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Paternal nutrient provisioning during male pregnancy in the seahorse Hippocampus abdominalis

Abstract

Vertebrates that incubate embryos on or within the body cavity exhibit diverse strategies to provide nutrients to developing embryos, ranging from lecithotrophy (solely yolk-provided nutrition) to substantial matrotrophy (supplemental nutrients from the mother before birth). Syngnathid fishes (seahorses, pipefishes and sea dragons) are the only vertebrates to exhibit male pregnancy. Therefore, they provide a unique opportunity for comparative evolutionary research, in examining pregnancy independent of the female reproductive tract. Here, we tested the hypothesis that the most complex form of syngnathid pregnancy involves nutrient transport from father to offspring. We compared the dry masses of newly fertilised Hippocampus abdominalis eggs with those of fully developed neonates to derive a patrotrophy index. The patrotrophy index of H. abdominalis was 1, indicating paternal nutrient supplementation to embryos during gestation. We also measured the lipid content of newly fertilised eggs and neonates and found that there was no significant decrease in lipid mass during embryonic development. Since lipids are likely to be the main source of energy during embryonic development, our results suggest that lipid yolk reserves being depleted by embryonic metabolism are replaced by the brooding father. The results of our study support the hypothesis that nutrient transport occurs in the most advanced form of male pregnancy in vertebrates.

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Acknowledgements

We thank the Applied and Evolutionary Zoology Lab, particularly S. Liang, C. Foster, J. Herbert and A. Buddle for assistance with animal husbandry, and S. Dowland, J. Dudley, and S. Khan for assistance with sample collection. We thank M. Emanuel for assistance with lipid extraction training, and M. Thomson for the use of his microscope with camera attachment. This work was supported by a University of Sydney Research Accelerator (SOAR) Prize and Australian Research Council funding (DP180103370) to CMW.

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Correspondence to Camilla M. Whittington.

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All authors declare that they have no conflict of interest.

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All applicable international, national and institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the University of Sydney (University of Sydney Animal Ethics Committee approval number 2018/1302).

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Communicated by Kathrin H. Dausmann.

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Skalkos, Z.M.G., Van Dyke, J.U. & Whittington, C.M. Paternal nutrient provisioning during male pregnancy in the seahorse Hippocampus abdominalis. J Comp Physiol B 190, 547–556 (2020). https://doi.org/10.1007/s00360-020-01289-y

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  • DOI: https://doi.org/10.1007/s00360-020-01289-y

Keywords

  • Brood pouch
  • Dry mass
  • Embryo incubation
  • Lipid mass
  • Matrotrophy
  • Parental care
  • Paternal investment
  • Patrotrophy
  • Syngnathid