Pathogenic bacteria modulate pheromone response to promote mating

Wu, Taihong; Ge, Minghai; Wu, Min; Duan, Fengyun; Liang, Jingting; Chen, Maoting; Gracida, Xicotencatl; Li, He; Yang, Wenxing; Rouf, Abdul; Li, Chengyin; Butcher, Rebecca A.; Saltzman, Arneet L.; Zhang, Yun

doi:10.1038/s41586-022-05561-9

Cited by 19 publications

(21 citation statements)

References 67 publications

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“…One interpretation of this finding is that by removing the need to search for mates, the mating pressure is reduced in males, thus allowing them to activate the otherwise gated behavior. This observation is further supported by recent evidence of increased mating by hermaphrodites previously exposed to pathogenic bacterium 72 . It is tempting to speculate that these two pathways co-evolve to maximize organismal fitness under dire conditions.…”

Section: Discussionsupporting

confidence: 78%

Modulation by NPYR underlies experience-dependent, sexually dimorphic learning

Peedikayil-Kurien,

Haque,

Gat

et al. 2023

Preprint

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The evolutionary paths taken by each sex within a given species sometimes diverge, resulting in behavioral differences that promote specific fitness outcomes for each sex. Given their distinct needs, the mechanism by which each sex learns from a shared experience is still an open question. We reveal a novel sexual dimorphism in learning: C. elegans males do not learn to avoid the pathogenic bacteria PA14 as efficiently and rapidly as hermaphrodites, even though their innate immunity recognizes the pathogen in a similar manner. Notably, we observe sexually dimorphic neuronal activity following pathogen exposure: hermaphrodites generate robust representations while males, in line with their behavior, exhibit contrasting representations, suggesting that a mechanism that modulates incoming sensory cues is at play. Transcriptomic and behavioral analysis revealed that the neuropeptide receptor npr-5, an ortholog of the mammalian NPY receptor, regulates male learning by modulating neuronal activity. Furthermore, we show the dependency of the males decision-making phenotype on their sexual status and demonstrate the pivotal role of npr-5 in this regulation as a sensory gatekeeper. Thus, collectively, we portray sex-specific plasticity in behavior toward a shared experience by modulating learning to fulfill the evolutionary needs.

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Section: Discussionsupporting

confidence: 78%

Modulation by NPYR underlies experience-dependent, sexually dimorphic learning

Peedikayil-Kurien,

Haque,

Gat

et al. 2023

Preprint

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“…food source, starvation, or population density. 52 We have found that C. nigoni does not express neuronal transgenes consistently even when using protocols optimized in other less-tractable nematode species such as C. briggsae 53 or Pristionchus pacificus , 54 and in the absence of efficient C. nigoni transgenesis, direct measurements or perturbations of AWA activity were not feasible. Finally, further experiments are required to define the sperm-related signal that suppresses female receptivity, and to ask whether the same signal suppresses chemotaxis to males in mated C. nigoni females and young adult C. tropicalis hermaphrodites.…”

Section: Discussionmentioning

confidence: 93%

Evolutionary transitions from female to hermaphrodite reproduction remodel olfactory and mating-receptive behaviors

Ebert,

Bargmann

2023

Preprint

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Male/hermaphrodite species have arisen multiple times from a male/female ancestral state in nematodes, providing a model to study behavioral adaptations to different reproductive strategies. Here we examined the mating behaviors of male/female (gonochoristic) Caenorhabditis species in comparison to male/hermaphrodite (androdiecious) close relatives. We find that females from two species in the Elegans group chemotax to volatile odor from males, a behavior described in only a few animal species. The females also display known mating-receptive behaviors such as sedation when male reproductive structures contact the vulva. Focusing on the male/female species C. nigoni, we show that female chemotaxis to males is limited to adult females approaching adult or near-adult males, and relies upon the AWA neuron-specific transcription factor ODR-7, as does male chemotaxis to female odor as previously shown in C. elegans. However, female receptivity during mating contact is odr-7-independent. All female behaviors are suppressed by mating, and all are absent in young hermaphrodites from the sister species C. briggsae. However, latent receptivity during mating contact can be uncovered in mutant or aged C. briggsae hermaphrodites that lack self-sperm. Young hermaphrodites from a second androdioecious species, C. tropicalis, are similarly unreceptive to males, but recover all female behaviors upon aging. These results reveal two mechanistically distinct components of the shift from female to hermaphrodite behavior: the loss of female-specific odr-7-dependent chemotaxis, and a sperm-dependent state of reduced receptivity to mating contact. The recovery of receptivity after sperm depletion has the potential to maximize hermaphrodite fitness across the lifespan.

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“…VSPs are primarily thought to signal sperm depletion, though it is possible that they could also be used by younger hermaphrodites in contexts that increase their motivation for outcrossing, e.g., pathogen exposure. 82 Identifying the molecular nature of these pheromones and the mechanisms that regulate their production will be important future goals for the field.…”

Section: Discussionmentioning

confidence: 99%

“…Our results demonstrate that males prefer to interact with virgin over previously mated hermaphrodites, and with well-fed over nutrientdeprived hermaphrodites. Males can likely assess other aspects of hermaphrodite state-recent studies have shown that hermaphrodites exposed to the pathogen Pseudomonas have an increased mating frequency, 82 but that males avoid mating with hermaphrodites infected with Orsay virus. 88 Each of the steps of mate-choice behavior we have described here are also likely plastic; understanding how they are influenced by a male's physiological status and reproductive experience, as well as the behavioral and physiological features of potential mates, will be exciting areas for future work.…”

Section: Discussionmentioning

confidence: 99%

C. elegansmales optimize mate-choice decisions via sex-specific responses to multimodal sensory cues

Luo

Barrios

Portman

2023

Preprint

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For sexually reproducing animals, selecting optimal mates is essential for maximizing reproductive fitness. Because the nematode C. elegans reproduces mostly by self-fertilization, little is known about its mate-choice behaviors. While several sensory cues have been implicated in males' ability to recognize hermaphrodites, achieving an integrated understanding of the ways males use these cues to assess relevant characteristics of potential mates has proven challenging. Here, we use a choice-based social-interaction assay to explore the ability of C. elegans males to make and optimize mate choices. We find that males use a combination of volatile sex pheromones (VSPs), ascaroside pheromones, surface-bound chemical cues, and other signals to robustly assess a variety of features of potential mates. Specific aspects of mate choice are communicated by distinct signals: the presence of a sperm-depleted, receptive hermaphrodite is likely signaled by VSPs, while developmental stage and sex are redundantly specified by ascaroside pheromones and surface-associated cues. Ascarosides also signal nutritional information, allowing males to choose well-fed over starved mates, while both ascarosides and surface-associated cues cause males to prefer virgin over previously mated hermaphrodites. The male-specificity of these behavioral responses is determined by both male-specific neurons and the male state of sex-shared circuits, and we reveal an unexpected role for the sex-shared ASH sensory neurons in male attraction to endogenously produced hermaphrodite ascarosides. Together, our findings lead to an integrated view of the signaling and behavioral mechanisms by which males use diverse sensory cues to assess multiple features of potential mates and optimize mate choice.

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Pathogenic bacteria modulate pheromone response to promote mating

Cited by 19 publications

References 67 publications

Modulation by NPYR underlies experience-dependent, sexually dimorphic learning

Modulation by NPYR underlies experience-dependent, sexually dimorphic learning

Evolutionary transitions from female to hermaphrodite reproduction remodel olfactory and mating-receptive behaviors

C. elegansmales optimize mate-choice decisions via sex-specific responses to multimodal sensory cues

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