the three most posterior pairs of rays and the male-specific serotonergic CP neurons), location of vulva (requiring the malespecific hook neurons), spicule insertion (requiring male-specific cholinergic neurons of the spicules and postcloacal sensilla), and sperm transfer into the mate's uterus (requiring the male-specific SPV spicule neurons) (Loer and Kenyon, 1993;Liu and Sternberg, 1995;Barr and Sternberg, 1999;Garcia et al, 2001). C. elegans male sexual behaviors are also regulated by components of the core nervous system: spicule protraction is modulated by the NSM neurosecretory head neurons, and sperm transfer requires input from the ventral nerve cord motor neurons (Gruninger et al, 2006;Schindelman et al, 2006).…”