A Hormone-Activated Central Pattern Generator for Courtship

Wagenaar, Daniel A.; Hamilton, M. S.; Huang, Tracy; Kristan, William B.; French, Kathleen A.

doi:10.1016/j.cub.2010.02.027

Cited by 56 publications

(64 citation statements)

References 36 publications

(34 reference statements)

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“…These pNPs regulate several aspects of physiology, including sexual behavior and reproduction (GnRH, achatin, oxytocin, and GnIH/SIFamide), diuresis (CRF/diuretic hormone, calcitonin, and vasopressin), gut and heart activity (achatin, luqin, and orcokinin), pain perception (opioid), and food intake (NPY, kinins, neuromedin-U, galanin/allatostatin-A, and orexin/allatotropin). These pNPs may have originated concomitantly with the origin of a complex bilaterian body plan having a through gut with novel controls for food intake and digestion, excretory and circulatory systems, light-controlled reproduction (50), a centralized nervous system (76), complex reproductive behavior (77,78), and learning (79). The stable association of receptor-ligand families across bilateria revealed the long-term coevolution of receptor-ligand pairs.…”

Section: Resultsmentioning

confidence: 99%

Global view of the evolution and diversity of metazoan neuropeptide signaling

Jékely

2013

Proc. Natl. Acad. Sci. U.S.A.

418

651

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Neuropeptides are signaling molecules that commonly act via G protein-coupled receptors (GPCRs) and are generated in neurons by proneuropeptide (pNP) cleavage. Present in both cnidarians and bilaterians, neuropeptides represent an ancient and widespread mode of neuronal communication. Due to the inherent difficulties of analyzing highly diverse and repetitive pNPs, the relationships among different families are often elusive. Using similarity-based clustering and sensitive similarity searches, I obtained a global view of metazoan pNP diversity and evolution. Clustering revealed a large and diffuse network of sequences connected by significant sequence similarity encompassing one-quarter of all families. pNPs belonging to this cluster were also identified in the early-branching neuronless animal Trichoplax adhaerens. Clustering of neuropeptide GPCRs identified several orthology groups and allowed the reconstruction of the phyletic distribution of receptor families. GPCR phyletic distribution closely paralleled that of pNPs, indicating extensive conservation and long-term coevolution of receptor-ligand pairs. Receptor orthology and intermediate sequences also revealed the homology of pNPs so far considered unrelated, including allatotropin and orexin. These findings, together with the identification of deuterostome achatin and luqin and protostome opioid pNPs, extended the neuropeptide complement of the urbilaterian. Several pNPs were also identified from the hemichordate Saccoglossus kowalevskii and the cephalochordate Branchiostoma floridae, elucidating pNP evolution in deuterostomes. Receptor-ligand conservation also allowed ligand predictions for many uncharacterized GPCRs from nonmodel species. The reconstruction of the neuropeptide-signaling repertoire at deep nodes of the animal phylogeny allowed the formulation of a testable scenario of the evolution of animal neuroendocrine systems.Platynereis | proenkephalin | Petromyzon N europeptides are diverse neuron-secreted peptides with neuromodulatory, neurotransmitter, or hormonal functions. Most neuropeptides signal via G protein-coupled receptors (GPCRs) (1), with a few exceptions (2-8). As modulators of neuronal activity, neuropeptides contribute to the generation of different outputs from the same neuronal circuit in a context-dependent manner (9), or orchestrate complex motor programs (10). Many neuropeptides act as hormones and are released into the haemolymph by neurohemal organs, such as the vertebrate pituitary gland, or the insect corpora cardiaca (11). These peptide hormones regulate various aspects of physiology, including growth, metabolism, and reproduction. Active neuropeptides are generated from an inactive proneuropeptide (pNP) that contains a single or multiple copies of active peptides. Active peptides are commonly short, with only a few families adopting well-defined, but unrelated, folds (e.g., prolactin and glycoprotein hormones). pNPs have a signal peptide (SP) and enter the secretory apparatus where dedicated proteases cleave them at mono...

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Section: Resultsmentioning

confidence: 99%

Global view of the evolution and diversity of metazoan neuropeptide signaling

Jékely

2013

Proc. Natl. Acad. Sci. U.S.A.

418

651

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“…Phenologs, by contrast, comprise conserved gene networks which become associated with very different phenotypes over the course of evolution [40]. For example, nonapeptides regulate pair-bonding behaviors across vertebrates [30,41], and orthologs of the oxytocin or vasopressin ancestral gene also regulate mating behavior in nematodes [48] and leeches [49]. The study of these convergent and divergent pathways in conjunction with a detailed understanding of the survival value and fitness consequences of specific behavior patterns promises to yield insights into general principles underlying social evolution at both proximate and ultimate levels.…”

Section: Neural Mechanisms In Social Speciesmentioning

confidence: 99%

An evolutionary framework for studying mechanisms of social behavior

Hofmann

Beery

Blumstein³

et al. 2014

Trends in Ecology & Evolution

172

133

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Social interactions are central to most animals and have a fundamental impact upon the phenotype of an individual. Social behavior (social interactions among conspecifics) represents a central challenge to the integration of the functional and mechanistic bases of complex behavior. Traditionally, studies of proximate and ultimate elements of social behavior have been conducted by distinct groups of researchers, with little communication across perceived disciplinary boundaries. However, recent technological advances, coupled with increased recognition of the substantial variation in mechanisms underlying social interactions, should compel investigators from divergent disciplines to pursue more integrative analyses of social behavior. We propose an integrative conceptual framework intended to guide researchers towards a comprehensive understanding of the evolution and maintenance of mechanisms governing variation in sociality.The study of social behavior in the 21st century All animals interact with conspecifics at some point in their lives. Members of the same species tend to be each other's fiercest competitors and strongest allies, as evidenced by the intense cooperation and conflict that characterize many intraspecific interactions [1]. These interactions are the products of genetic, epigenetic, endocrine, and neural mechanisms that -in conjunction with environmental conditions -affect Darwinian fitness and evolve via natural selection. Building upon Aristotle's four questions, Tinbergen [2] posited that understanding behavior requires the integration of studies of mechanism and function. Only by asking questions both from a proximate perspective (i.e., focusing on causation and development) and an ultimate perspective (i.e., focusing on adaptive value and evolutionary descent) can behavior be fully understood. Social behavior in particular lends itself to such an integrative approach not only because it commands the attention of many disciplines [3] but also because even many behaviors commonly considered nonsocial often occur in a social context (e.g., mating, fighting, parental care). Social behavior is also special because the selective agents are other members of the same species, and this results in intriguing evolutionary dynamics. Nevertheless, in the intervening decades since Tinbergen's

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“…For both visual and mechanical experiments, the lateral roots of ganglia 9 to 11 were cut and those three ganglia were immobilized using fine tungsten pins on a thin, rectangular slab of PDMS. In the context of leech electrophysiology, these preparations can be considered 'nearly intact', as similarly prepared leeches are known to exhibit approximately normal swimming behavior (Kristan et al, 1974) and much more reduced preparations still exhibit essential features of reproductive behaviors (Wagenaar et al, 2010). Critically, in the mechanical experiments, the cilia on the dorsal side remain in contact with the water as normal, and in the visual experiments, the light path to the sensilla is essentially unobstructed.…”

Section: Electrophysiologymentioning

confidence: 99%

Responses to mechanically and visually cued water waves in the nervous system of the medicinal leech

Lehmkuhl

Muthusamy

Wagenaar

2018

Journal of Experimental Biology

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Sensitivity to water waves is a key modality by which aquatic predators can detect and localize their prey. For one such predatorthe medicinal leech, Hirudo verbana -behavioral responses to visual and mechanical cues from water waves are well documented. Here, we quantitatively characterized the response patterns of a multisensory interneuron, the S cell, to mechanically and visually cued water waves. As a function of frequency, the response profile of the S cell replicated key features of the behavioral prey localization profile in both visual and mechanical modalities. In terms of overall firing rate, the S cell response was not direction selective, and although the direction of spike propagation within the S cell system did follow the direction of wave propagation under certain circumstances, it is unlikely that downstream neuronal targets can use this information. Accordingly, we propose a role for the S cell in the detection of waves but not in the localization of their source. We demonstrated that neither the head brain nor the tail brain are required for the S cell to respond to visually cued water waves.

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A Hormone-Activated Central Pattern Generator for Courtship

Cited by 56 publications

References 36 publications

Global view of the evolution and diversity of metazoan neuropeptide signaling

Global view of the evolution and diversity of metazoan neuropeptide signaling

An evolutionary framework for studying mechanisms of social behavior

Responses to mechanically and visually cued water waves in the nervous system of the medicinal leech

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