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Histomorphological comparison of testes in species of box jellyfish (Cnidaria; Cubozoa): does morphology differ with mode of reproduction and fertilization?

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Abstract

Cubozoa jellyfish species exhibit either internal or external fertilization, and reproductive behavior involving spermcasting or complex copulatory sexual behavior, but male gonad morphology has not been investigated broadly in cubozoans. In this study, a histological comparison was conducted of the testes of four cubozoan species in two orders: Carybdea marsupialis (Carybdeidae), Morbakka virulenta (Carukiidae), and Tamoya cf. haplonema (Tamoyidae) in Carybdeida and Chiropsalmus quadrumanus (Chiropsalmidae) in Chirodropida. Our results show spermatic follicles present in all species, with spermatogenesis occurring in two layers, the gastrodermis and the gonadal mesoglea. Specimens were either immature males or unspawned males, except in the case of Tamoya cf. haplonema which displayed rupture sites in the wall of the follicles, indicating prior release of sperm. Interspecific comparative histological study revealed that spermatogenesis generally occurs in a polarized manner towards the lumen of the spermatic follicle, with mature spermatozoa in the center awaiting gonadal rupture and release for either internal or external fertilization. Furthermore, we provide a synopsis of the histological findings to date on cubozoan testes, emphasizing incidences of conserved male gonad morphology regardless of mode of fertilization, in addition to separate novelties that have arisen in two internally fertilizing lineages, each exhibiting unique reproductive behavior. Further taxon-sampling of additional species at different development stages may reveal a broader diversity in testes morphology across Cubozoa and serve as a basis for a deeper investigation into the emergence of novel modes of sexual reproduction in non-bilaterian animals.

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Acknowledgments

We would like to thank André Morandini for providing the material and for encouragement and discussions on an early draft of the manuscript; Maria Mendoza-Becerril for her comments; and Alvaro Migotto, Eduardo Obis, and Bastian Bentlage for cubomedusae photographs. We would also like to thank Sho Toshino for photography as well as tissue samples and Melissa J. Acevedo for tissue samples. We also acknowledge Enio Mattos and Phillip Lenktaitis for their assistance in the histology lab.

Funding

This study was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (134663/2013-6, 305805/2013-4, 445444/2014-2, 309995/2017-5, 140235/2018-3), by Fundação de Amparo à Pesquisa do Estado de São Paulo (2004/09961-4, 2011/50242-5), by Coordenação de Pessoal de Nível Superior (CAPES), and by São Paulo Research Foundation (FAPESP) (grant no. 2004/09961-4, 2011/50242-5, 2019/01370-2). This is a contribution of the NP-BioMar (USP).

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  1. Institute of Biosciences, University of São Paulo, R. Matão Tr. 14, 101, Sao Paulo, 05508-090, Brazil

    Jimena García-Rodríguez, José Eduardo A. R. Marian & Antonio Carlos Marques

  2. Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, WA, USA

    Cheryl Lewis Ames

  3. Graduate School of Agricultural Science, Faculty of Agriculture, Tohoku University, Sendai, 980-8572, Japan

    Cheryl Lewis Ames

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  1. Jimena García-Rodríguez
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Correspondence to Jimena García-Rodríguez.

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García-Rodríguez, J., Ames, C.L., Marian, J.E.A.R. et al. Histomorphological comparison of testes in species of box jellyfish (Cnidaria; Cubozoa): does morphology differ with mode of reproduction and fertilization?. Org Divers Evol 20, 25–36 (2020). https://doi.org/10.1007/s13127-019-00427-x

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