Scott W. Emmons

The Connectome of a Decision-Making Neural Network

The Male Wiring Diagram The function of the nervous system is thought to represent an emergent property of its network connectivity. However, there are few complete descriptions of all the physical connections between neurons within a real nervous system. Working in nematodes, Jarrell et al. (p. 437; see the Perspective by Chklovskii and Bargmann) identified the complete connectome—every single chemical and gap junction synapse—of the tail ganglia, which govern mating behavior. The complete wiring structure of the synaptic network governing mating behavior of male nematodes is revealed. In order to understand the nervous system, it is necessary to know the synaptic connections between the neurons, yet to date, only the wiring diagram of the adult hermaphrodite of the nematode Caenorhabditis elegans has been determined. Here, we present the wiring diagram of the posterior nervous system of the C. elegans adult male, reconstructed from serial electron micrograph sections. This region of the male nervous system contains the sexually dimorphic circuits for mating. The synaptic connections, both chemical and gap junctional, form a neural network with four striking features: multiple, parallel, short synaptic pathways directly connecting sensory neurons to end organs; recurrent and reciprocal connectivity among sensory neurons; modular substructure; and interneurons acting in feedforward loops. These features help to explain how the network robustly and rapidly selects and executes the steps of a behavioral program on the basis of the inputs from multiple sensory neurons.

Evidence for a transposon in caenorhabditis elegans

The C. elegans genome contains a 1.7 kb repeated DNA sequence (Tc1) that is present in different numbers in various strains. In strain Bristol and 10 other strains analyzed, there are 20 +/- 5 copies of Tc1, and these are located at a nearly constant set of sites in the DNA. In Bergerac, however, there are 200 +/- 50 interspersed copies of Tc1 that have arisen by insertion of Tc1 elements into new genomic sites. The interspersed copies of Tc1 have a conserved, nonpermuted structure. The structure of genomic Tc1 elements was analyzed by the cloning of a single Tc1 element from Bergerac and the comparison of its structure with homologous genomic sequences in Bristol and Bergerac. Tc1 elements at three sites analyzed in Bergerac undergo apparently precise excision from their points of insertion at high frequency.

Mate Searching in Caenorhabditis elegans: A Genetic Model for Sex Drive in a Simple Invertebrate

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.

Widespread occurrence of the Tc1 transposon family: Tc1-like transposons from teleost fish

We characterized five transposable elements from fish: one from zebrafish (Brachydanio rerio), one from rainbow trout (Salmo gairdneri), and three from Atlantic salmon (Salmo salar). All are closely similar in structure to the Tel transposon of the nematode Caenorhabditis elegans. A comparison of 17 Tc1-like transposons from species representing three phyla (nematodes, arthropods, and chordates) showed that these elements make up a highly conserved transposon family. Most are close to 1.7 kb in length, have inverted terminal repeats, have conserved terminal nucleotides, and each contains a single gene encoding similar poly peptides. The phylogenetic relationships of the transposons were reconstructed from the amino acid sequences of the conceptual proteins and from DNA sequences. The elements are highly diverged and have evidently inhabited the genomes of these diverse species for a long time. To account for the data, it is not necessary to invoke recent horizontal transmission.

High-frequency excision of transposable element Tc1 in the nematode caenorhabditis elegans is limited to somatic cells

Tc 1 transposable elements in the nematode Caenorhabditis elegans undergo excision at high frequency. We show here that this excision occurs primarily or entirely in the somatic tissues of the organism. Absence of germ-line excision is demonstrated by showing that Tc 1 elements are genetically stable; elements at particular genomic sites, as well as the overall number of elements in the genome, were stably maintained during a year of continuous, nonselective propagation. Somatic excision is demonstrated by showing that empty Tc 1 sites arise during a single generation of growth of a synchronous population and are not inherited by the next generation. These results suggest that excision of Tc 1 elements is under the control of tissue-specific factors.

Reproductive isolation in rhabditidae (nematoda:secernentea); mechanisms that isolate six species of three genera

We have attempted interspecific hybridizations among six species of rhabditid nematodes: Caenorhabditis elegans, Caenorhabditis briggsae, Caenorhabditis remanei, Caenorhabditis sp. v, Rhabditis sp., and Pelodera teres. Copulation was observed in all crosses between Caenorhabditis species; however, none resulted in the generation of stable hybrid populations. No copulation was observed in crosses between Caenorhabditis males and Rhabditis or Pelodera females, even when congeneric females were present, suggesting that Caenorhabditis males are able to selectively recognize congeneric females by a short‐range stimulus. All pairwise combinations of Caenorhabditis species were isolated to some degree by gametic mechanisms; 7 of 12 combinations were cross infertile and 5 of 12 were cross‐fertile but had low brood sizes. In cross‐fertile combinations, most hybrid embryos were inviable and arrested prior to gastrulation. Only in crosses of C. briggsae males to C. sp. v females did any hybrids survive embryogenesis. Most of these C. briggsae/C. sp. v hybrids arrested during larval development, and the few that reached adulthood invariably were female. These results are consistent with the presence of at least two lethal factors in the C. briggsae‐C. sp. v combination: a maternal lethal factor in the cytoplasm of C. briggsae and a recessive lethal factor on the X chromosome of C. sp. v.

Male Development and Mating Behavior

I. INTRODUCTION AND OVERVIEW OF MALE ANATOMY The complexity of the anatomy and mating behavior of Caenorhabditis elegans males poses a variety of interesting questions in neurobiology and developmental biology. The mating structures of the male tail differ in form between nematode species and hence provide an opportunity to study the determinants of morphology and their evolution. The fact that the male is dispensable for laboratory culture makes genetic analysis of the male attractive because strains can be easily maintained as hermaphrodites, and their defective males can be studied. In particular, mutant males are often examined as the progeny of Him (high incidence of males) hermaphrodites (Hodgkin et al. 1979), which segregate XO male progeny by X chromosome nondisjunction during meiosis. We discuss here the major features of male development and behavior and those aspects that have been analyzed most intensively. We begin with an overview of male anatomy, discuss mating behavior, and then discuss the development of each structure. Table 1 summarizes the male-specific neurons, Table 2 summarizes the other cells discussed in this chapter, and Table 3 summarizes the genes discussed in this chapter. The male anatomy differs from that of the hermaphrodite in that the male has a single-armed somatic gonad of only 55 cells as well as 41 specialized muscles, 79 additional neurons (87 sex-specific; White et al. 1976; Sulston et al. 1980), 36 extra neuronal support cells (socket and sheath cells), 23 proctodeal cells, and 16 hypodermal cells associated with mating structures. Most of these...

Sensory Regulation of C. elegans Male Mate-Searching Behavior

How do animals integrate internal drives and external environmental cues to coordinate behaviors? We address this question by studying mate-searching behavior in C. elegans. C. elegans males explore their environment in search of mates (hermaphrodites) and will leave food if mating partners are absent. However, when mates and food coincide, male exploratory behavior is suppressed and males are retained on the food source. We show that the drive to explore is stimulated by male-specific neurons in the tail, the ray neurons. Periodic contact with the hermaphrodite detected through ray neurons changes the males behavior during periods of no contact and prevents the male from leaving the food source. The hermaphrodite signal is conveyed by male-specific interneurons that are postsynaptic to the rays and that send processes to the major integrative center in the head. This study identifies key parts of the neural circuit that regulates a sexual appetitive behavior in C. elegans.

PDF-1 neuropeptide signaling modulates a neural circuit for mate-searching behavior in C. elegans

Appetitive behaviors require complex decision making that involves the integration of environmental stimuli and physiological needs. C. elegans mate searching is a male-specific exploratory behavior regulated by two competing needs: food and reproductive appetite. We found that the pigment dispersing factor receptor (PDFR-1) modulates the circuit that encodes the male reproductive drive that promotes male exploration following mate deprivation. PDFR-1 and its ligand, PDF-1, stimulated mate searching in the male, but not in the hermaphrodite. pdf-1 was required in the gender-shared interneuron AIM, and the receptor acted in internal and external environment-sensing neurons of the shared nervous system (URY, PQR and PHA) to produce mate-searching behavior. Thus, the pdf-1 and pdfr-1 pathway functions in non–sex-specific neurons to produce a male-specific, goal-oriented exploratory behavior. Our results indicate that secretin neuropeptidergic signaling is involved in regulating motivational internal states.

The Caenorhabditis elegans schnurri homolog sma-9 mediates stage- and cell type-specific responses to DBL-1 BMP-related signaling

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.