Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE (Open Access)

Sperm morphology of the Australasian hydromyine rodents and the interactions between the spermatozoon and oocyte at the time of fertilisation

William G. Breed https://orcid.org/0000-0003-1739-6593 A * , Chris M. Leigh B , Emily Roycroft C and Ingrid Ahmer A
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, Faculty of Sciences, The University of Adelaide, Adelaide, SA 5005, Australia.

B Adelaide Microscopy Unit, The University of Adelaide, Adelaide, SA 5005, Australia.

C School of Biological Sciences, Monash University, Melbourne, Vic, Australia.

* Correspondence to: bill.breed@adelaide.edu.au

Handling Editor: Mark Baker

Reproduction, Fertility and Development 37, RD25012 https://doi.org/10.1071/RD25012
Submitted: 3 February 2025  Accepted: 18 March 2025  Published online: 7 April 2025

© 2025 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context

This paper explores the morphology of spermatozoa in Australian hydromyine rodents, specifically focusing on the plains mouse (Pseudomys australis), and examines the interactions between sperm and eggs at time of fertilisation.

Aims

The aim of this study is to provide an overview of sperm morphology of hydromyine rodents, comparing its morphology across the different species and to investigate the interactions between the gametes at fertilisation in the plains mouse.

Methods

We summarise the sperm head morphology of the hydromyine rodents across the six divisions, with emphasis on the structure in the plains mouse and its interactions with the zona pellucida during fertilisation.

Key results

Most hydromyine rodents, including the plains mouse, exhibit a highly complex sperm head morphology with two prominent ventral processes in addition to the apical hook. These processes primarily contain filamentous actin with some species of the New Guinea Pogonomys Division having a nuclear extension into the lower process. Nevertheless three species in the Pogonomys Division and a few in the Pseudomys Division have derived sperm heads which lack the ventral processes which in the plains mouse bind the sperm to the zona pellucida around the ovulated oocyte. This may stabilise the sperm head at this time and facilitate zona pellucida penetration and fusion with the oolemma at this time.

Conclusion

The complex sperm head morphology in most of the hydromyine rodents is likely to date back over one million years with, in the plains mouse, interaction between sperm and egg during fertilisation involving sperm head stabilisation and zona pellucida attachment.

Implications

These findings suggest in hydromyine rodents valuable insights into the evolutionary development of sperm morphology and sperm-egg interactions during fertilisation, and in particular that the role of the ventral processes may be critical for successful fertilisation in this group. Understanding these processes could give insight into broader studies on reproductive strategies and evolutionary biology in rodents.

Keywords: Australasian rodents, evolution, fertilisation, Hydromyinae, morphology, plains mouse, sperm diversity, sperm-oocyte interactions, ventral processes.

References

Bauer M, Leigh C, Peirce E, Breed WG (2005) Comparative study of sperm chromatin condensation in the excurrent ducts of the laboratory mouse Mus musculus and spinifex hopping mouse Notomys alexis. Reproduction, Fertility and Development 17, 611-616.
| Crossref | Google Scholar |

Breed WG (1983) Variation in sperm morphology in the Australian rodent genus, Pseudomys (Muridae). Cell and Tissue Research 229, 611-625.
| Crossref | Google Scholar |

Breed WG (1984) Sperm head structure in the Hydromyinae (Rodentia:Muridae): a further evolutionary development of the subacrosomal space in mammals. Gamete Research 10, 31-44.
| Crossref | Google Scholar |

Breed WG (1997) Evolution of the spermatozoon in Australasian rodents. Australian Journal of Zoology 45, 459-478.
| Crossref | Google Scholar |

Breed WG, Leigh CM (1991) Distribution of filamentous actin in and around spermatids and in spermatozoa of Australian conilurine rodents. Molecular Reproduction and Development 30, 369-384.
| Crossref | Google Scholar |

Breed WG, Leigh CM (2010) The spermatozoon of the old endemic Australo-Papuan and Philippine rodents – its morphological diversity and evolution. Acta Zoologica 91, 279-294.
| Crossref | Google Scholar |

Breed WG, Idriss D, Oko RJ (2000) Protein composition of the ventral processes on the sperm head of Australian hydromyine rodents. Biology of Reproduction 63, 629-634.
| Crossref | Google Scholar |

Breed WG, Leigh CM, Robertson H, Mantellato L, Lambert C, Jequier A, Matson P (2007) Interspecific variation of sperm morphology in the Australian rodent genus Zyzomys. Acta Zoologica 88, 257-263.
| Crossref | Google Scholar |

Breed WG, Leigh CM, Peirce EJ (2020) Reproductive biology of the mice and rats (Family Muridae) in New Guinea – diversity and evolution. Records of the Australian Museum 72, 303-316.
| Crossref | Google Scholar |

Cummins JM, Woodall PF (1985) On mammalian sperm dimensions. Journal of Reproduction and Fertility 75, 153-175.
| Crossref | Google Scholar |

Drew S, Leigh C, Breed WG (2014) Spermatozoa of the old endemic rodents of Australia – the possible functional significance of their ventral processes. Reproduction, Fertility and Development 26, 1183-1187.
| Crossref | Google Scholar |

Firman RC, Simmons LW (2009) Sperm competition and the evolution of the sperm hook in house mice. Journal of Evolutionary Biology 22, 2505-2511.
| Crossref | Google Scholar |

Firman RC, Bentley B, Bowman F, Marchant FG-S, Parthenay J, Sawyer J, Stewart T, O’Shea JE (2013) No evidence of sperm conjugate formation in an Australian mouse bearing sperm with three hooks. Ecology and Evolution 3(7), 1856-1863.
| Crossref | Google Scholar |

Flaherty SP, Breed WG (1983) The sperm head of the plains mouse, Pseudomys australis: ultrastructure and effects of chemical treatments. Gamete Research 8, 231-244.
| Crossref | Google Scholar |

Flaherty SP, Breed WG (1987) Formation of the ventral hooks on the sperm head of the plains mouse, Pseudomys australis. Gamete Research 17, 115-129.
| Crossref | Google Scholar |

Flaherty SP, Breed WG, Sarafis V (1983) Localization of actin in the sperm head of the plains mouse, Pseudomys australis. Journal of Experimental Biology 225, 497-500.
| Crossref | Google Scholar |

Immler S, Moore HDM, Breed WG, Birkhead TR (2007) By hook or by crook? Morphometry, competition, and cooperation in rodent sperm. PLoS ONE 2(1), e170.
| Crossref | Google Scholar |

Lalli M, Clermont Y (1981) Structural changes of the head components of the rat spermatid during late spermiogenesis. American Journal of Anatomy 160, 419-434.
| Crossref | Google Scholar |

McGregor L, Flaherty SP, Breed WG (1989) Structure of the zona pellucida and cumulus oophorus in three species of native Australian rodents. Gamete Research 23, 279-287.
| Crossref | Google Scholar |

McLennan HJ, Lüpold S, Smissen P, Rowe KC, Breed WG (2017) Greater sperm complexity in the Australasian old endemic rodents (Tribe: Hydromyini) is associated with increased levels of inter-male sperm competition. Reproduction, Fertility and Development 29, 921-930.
| Crossref | Google Scholar |

Moore H, Dvoráková K, Jenkins N, Breed W (2002) Exceptional sperm cooperation in the wood mouse. Nature 418, 174-177.
| Crossref | Google Scholar |

Oko R, Clermont Y (1988) Isolation, structure and protein composition of the perforatorium of rat spermatozoa. Biology of Reproduction 39, 673-687.
| Crossref | Google Scholar |

Pahl T, McLennan HJ, Wang Y, Achmadi AS, Rowe KC, Aplin K, Breed WG (2018) Sperm morphology of the Rattini – are the interspecific differences due to variation in intensity of intermale sperm competition? Reproduction, Fertility and Development 30, 1434-1442.
| Crossref | Google Scholar |

Ramm SA, Stockley P (2010) Sperm competition and sperm length influence the rate of mammalian spermatogenesis. Biology Letters 6, 219-221.
| Crossref | Google Scholar |

Rowe KC, Achmadi AS, Fabre P-H, Schenk JJ, Steppan SJ, Esselstyn JA (2019) Oceanic islands of Wallacea as a source for dispersal and diversification of murine rodents. Journal of Biogeography 46, 2752-2768.
| Crossref | Google Scholar |

Roycroft E, Fabre P-H, MacDonald AJ, Moritz C, Moussalli A, Rowe KC (2022) New Guinea uplift opens ecological opportunity across a continent. Current Biology 32, 4215-4224.e3.
| Crossref | Google Scholar |

Roycroft E, Ford F, Ramm T, Schembri R, Breed WG, Burns PA, Rowe KC, Moritz C (2024) Speciation across biomes: rapid diversification with reproductive isolation in the Australian delicate mice. Molecular Ecology 33, e17301.
| Crossref | Google Scholar |

Šandera M, Andrlíková P, Frolíková M, Stopka P (2011) Changes in the curvature of sperm apical hooks in murine rodents. Biologia 66(5), 916-921.
| Crossref | Google Scholar |

Suarez SS (1987) Sperm transport and motility in the mouse oviduct: observations in situ. Biology of Reproduction 36, 203-210.
| Crossref | Google Scholar |

Suttle JM, Moore HDM, Peirce EJ, Breed WG (1988) Quantitative studies on variation in sperm head morphology of the hopping mouse, Notomys alexis. Journal of Experimental Zoology 247, 166-171.
| Crossref | Google Scholar |

Timothy Smith T, Yanagimachi R (1990) The viability of hamster spermatozoa stored in the isthmus of the oviduct: the importance of sperm – epithelium contact for sperm survival. Biology of Reproduction 42, 450-457.
| Crossref | Google Scholar |

Tourmente M, Zarka-Trigo D, Roldan ERS (2016) Is the hook of muroid rodent’s sperm related to sperm train function? Journal of Evolutionary Biology 29, 1168-1177.
| Crossref | Google Scholar |

Varea-Sanchez M, Tourmente M, Bastir M, Roldan ERS (2016) Unraveling the sperm bauplan: relationships between sperm head morphology and sperm function in rodents. Biology of Reproduction 95(1), 25.
| Crossref | Google Scholar |