Much of animal behavior is regulated to accomplish goals necessary for survival and reproduction. Little is known about the underlying motivational or drive states that are postulated to mediate such goal-directed behaviors. Here, we describe a mate-searching behavior of the Caenorhabditis elegans male that resembles the motivated behaviors of vertebrates. Adult C. elegans males, if isolated from mating partners, will leave the area of a food source and wander about their environment in an apparent search for a mate. When mating partners are present on the food source, males do not wander but remain with them. This behavior is sexually dimorphic for C. elegans and two additional male/hermaphrodite species studied; for these species, hermaphrodites leave food significantly slower than males. In contrast, for three male-female species examined, both males and females left food, in two cases with similar frequency, suggesting coordinate evolution of behavioral dimorphism with hermaphroditism. We use a quantitative behavioral assay to show that C. elegans male mate searching is regulated by signals from hermaphrodites and by physiological signals indicating nutritional and reproductive status. We identify genes in the serotonin, insulin, and sex determination pathways that affect the rate of mate searching. These genes may contribute to physiological and reproductive regulatory mechanisms. Our results establish C. elegans as a model genetic animal with a simple nervous system in which neural pathways leading to a motivated behavior may be genetically dissected.

Mutations inCaenorhabditis elegans gene mab-23 cause abnormal male tail morphology and abolish male fecundity but have no obvious effect in the hermaphrodite. Here we show that mab-23 encodes a DM (Doublesex/MAB-3) domain transcription factor necessary for specific aspects of differentiation in sex-specific tissues of the male. mab-23 is required for the patterning of posterior sensory neurons in the male nervous system, sex muscle differentiation, and morphogenesis of the posterior hypodermis, spicules, and proctodeum. Failure of mab-23 mutant males to sire progeny is due primarily to defective sex muscle-mediated turning during copulatory behavior and likely compounded by impairment of sperm passage through the proctodeum. In the male nervous system, mab-23 refines ray neuron subtype distribution by restricting expression of dopaminergic neurotransmitter identity through interactions with the Hox gene egl-5 and a TGF-␤-related signaling pathway. mab-23 has distinct roles and functions independent of mab-3, indicating different aspects of C. elegans male sexual differentiation are coordinated among DM domain family members. Our results support the hypothesis that DM domain genes derive from an ancestral male sexual regulator and suggest how regulation of sexual development has evolved in distinct ways in different phyla.

Penetration of a male copulatory organ into a suitable mate is a conserved and necessary behavioral step for most terrestrial matings; however, the detailed molecular and cellular mechanisms for this distinct social interaction have not been elucidated in any animal. During mating, the Caenorhabditis elegans male cloaca is maintained over the hermaphrodite's vulva as he attempts to insert his copulatory spicules. Rhythmic spicule thrusts cease when insertion is sensed. Circuit components consisting of sensory/motor neurons and sex muscles for these steps have been previously identified, but it was unclear how their outputs are integrated to generate a coordinated behavior pattern. Here, we show that cholinergic signaling between the cloacal sensory/motor neurons and the posterior sex muscles sustains genital contact between the sexes. Simultaneously, via gap junctions, signaling from these muscles is transmitted to the spicule muscles, thus coupling repeated spicule thrusts with vulval contact. To transit from rhythmic to sustained muscle contraction during penetration, the SPC sensory-motor neurons integrate the signal of spicule's position in the vulva with inputs from the hook and cloacal sensilla. The UNC-103 K+ channel maintains a high excitability threshold in the circuit, so that sustained spicule muscle contraction is not stimulated by fewer inputs. We demonstrate that coordination of sensory inputs and motor outputs used to initiate, maintain, self-monitor, and complete an innate behavior is accomplished via the coupling of a few circuit components.

In Caenorhabditis elegans, the DBL-1 pathway, a BMP/TGFβ-related signaling cascade, regulates body size and male tail development. We have cloned a new gene, sma-9, that encodes the C. elegans homolog of Schnurri, a large zinc finger transcription factor that regulates dpp target genes in Drosophila. Genetic interactions, the sma-9 loss-of-function phenotype, and the expression pattern suggest that sma-9 acts as a downstream component and is required in the DBL-1 signaling pathway, and thus provide the first evidence of a conserved role for Schnurri proteins in BMP signaling. Analysis of sma-9 mutant phenotypes demonstrates that SMA-9 activity is temporally and spatially restricted relative to known DBL-1 pathway components. In contrast with Drosophila schnurri, the presence of multiple alternatively spliced sma-9 transcripts suggests protein isoforms with potentially different cell sublocalization and molecular functions. We propose that SMA-9 isoforms function as transcriptional cofactors that confer specific responses to DBL-1 pathway activation.

Many evolutionarily significant behaviors, such as mating, involve dynamic interactions with animate targets. This raises the question of what features of neural circuit design are essential to support these complex types of behavior. The Caenorhabditis elegans male uses 18 ray sensilla of the tail to coordinate mate apposition behavior, which facilitates a systematic search of the hermaphrodite surface for the vulva. Precisely how ray neuron types, A and B, robustly endow the male with a high degree of spatial and temporal precision is unknown. We show that the appositional postures that drive the search trajectory reflect the complex interplay of ray neuron type-induced motor outputs. Cell-type-specific ablations reveal that the A-neurons are required for all appositional postures. Their activity is instructive because the A-neurons can induce scanning-and turning-like appositional postures when artificially activated with channelrhodopsin (ChR2). B-neurons are essential only for initiation of the behavior in which they enhance male responsiveness to hermaphrodite contact. When artificially activated using ChR2, A-and B-neurons produce different tail ventral curl postures. However, when coactivated, A-neuron posture dominates, limiting B-neuron contributions to initiation or subsequent postures. Significantly, males lacking the majority of rays retain a high degree of postural control, indicating significant functional resilience in the system. Furthermore, eliminating a large number of male-specific ray neuron targets only partially attenuates tail posture control revealing that gender-common cells make an important contribution to the behavior. Thus, robustness may be a crucial feature of circuits underlying complex behaviors, such as mating, even in simple animals. IntroductionHow animals sense the relevant features of their environment and translate this information into appropriate motor responses is perhaps the overarching question in neuroscience. Ultimate and proximate mechanisms underlying mating success and the transmission of heritable information to the next generation is a central concern for evolutionary biology. The nematode worm Caenorhabditis elegans represents a valuable model system for exploring the molecular and cellular underpinnings of these two fundamental questions. Many studies of C. elegans behavior (for example, chemotaxis, thermotaxis, and mechanosensation) use hermaphrodites in simple behavioral assays (for review, see Bargmann, 2006;Goodman, 2006;Garrity et al., 2010). These behaviors are mediated by relatively few sensory receptor cells with limited in-built redundancy (Chalfie and Sulston, 1981;Bargmann and Horvitz, 1991;Biron et al., 2008). However, many evolutionarily significant behaviors involve dynamic interactions with animate targets. This raises the question of what features of neural circuit design are essential for supporting these more complex types of behavior. C. elegans male mating behavior consists of a carefully orchestrated sequence of sensorimotor transformati...