Mating Damages the Cuticle of C. elegans Hermaphrodites

Woodruff, Gavin C.; Knauss, Christine M.; Maugel, Timothy K.; Haag, Eric S.

doi:10.1371/journal.pone.0104456

Cited by 21 publications

(17 citation statements)

References 34 publications

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“…Male sperm and seminal fluid also trigger physiological changes in mated hermaphrodites (38). It also has been shown that the act of mating is followed by the appearance of cuticular damage around the hermaphrodite vulva (39). Unfortunately, whether any of these physiological and lifespan alterations are detrimental to hermaphrodite fecundity or the fitness of their offspring is unclear.…”

Section: Discussionmentioning

confidence: 99%

Communication between oocytes and somatic cells regulates volatile pheromone production in Caenorhabditis elegans

Leighton

Choe

et al. 2014

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

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Males of the androdioecious species Caenorhabditis elegans are more likely to attempt to mate with and successfully inseminate C. elegans hermaphrodites that do not concurrently harbor sperm. Although a small number of genes have been implicated in this effect, the mechanism by which it arises remains unknown. In the context of the battle of the sexes, it is also unknown whether this effect is to the benefit of the male, the hermaphrodite, or both. We report that successful contact between mature sperm and oocyte in the C. elegans gonad at the start of fertilization causes the oocyte to release a signal that is transmitted to somatic cells in its mother, with the ultimate effect of reducing her attractiveness to males. Changes in hermaphrodite attractiveness are tied to the production of a volatile pheromone, the first such pheromone described in C. elegans.fertilization | sex pheromones | egg-soma communication I ts properties of self-fertilization and rapid generation, along with its extensive library of mutants, make Caenorhabditis elegans an excellent system in which to study reproductive events. The generation time of C. elegans is under 3 d, and a single hermaphroditic worm can use its sperm to fertilize its own eggs, without the need for mating (1). C. elegans and related nematodes have a robust sperm sensation pathway that limits unfruitful oocyte maturation and ovulation (2). Both self-sperm and nonself-sperm secrete protein ligands, known as major sperm proteins (MSPs), that activate signal transduction pathways in both unfertilized oocytes, leading to activation of mitogen-activated protein kinase (MPK-1), and the somatic gonad, involving transcription factor CEH-18. The result of this signaling is the release of oocytes from prophase I arrest and the ovulation of unarrested oocytes into the uterus (3, 4).Several behaviors of female and hermaphroditic nematodes have been demonstrated to correlate with either the presence of sperm or the recentness of mating. C. elegans hermaphrodites that have exhausted their supply of self-sperm are more likely to elicit a mating response from males of their species, and less likely to resist an attempted mating. Mutant C. elegans hermaphrodites that develop without self-sperm also elicit more mating attempts, and this increase in attractiveness vanishes after a successful mating (5, 6). In the gonochoristic species Caenorhabditis brenneri and Caenorhabditis remanei, males are attracted to a volatile pheromone produced only by females that have not recently mated (7). The mechanisms that link these behaviors to sperm status remain unknown.Pheromones have been shown to exist in dozens of nematode species (8-10) and have been positively identified in several, including C. elegans (11-14). Although HPLC-MS studies have led to the identification of more than 140 pheromones and pheromone-related metabolites in C. elegans (15), little is known about how production of such pheromones is regulated. Life stage and environmental conditions have been shown to affect pheromone o...

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Section: Discussionmentioning

confidence: 99%

Communication between oocytes and somatic cells regulates volatile pheromone production in Caenorhabditis elegans

Leighton

Choe

et al. 2014

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

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“…The results of these changes are body fragility/shrinkage, reduced osmotic stress resistance, and general behavioral decrepitude. Why excessive male secretions deleteriously alter the hermaphrodite is not known, but this is speculated to be either a form of male-directed population control or sexual conflict to limit the outcrossed hermaphrodite from further copulation (Maures et al 2014;Shi and Murphy 2014;Ting et al 2014;Woodruff et al 2014;Palopoli et al 2015).…”

Section: Physiology and Behavior: Sex-specific And Sexually Modulatedmentioning

confidence: 99%

Sexual Dimorphism and Sex Differences in Caenorhabditis elegans Neuronal Development and Behavior

2018

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As fundamental features of nearly all animal species, sexual dimorphisms and sex differences have particular relevance for the development and function of the nervous system. The unique advantages of the nematode have allowed the neurobiology of sex to be studied at unprecedented scale, linking ultrastructure, molecular genetics, cell biology, development, neural circuit function, and behavior. Sex differences in the nervous system encompass prominent anatomical dimorphisms as well as differences in physiology and connectivity. The influence of sex on behavior is just as diverse, with biological sex programming innate sex-specific behaviors and modifying many other aspects of neural circuit function. The study of these differences has provided important insights into mechanisms of neurogenesis, cell fate specification, and differentiation; synaptogenesis and connectivity; principles of circuit function, plasticity, and behavior; social communication; and many other areas of modern neurobiology.

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“…Sexual conflict in Caenorhabditis also may involve maleinduced harm to females. Male spicules scrape and physically damage the hermaphrodite cuticle in the vicinity of the vulva [73], and mating reduces her lifespan owing in part to physiological changes induced by sensing the chemical secretions of males [74][75][76]. The mating structure of males provides one of the most conspicuous and rapidly evolving morphological traits in Caenorhabditis [5], as in many other organisms [69], implicating selection of some form in its evolution.…”

Section: How Intense Are Sexual Selection and Sexual Conflict In Nature?mentioning

confidence: 99%

Caenorhabditis evolution in the wild

Cutter

2015

BioEssays

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Recent research has filled many gaps about Caenorhabditis natural history, simultaneously exposing how much remains to be discovered. This awareness now provides means of connecting ecological and evolutionary theory with diverse biological patterns within and among species in terms of adaptation, sexual selection, breeding systems, speciation, and other phenomena. Moreover, the heralded laboratory tractability of C. elegans, and Caenorhabditis species generally, provides a powerful case study for experimental hypothesis testing about evolutionary and ecological processes to levels of detail unparalleled by most study systems. Here, I synthesize pertinent theory with what we know and suspect about Caenorhabditis natural history for salient features of biodiversity, phenotypes, population dynamics, and interactions within and between species. I identify topics of pressing concern to advance Caenorhabditis biology and to study general evolutionary processes, including the key opportunities to tackle problems in dispersal dynamics, competition, and the dimensionality of niche space.

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Mating Damages the Cuticle of C. elegans Hermaphrodites

Cited by 21 publications

References 34 publications

Communication between oocytes and somatic cells regulates volatile pheromone production in Caenorhabditis elegans

Communication between oocytes and somatic cells regulates volatile pheromone production in Caenorhabditis elegans

Sexual Dimorphism and Sex Differences in Caenorhabditis elegans Neuronal Development and Behavior

Caenorhabditis evolution in the wild

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