Internal fertilization and sperm storage in cnidarians: a response to Orr and Brennan

Marques, Antônio Carlos; García, J. J.; Ames, Cheryl Lewis

doi:10.1016/j.tree.2015.06.002

Cited by 27 publications

(5 citation statements)

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“…The homology between gametoducts in Staurozoa and gonopores in Periphylla periphylla remains to be tested. Indeed, recent research is beginning to uncover more complex reproductive systems in different cnidarians (Cartwright & Nawrocki, 2010; Schiariti et al, 2012), especially some species belonging to the class Cubozoa (Garm, Lebouvier & Tolunay, 2015; Marques, García & Lewis Ames, 2015). Although plesiomorphic external fertilization would be expected in adult medusae (Marques & Collins, 2004), certain cubomedusae can present courtship behavior, specialized internal fertilization, and sperm storage (Lewis & Long, 2005; Garm, Lebouvier & Tolunay, 2015; Marques, García & Lewis Ames, 2015), which demonstrate the importance to highlight different cnidarian reproductive strategies in order to study their evolution.…”

Section: Discussionmentioning

confidence: 99%

Comparative internal anatomy of Staurozoa (Cnidaria), with functional and evolutionary inferences

Miranda

Collins

Hirano

et al. 2016

PeerJ

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Comparative efforts to understand the body plan evolution of stalked jellyfishes are scarce. Most characters, and particularly internal anatomy, have neither been explored for the class Staurozoa, nor broadly applied in its taxonomy and classification. Recently, a molecular phylogenetic hypothesis was derived for Staurozoa, allowing for the first broad histological comparative study of staurozoan taxa. This study uses comparative histology to describe the body plans of nine staurozoan species, inferring functional and evolutionary aspects of internal morphology based on the current phylogeny of Staurozoa. We document rarely-studied structures, such as ostia between radial pockets, intertentacular lobules, gametoducts, pad-like adhesive structures, and white spots of nematocysts (the last four newly proposed putative synapomorphies for Staurozoa). Two different regions of nematogenesis are documented. This work falsifies the view that the peduncle region of stauromedusae only retains polypoid characters; metamorphosis from stauropolyp to stauromedusa occurs both at the apical region (calyx) and basal region (peduncle). Intertentacular lobules, observed previously in only a small number of species, are shown to be widespread. Similarly, gametoducts were documented in all analyzed genera, both in males and females, thereby elucidating gamete release. Finally, ostia connecting adjacent gastric radial pockets appear to be universal for Staurozoa. Detailed histological studies of medusozoan polyps and medusae are necessary to further understand the relationships between staurozoan features and those of other medusozoan cnidarians.

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Section: Discussionmentioning

confidence: 99%

Comparative internal anatomy of Staurozoa (Cnidaria), with functional and evolutionary inferences

Miranda

Collins

Hirano

et al. 2016

PeerJ

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“…The homology between gametoducts in Staurozoa and gonopores in Periphylla periphylla remains to be tested. Indeed, recent research is beginning to uncover more complex reproductive systems in different cnidarians (Cartwright & Nawrocki, 2010;Schiariti et al, 2012), especially some species belonging to the class Cubozoa (Garm, Lebouvier & Tolunay, 2015;Marques, García & Ames 2015). Although plesiomorphic external fertilization would be expected in adult medusae (Marques & Collins, 2004), certain cubomedusae can present courtship behavior, specialized internal fertilization, and sperm storage (Lewis & Long, 2005;Garm, Lebouvier & Tolunay, 2015;Marques, García & Ames 2015), which demonstrate the PeerJ reviewing PDF | (2016:06:11332:1:0:NEW 21 Aug 2016)…”

Section: Gonads and Gametoductmentioning

confidence: 99%

Peer Review #2 of "Comparative internal anatomy of Staurozoa (Cnidaria), with functional and evolutionary inferences (v0.1)"

Daly¹

2016

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Comparative efforts to understand the body plan evolution of stalked jellyfishes are scarce. Most characters, and particularly internal anatomy, have neither been explored for the class Staurozoa, nor broadly applied in its taxonomy and classification. Recently, a molecular phylogenetic hypothesis was derived for Staurozoa, allowing for the first broad histological comparative study of staurozoan taxa. This study uses comparative histology to describe the body plans of nine staurozoan species, inferring functional and evolutionary aspects of internal morphology based on the current phylogeny of Staurozoa. We document rarely-studied structures, such as ostia between radial pockets, intertentacular lobules, gametoducts, pad-like adhesive structures, and white spots of nematocysts (the last four newly proposed putative synapomorphies for Staurozoa). Two different regions of nematogenesis are documented. This work falsifies the view that the peduncle region of stauromedusae only retains polypoid characters, discussing that metamorphosis from stauropolyp to stauromedusa occurs both at the apical region (calyx) and basal region (peduncle). Intertentacular lobules, observed previously in only a small number of species, are shown to be widespread. Similarly, gametoducts were documented in all analyzed genera, both in males and females, thereby elucidating gamete release. Finally, ostia connecting adjacent gastric radial pockets appear to be universal for Staurozoa. Detailed histological studies of medusozoan polyps and medusae are necessary to further understand the relationships between staurozoan features and those of other medusozoan cnidarians.

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“…A. alata females exhibit internal fertilization during monthly inshore spermcasting aggregations (Bentlage et al, ; Lewis et al, ; Lewis Ames et al, ), while species of Tripedaliidae exhibit sexual dimorphism, spermatophore production and courtship behavior during seasonal copulation events (Bennett et al, ; Bentlage et al, ; Garm et al, ; Lewis & Long, ; Lewis et al, ; Straehler‐Pohl et al, ; Toshino et al, , 2017). Since C. sivickisi males can produce multiple spermatophores and copulate with multiple females, and females can copulate with multiple males, workers have speculated that sperm storage structures may have evolved under strict selective pressures (Marques, García, & Lewis Ames, ). However, an extensive morphological investigation of putative sperm storage structures (e.g., subgastric sacs) in C. sivickisi is needed before a definitive role in sexual reproduction can be established.…”

Section: Introductionmentioning

confidence: 99%

Gonadal histology of box jellyfish (Cnidaria: Cubozoa) reveals variation between internal fertilizing species Alatina alata (Alatinidae) and Copula sivickisi (Tripedaliidae)

García-Rodríguez

Ames

Marian

et al. 2018

Journal of Morphology

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Cubozoans (box jellyfish) are gonochoristic cnidarians with distinct reproductive strategies. This comparative histological study examines the gonad organization of Alatina alata and Copula sivickisi, two box jellyfish species that exhibit different modes of internal fertilization. A. alata reproduces via spermcasting aggregations while C. sivickisi reproduces via copulation; in both cases, internal fertilization occurs in the gastrovascular cavity. Herein, we provide the first histological description of subgastric sacs-structures unique to C. sivickisi. Although previously thought to function as sperm storage sacs, our findings reveal that subgastric sacs are nematocyst nests lacking sperm entirely. Conversely, we discovered that velarial spots in C. sivickisi females correspond to actual sperm storage structures. Histological examination of cubozoan sperm packages revealed that while sperm packages from both species have motile flagella, A. alata males produce nonencapsulated sperm bundles (i.e., "spermatozeugmata"), and C. sivickisi males produce encapsulated packages (i.e., "spermatophores"). Our findings corroborate the presence of several types of nematocysts in C. sivickisi embryo strands and spermatophores, and indicate their provenance to be both female and male gonads respectively, as well as subgastric sacs (i.e., nematocyst nests). In contrast to our findings of velarial spots as sperm storages structures in C. sivickisi females, and of nematocysts in the gonads of both sexes, we report that A. alata medusae lack both sperm storage structures and gonadal nematocysts. Finally, we discuss our findings on reproductive morphology of C. sivickisi and A. alata in light of the respective reproductive behavior of these two cubozoan species.

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Internal fertilization and sperm storage in cnidarians: a response to Orr and Brennan

Cited by 27 publications

References 10 publications

Comparative internal anatomy of Staurozoa (Cnidaria), with functional and evolutionary inferences

Comparative internal anatomy of Staurozoa (Cnidaria), with functional and evolutionary inferences

Peer Review #2 of "Comparative internal anatomy of Staurozoa (Cnidaria), with functional and evolutionary inferences (v0.1)"

Gonadal histology of box jellyfish (Cnidaria: Cubozoa) reveals variation between internal fertilizing species Alatina alata (Alatinidae) and Copula sivickisi (Tripedaliidae)

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