The effects of temperature and pH on the reproductive ecology of sand dollars and sea urchins: Impacts on sperm swimming and fertilization

Leuchtenberger, Sara Grace; Daleo, Maris; Gullickson, Peter; Delgado, Andi; Lo, Carly; Nishizaki, Michael T.

doi:10.1371/journal.pone.0276134

Cited by 4 publications

(1 citation statement)

References 120 publications

(146 reference statements)

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“…lack of monophyly for the stony corals), demonstrating a possibly ancient origin for sAC in this phylum, which supports a conserved role for sAC in foundational biological processes such as sexual reproduction. Given that the activation of the sAC-cAMP-PKA pathway is stimulated by alkalinization of the sperm cytosol, this result also has important implications for the reproduction of broadcast spawning marine invertebrates in the face of anthropogenic ocean acidification, which is already known to alter sperm motility in many species after exposure of either sperm or adult males prior to spawning [6,[54][55][56][57][58][59]. Future work should investigate the role of sAC-cAMP-PKA signalling in sperm from a broader diversity of species to clarify the mechanisms by which ocean acidification might impact reproduction across invertebrate phyla in future seas.…”

Section: (D) Cnidarian Sac Homologues Display Broad Structural and Fu...mentioning

confidence: 99%

Characterization of a sperm motility signalling pathway in a gonochoric coral suggests conservation across cnidarian sexual systems

Glass,

Ashey,

Okongwu

et al. 2023

Proc. R. Soc. B.

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Most stony corals liberate their gametes into the water column via broadcast spawning, where fertilization hinges upon the activation of directional sperm motility. Sperm from gonochoric and hermaphroditic corals display distinct morphological and molecular phenotypes, yet it is unknown whether the signalling pathways controlling sperm motility are also distinct between these sexual systems. Here, we addressed this knowledge gap using the gonochoric, broadcast spawning coral Astrangia poculata . We found that cytosolic alkalinization of sperm activates the pH-sensing enzyme soluble adenylyl cyclase (sAC), which is required for motility. Additionally, we demonstrate for the first time in any cnidarian that sAC activity leads to protein kinase A (PKA) activation, and that PKA activity contributes to sperm motility activation. Ultrastructures of A. poculata sperm displayed morphological homology with other gonochoric cnidarians, and sAC exhibited broad structural and functional conservation across this phylum. These results indicate a conserved role for pH-dependent sAC-cAMP-PKA signalling in sperm motility across coral sexual systems, and suggest that the role of this pathway in sperm motility may be ancestral in metazoans. Finally, the dynamics of this pH-sensitive pathway may play a critical role in determining the sensitivity of marine invertebrate reproduction to anthropogenic ocean acidification.

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Section: (D) Cnidarian Sac Homologues Display Broad Structural and Fu...mentioning

confidence: 99%

Characterization of a sperm motility signalling pathway in a gonochoric coral suggests conservation across cnidarian sexual systems

Glass,

Ashey,

Okongwu

et al. 2023

Proc. R. Soc. B.

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Fertilisation kinetics among common Indo-Pacific broadcast spawning corals with distinct and shared functional traits

Buccheri,

Ricardo,

Babcock

et al. 2023

Coral Reefs

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Indo-Pacific corals predominantly reproduce using synchronous mass spawning events to maximise fertilisation. However, as disturbances continue to thin population densities, the quantities of gametes released declines and colonies become more isolated, reducing the likelihood of cross-fertilisation. Local hydrodynamic conditions can promote or inhibit gamete contact; thus, the interaction between the abiotic environment and sperm density will determine the amount of time gametes interact. In this study, we investigated the sensitivity of reproduction to manipulations of two key limiting factors of fertilisation: sperm concentration and contact time between gametes. We explored fertilisation kinetics of phylogenetically and functionally similar and diverse coral taxa on the Great Barrier Reef and Western Australia (Acropora digitifera, A. tenuis; Coelastrea aspera, Platygyra daedalea). Results indicate that fertilisation is optimised at sperm concentrations > 103 sperm mL−1 and contact times > 30 s, but the extent of these relationships is species-specific. All species showed clear differences in fertilisation success across contact times, although these differences were less distinct for A. tenuis and P. daedalea at very high sperm concentrations. Acropora digitifera and P. daedalea exhibited nonlinear trends with steep slopes of increased fertilisation success once sperm concentration surpassed values of 104 sperm mL−1 and 102 sperm mL−1, respectively, followed by slight declines. Acropora tenuis and A. digitifera had the highest maximum fertilisation success, likely owing to beneficial evolved functional traits like large egg sizes. The present analysis underpins studies of fertilisation kinetics in natural reef populations to help inform management and restoration practices that assist population resilience and recovery.

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Parental exposure to ocean acidification impacts gamete production and physiology but not offspring performance in Nematostella vectensis

et al. 2023

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Ocean acidification (OA) resulting from anthropogenic CO2 emissions is impairing the reproduction of marine organisms. While parental exposure to OA can protect offspring via carryover effects, this phenomenon is poorly understood in many marine invertebrate taxa. Here, we examined how parental exposure to acidified (pH 7.40) versus ambient (pH 7.72) seawater influenced reproduction and offspring performance across six gametogenic cycles (13 weeks) in the estuarine sea anemone Nematostella vectensis. Females exhibited reproductive plasticity under acidic conditions, releasing significantly fewer but larger eggs compared to ambient females after four weeks of exposure, and larger eggs in two of the four following spawning cycles despite recovering fecundity, indicating long-term acclimatization and greater investment in eggs. Males showed no changes in fecundity under acidic conditions, but produced a greater percentage of sperm with high mitochondrial membrane potential (MMP; a proxy for elevated motility), which corresponded with higher fertilization rates relative to ambient males. Finally, parental exposure to acidic conditions did not significantly influence offspring development rates, respiration rates, or heat tolerance. Overall, this study demonstrates that parental exposure to acidic conditions impacts gamete production and physiology but not offspring performance in N. vectensis, suggesting that increased investment in individual gametes may promote fitness.

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The effects of temperature and pH on the reproductive ecology of sand dollars and sea urchins: Impacts on sperm swimming and fertilization

Cited by 4 publications

References 120 publications

Characterization of a sperm motility signalling pathway in a gonochoric coral suggests conservation across cnidarian sexual systems

Characterization of a sperm motility signalling pathway in a gonochoric coral suggests conservation across cnidarian sexual systems

Fertilisation kinetics among common Indo-Pacific broadcast spawning corals with distinct and shared functional traits

Parental exposure to ocean acidification impacts gamete production and physiology but not offspring performance in Nematostella vectensis

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