Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Interspecific diversity of testes mass and sperm morphology in the Philippine chrotomyine rodents: implications for differences in breeding systems across the species

William G. Breed https://orcid.org/0000-0003-1739-6593 A C E , Hazirah Hassan A D , Macarena Gonzalez A , Hanna J. McLennan A , Chris M. Leigh A and Lawrence R. Heaney B
+ Author Affiliations
- Author Affiliations

A Robinson Research Institute, School of Medicine, The University of Adelaide, Adelaide, SA 5005, Australia.

B Field Museum of Natural History, Division of Mammals, 1400 South Lake Shore Drive, Chicago, Illinois 60605, USA.

C Present address: School of Biological Sciences, The University of Adelaide, Adelaide, SA 5005, Australia.

D Present address: Department of Biochemistry, Faculty of Medicine, Universiti Kebangsaan Malaysia, 56000 Cheras, Kuala Lumpur, Malaysia.

E Corresponding author. Email: bill.breed@adelaide.edu.au

Reproduction, Fertility and Development 31(4) 705-711 https://doi.org/10.1071/RD18278

Abstract

The high diversity of native Philippine murid rodents includes an old endemic group, the chrotomyines, which are the sister group of the Australasian hydromyines. Herein we detail their interspecific diversity of relative testes mass (RTM) and sperm morphology. We find that in chrotomyines, as in the Australasian hydromyines, testes mass relative to body mass differs by an order of magnitude across the species and ranges from a large RTM in Soricomys and Chrotomys species to a small RTM in Apomys. Sperm morphology is associated with these findings, with individuals in species of Soricomys and Chrotomys producing relatively larger spermatozoa with a prominent apical hook and long tail, whereas, by contrast, the Apomys species have a sperm head that either has a very short or no apical hook and a shorter tail. These findings indicate coevolution of RTM with sperm morphological traits across the species, with the marked interspecific differences in RTM suggesting differences in the intensity of intermale sperm competition and hence breeding system. Thus, we hypothesise that species of Soricomys and Chrotomys that produce more streamlined spermatozoa with longer tails have a polyandrous or promiscuous mating system, whereas the Apomys species, which produce smaller and less streamlined spermatozoa, may exhibit monogamy.

Additional keywords: mating system, Philippine rodents, sexual selection, testis size.


References

Bauer, M., and Breed, W. G. (2008). Testis mass of the spinifex hopping mouse and its impact on fertility potential. J. Zool. (Lond.) 274, 349–356.
Testis mass of the spinifex hopping mouse and its impact on fertility potential.Crossref | GoogleScholarGoogle Scholar |

Birkhead, T. R., and Møller, P. (1998) ‘Sperm Competition and Sexual Selection.’ (Academic Press: London.)

Birkhead, T. R., Hosken, D. J., and Pitnick, S. (2009). ‘Sperm Biology: An Evolutionary Perspective.’ (Academic Press: Amsterdam.)

Breed, W. G. (1997). Interspecific variation of testis size and epididymal sperm numbers in Australasian rodents with special reference to the Genus Notomys. Aust. J. Zool. 45, 651–669.
Interspecific variation of testis size and epididymal sperm numbers in Australasian rodents with special reference to the Genus Notomys.Crossref | GoogleScholarGoogle Scholar |

Breed, W. G., and Leigh, C. M. (2010). The spermatozoon of the Old Endemic Australo-Papuan and Philippine rodents – its morphological diversity and evolution. Acta Zool. 91, 279–294.
The spermatozoon of the Old Endemic Australo-Papuan and Philippine rodents – its morphological diversity and evolution.Crossref | GoogleScholarGoogle Scholar |

Breed, W. G., and Taylor, J. (2000). Body size, testes mass, and sperm size in murine rodents. J. Mammal. 81, 758–768.
Body size, testes mass, and sperm size in murine rodents.Crossref | GoogleScholarGoogle Scholar |

Briskie, J. V., Montgomerie, R., and Birkhead, T. R. (1997). The evolution of sperm size in birds. Evolution 51, 937–945.
The evolution of sperm size in birds.Crossref | GoogleScholarGoogle Scholar |

Byrne, P. G., Simmons, L. W., and Roberts, J. D. (2003). Sperm competition and the evolution of gamete morphology in frogs. Proc. Biol. Sci. 270, 2079–2086.
Sperm competition and the evolution of gamete morphology in frogs.Crossref | GoogleScholarGoogle Scholar |

Calhim, S., Immler, S., and Birkhead, T. R. (2007). Postcopulatory sexual selection is associated with reduced variation in sperm morphology. PLoS One 2, e413.
Postcopulatory sexual selection is associated with reduced variation in sperm morphology.Crossref | GoogleScholarGoogle Scholar |

Gomendio, M., and Roldan, E. R. S. (1991). Sperm competition influences sperm size in mammals. Proc. Biol. Sci. 243, 181–185.
Sperm competition influences sperm size in mammals.Crossref | GoogleScholarGoogle Scholar |

Gómez Montoto, L., Varea Sánchez, M., Tourmente, M., Martín-Coello, J., Luque-Larena, J. J., Gomendio, M., and Roldan, E. R. (2011a). Sperm competition differently affects swimming velocity and size of spermatozoa from closely related muroid rodents. Reproduction 142, 819–830.
Sperm competition differently affects swimming velocity and size of spermatozoa from closely related muroid rodents.Crossref | GoogleScholarGoogle Scholar |

Gómez Montoto, L., Magana, C., Tourmente, M., Martin-Coello, J., Crespo, C., Luque-Larena, J. J., Gomendio, M., and Roldan, E. R. S. (2011b). Sperm competition, sperm numbers and sperm quality in muroid rodents. PLoS One 6, e18173.
Sperm competition, sperm numbers and sperm quality in muroid rodents.Crossref | GoogleScholarGoogle Scholar |

Harcourt, A. H., Harvey, P. S., Larson, S. G., and Short, R. V. (1981). Testes weight, body weight, and breeding systems in primates. Nature 293, 55–57.
Testes weight, body weight, and breeding systems in primates.Crossref | GoogleScholarGoogle Scholar |

Heaney, L. R., Balete, D. S., Rickart, E. A., Alviola, P. A., Duya, M. R. M., Duya, M. V., Veluz, M. J., Van de Vrede, L., and Steppan, S. J. (2011). Chapter 1: seven new species and a new subgenus of forest mice (Rodentia: Muridae: Apomys) from Luzon Island. Fieldiana Life Earth Sci. 2, 1–60.
Chapter 1: seven new species and a new subgenus of forest mice (Rodentia: Muridae: Apomys) from Luzon Island.Crossref | GoogleScholarGoogle Scholar |

Heaney, L. R., Balete, D. S., and Rickart, E. A. (2016a). ‘The Mammals of Luzon Island: Biogeography and Natural History of a Philippine Fauna.’ (Johns Hopkins University Press: Baltimore.)

Heaney, L. R., Balete, D. S., Duya, M. R. M., Duya, M. V., Jansa, S. A., Steppan, S. J., and Rickart, E. A. (2016b). Doubling diversity: a cautionary tale of previously unsuspected mammalian diversity on a tropical oceanic island. Front. Biogeogr. 8, e29667.
Doubling diversity: a cautionary tale of previously unsuspected mammalian diversity on a tropical oceanic island.Crossref | GoogleScholarGoogle Scholar |

Hosken, D. J. (1997). Sperm competition in bats. Proc. Biol. Sci. 264, 385–392.
Sperm competition in bats.Crossref | GoogleScholarGoogle Scholar |

Immler, S., Moore, H. D. M., Breed, W. G., and Birkhead, T. R. (2007). By hook or by crook? Morphometry, competition and cooperation in rodent sperm. PLoS One 2, e170.
By hook or by crook? Morphometry, competition and cooperation in rodent sperm.Crossref | GoogleScholarGoogle Scholar |

Jansa, S. A., Barker, F. K., and Heaney, L. R. (2006). The pattern and timing of diversification of Philippine endemic rodents: evidence from mitochondrial and nuclear gene sequences. Syst. Biol. 55, 73–88.
The pattern and timing of diversification of Philippine endemic rodents: evidence from mitochondrial and nuclear gene sequences.Crossref | GoogleScholarGoogle Scholar |

Justiniano, R., Schenk, J. J., Balete, D. S., Rickart, E. A., Esselstyn, J. A., Heaney, L. R., and Steppan, S. J. (2015). Testing diversification models of endemic Philippine forest mice (Apomys) with nuclear phylogenies across elevational gradients reveals repeated colonization of isolated mountain ranges. J. Biogeogr. 42, 51–64.
Testing diversification models of endemic Philippine forest mice (Apomys) with nuclear phylogenies across elevational gradients reveals repeated colonization of isolated mountain ranges.Crossref | GoogleScholarGoogle Scholar |

Kenagy, G. J., and Trombulak, S. G. (1986). Size and function of mammalian testes in relation to body size. J. Mammal. 67, 1–22.
Size and function of mammalian testes in relation to body size.Crossref | GoogleScholarGoogle Scholar |

Kyriazis, C. C., Bates, J. M., and Heaney, L. R. (2017). Dynamics of genetic and morphological diversification in an incipient intra-island radiation of Philippine rodents (Muridae: Bullimus). J. Biogeogr. 44, 2585–2594.
Dynamics of genetic and morphological diversification in an incipient intra-island radiation of Philippine rodents (Muridae: Bullimus).Crossref | GoogleScholarGoogle Scholar |

McLennan, H. J., Lüpold, S., Smissen, P., Rowe, K. C., and Breed, W. G. (2017). Greater sperm complexity in the Australasian old endemic rodents (Tribe: Hydromyini) is associated with increased levels of inter-male sperm competition. Reprod. Fertil. Dev. 29, 921–930.
Greater sperm complexity in the Australasian old endemic rodents (Tribe: Hydromyini) is associated with increased levels of inter-male sperm competition.Crossref | GoogleScholarGoogle Scholar |

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

Musser, G. G., and Heaney, L. R. (1992). Philippine rodents: definitions of Tarsomys and Limnomys plus a preliminary assessment of phylogenetic patterns among native Philippine murines (Murinae, Muridae). Bull. Am. Mus. Nat. Hist. 211, 1–136.

Pahl, T., McLennan, H. J., Wang, Y., Achmedi, A. S., Rowe, K. C., Aplin, K., and Breed, W. G. (2018). Sperm morphology in the Rattini – are the interspecific differences due to variation in intensity of intermale sperm competition. Reprod. Fertil. Dev. 30, 1434–1442.
Sperm morphology in the Rattini – are the interspecific differences due to variation in intensity of intermale sperm competition.Crossref | GoogleScholarGoogle Scholar |

Parker, G. A. (1982). Why are there so many tiny sperm? Sperm competition and the maintenance of the two sexes. J. Theor. Biol. 96, 281–294.
Why are there so many tiny sperm? Sperm competition and the maintenance of the two sexes.Crossref | GoogleScholarGoogle Scholar |

Parker, G. A. (1990). Sperm competition: raffles and roles. Proc. Biol. Sci. 242, 120–126.
Sperm competition: raffles and roles.Crossref | GoogleScholarGoogle Scholar |

Parker, G. A. (2016). The evolution of expenditure on testes. J. Zool. (Lond.) 298, 3–19.
The evolution of expenditure on testes.Crossref | GoogleScholarGoogle Scholar |

Ramm, S. A., and Schärer, L. (2014). The evolutionary ecology of testicular function: size isn’t everything. Biol. Rev. Camb. Philos. Soc. 89, 874–888.
The evolutionary ecology of testicular function: size isn’t everything.Crossref | GoogleScholarGoogle Scholar |

Ramm, S. A., Parker, G. A., and Stockley, P. (2005). Sperm competition and the evolution of male reproductive anatomy in rodents. Proc. Biol. Sci. 272, 949–955.
Sperm competition and the evolution of male reproductive anatomy in rodents.Crossref | GoogleScholarGoogle Scholar |

Rowe, K. C., Reno, M. L., Richmond, D. M., Adkins, R. M., and Steppan, S. J. (2008). Pliocene colonisation and adaptive radiations in Australia and New Guinea (Sahul): multilocus systematics of the old endemic rodents (Muroidea: Murinae). Mol. Phylogenet. Evol. 47, 84–101.
Pliocene colonisation and adaptive radiations in Australia and New Guinea (Sahul): multilocus systematics of the old endemic rodents (Muroidea: Murinae).Crossref | GoogleScholarGoogle Scholar |

Rowsey, D. M., Heaney, L. R., and Jansa, S. A. (2018). Diversification rates of the ‘Old Endemic’ murine rodents of Luzon Island, Philippines, are inconsistent with incumbency and ecological opportunity. Evolution 72, 1420–1435.
Diversification rates of the ‘Old Endemic’ murine rodents of Luzon Island, Philippines, are inconsistent with incumbency and ecological opportunity.Crossref | GoogleScholarGoogle Scholar |

Šandera, M., Albrecht, T., and Stopka, P. (2013). Variation in apical hook length reflects the intensity of sperm competition in murine rodents. PLoS One 8, e68427.
Variation in apical hook length reflects the intensity of sperm competition in murine rodents.Crossref | GoogleScholarGoogle Scholar |

Simmons, L. W., and Fitzpatrick, J. L. (2012). Sperm wars and the evolution of male fertility. Reproduction 144, 519–534.
Sperm wars and the evolution of male fertility.Crossref | GoogleScholarGoogle Scholar |

Smissen, P. J., and Rowe, K. C. (2018). Repeated biome transitions in the evolution of Australian rodents. Mol. Phylogenet. Evol. 128, 182–191.
Repeated biome transitions in the evolution of Australian rodents.Crossref | GoogleScholarGoogle Scholar |

Soulsbury, C. D. (2010). Genetic patterns of paternity and testes size in mammals. PLoS One 5, e9581.
Genetic patterns of paternity and testes size in mammals.Crossref | GoogleScholarGoogle Scholar |

Steppan, S. J., and Schenk, J. J. (2017). Muroid rodent phylogenetics: 900-species tree reveals increasing diversification rates. PLoS One 12, e0183070.
Muroid rodent phylogenetics: 900-species tree reveals increasing diversification rates.Crossref | GoogleScholarGoogle Scholar |

Tourmente, M., Gomendio, M., and Roldan, E. R. S. (2011). Sperm competition and the evolution of sperm design in mammals. BMC Evol. Biol. 11, 12.
Sperm competition and the evolution of sperm design in mammals.Crossref | GoogleScholarGoogle Scholar |

van der Horst, G., and Maree, L. (2014). Sperm form and function in absence of sperm competition. Mol. Reprod. Dev. 81, 204–216.
Sperm form and function in absence of sperm competition.Crossref | GoogleScholarGoogle Scholar |

van der Horst, G., Maree, L., Kotzé, S. H., and O’Riain, M. J. (2011). Sperm structure and motility in the eusocial naked mole-rat Heterocephlus glaber: a case of degenerative orthogenesis in the absence of sperm competition. BMC Evol. Biol. 11, 351.
Sperm structure and motility in the eusocial naked mole-rat Heterocephlus glaber: a case of degenerative orthogenesis in the absence of sperm competition.Crossref | GoogleScholarGoogle Scholar |

Varea-Sánchez, M., Tourmente, M., Bastir, M., and Roldan, E. R. S. (2016). Unraveling the sperm bauplan: relationships between sperm head morphology and sperm function in rodents. Biol. Reprod. 95, 25.
Unraveling the sperm bauplan: relationships between sperm head morphology and sperm function in rodents.Crossref | GoogleScholarGoogle Scholar |