Body stiffness is a mechanical property that facilitates contact-mediated mate recognition in Caenorhabditis elegans

Creators: Weng, Jen-Wei; Park, Heenam; Valotteau, Claire; Chen, Rui-Tsung; Essmann, Clara L.; Pujol, Nathalie; Sternberg, Paul W.¹; Chen, Chun-Hao

1. California Institute of Technology

Abstract

Physical contact is prevalent in the animal kingdom to recognize suitable mates by decoding information about sex, species, and maturity. Although chemical cues for mate recognition have been extensively studied, the role of mechanical cues remains elusive. Here, we show that C. elegans males recognize conspecific and reproductive mates through short-range cues, and that the attractiveness of potential mates depends on the sex and developmental stages of the hypodermis. We find that a particular group of cuticular collagens is required for mate attractiveness. These collagens maintain body stiffness to sustain mate attractiveness but do not affect the surface properties that evoke the initial step of mate recognition, suggesting that males utilize multiple sensory mechanisms to recognize suitable mates. Manipulations of body stiffness via physical interventions, chemical treatments, and 3D-printed bionic worms indicate that body stiffness is a mechanical property for mate recognition and increases mating efficiency. Our study thus extends the repertoire of sensory cues of mate recognition in C. elegans and provides a paradigm to study the important roles of mechanosensory cues in social behaviors.

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Acknowledgement

We thank the members of the Chen and the Sternberg laboratories for insightful discussions. We also thank Ray Hong, Chun-Liang Pan, Yi-Chun Wu, and Shih-Peng Chan for sharing reagents and strains. We thank WormBase for providing organized genetic and genomic information. Some strains were provided by the C. elegans Genetics Center, funded by the NIH Office of Research Infrastructure Programs (P40 OD010440). We are grateful for the technical assistance of Technology Commons, College of Life Science, National Taiwan University with scanning electron microscopy (SEM) and confocal microscopy (CLSM). We thank the C. elegans Core Facility of the National Core Facility for Biopharmaceuticals, Ministry of Science of Technology in Taiwan. This study was funded by the Ministry of Science and Technology and National Science and Technology Council, Taiwan, to C.-H.C. (MOST 109-2636-B-002-016, MOST 110-2636-B-002-013, and NSTC 111-2636-B-002-027) and NIH to P.W.S. (R01NS113119 and R240D023041). The study is also funded by the French National Research Agency ANR-22-CE13-0037-01, by the “Investissements d’Avenir” French Government program (ANR-16-CONV-0001), by France 2030, and by the Excellence Initiative of Aix-Marseille University-A^∗MIDEX and institutional grants from CNRS, Aix Marseille University, National Institute of Health and Medical Research (INSERM) to the CIML. The NanoWizard III (JPK) was funded by the Ministry of Science, Research and the Arts of Baden-Württemberg (Az: 33-7532.20) and the University of Freiburg (“Strategiefonds”), granted to Winfried Römer.

Contributions

Conceptualization, C.-H.C., J.-W.W., and P.W.S.; methodology, J.-W.W., H.P., R.-T.C., C.V., N.P., and C.-H.C.; investigation, J.-W.W., H.P., R.-T.C., C.V., C.L.E., N.P., and C.-H.C.; writing – original draft, C.-H.C., J.-W.W., and P.W.S.; writing – review & editing, C.-H.C., J.-W.W., and P.W.S.; supervision, C.-H.C. and P.W.S.; funding acquisition, C.-H.C. and P.W.S.

Data Availability

All the primary data used in this study have been deposited at Figshare and are publicly available as of the date of publication. The DOI is listed in the key resources table. Microscopy data reported in this study will be shared by the lead contact upon request.
This study does not use original code for data analysis.
Any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request.
Document S1. Figures S1–S6
Table S1. Sequence information of strains generated by the CRISPR STOP-IN method, related to STAR Methods and Figure S4
Data S1. List of differentially expressed genes in the blmp-1 mutant for gene ontology analysis, related to STAR Methods and Figure 2

Conflict of Interest

The authors declare no competing interests.

Additional Information

We support inclusive, diverse, and equitable conduct of research.

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