Behaviors need to be tightly coordinated to occur at the appropriate time. We used the spicule protraction step of male mating behavior to uncover how this regulation is achieved at the molecular level. The male's spicules should only protract from their cloaca after the hermaphrodite vulva is penetrated. Many different components of the male circuit have to be coordinated to respond at the appropriate time. If elements of the circuitry regulating spicule protraction are disrupted, the males display a protraction constitutive (Prc) phenotype, whereby the copulatory spicule permanently protrudes from the male tail, rendering sperm transfer impossible. We identified the BK K+ channel
slo-1 as an important component regulating spicule protraction. 70% of males with an early nonsense mutation in
slo-1(
js379) display the Prc phenotype.
slo-1 is a calcium and voltage sensitive K+ channel that may help control the function of
egl-19 L-type Ca2+ channels in muscle. We show that two other K+ channels are involved in regulating
egl-19 in the male mating circuit, the ether-a-go-go related gene K+ channel
unc-103 and the ether-a-go-go K+ channel
egl-2. The
slo-1(
js379) phenotype can be reduced from 70% to 30% by removing
egl-2. This indicates that another molecule, possibly
unc-103, is up-regulated in the
slo-1(
js379)
egl-2(0) background and can compensate for the loss of both of these channels. A triple mutant knocking out
unc-103,
egl-2, and
slo-1 function causes 79% of males to protract their spicules, similar to
slo-1(
js379) alone. In addition, expressing a transgenic dominant negative allele of
unc-103 in the sex muscles of
slo-1(
js379)
egl-2(0) males results in 72% those males prematurely protracting their spicules. While
unc-103 can compensate for the loss of
slo-1 function when males are fed,
egl-2 compensates for
slo-1(lf) under starved conditions.
slo-1(
js379) and
slo-1(
js379)
egl-2(0) males are ~30% Prc when starved as they mature from L4s to adults. Sex-muscle specific expression of a mutant form of the
egl-2 K+ channel, which has an increased open probability, suppresses
slo-1(
js379)-induced Prc when the males are starved. Interestingly, under fed conditions, sex-muscle expressed
egl-2(gf) increases the instance of Prc in a
slo-1(
js379)
egl-2(0) background. This supports the hypothesis that
unc-103 function is up-regulated to compensate for the loss of
egl-2 and can also reverse some of the adverse effects of
slo-1(lf). We propose that the functions of the
slo-1,
unc-103, and
egl-2 K+ channels are balanced in the male sex muscles to achieve precise regulation of the timing of spicule protraction.