Sperm morphology of the Rattini – are the interspecific differences due to variation in intensity of intermale sperm competition?
Tessa Pahl A , Hanna J. McLennan A , Yun Wang A , Anang S. Achmadi B , Kevin C. Rowe C D , Ken Aplin E and William G. Breed A F GA Adelaide Medical School, Faculty of Health and Medical Sciences & The Robinson Research Institute, The University of Adelaide, SA 5005, Australia.
B Museum Zoologicum Bogoriense, Research Center for Biology, Cibinong, Jawa Barat, Indonesia.
C Natural Sciences Department, Museums Victoria, Vic. 3001, Australia.
D School of Biosciences, University of Melbourne, Melbourne, Vic. 3010, Australia.
E Australian Museum, 1 William Street, Sydney, NSW 2010, Australia.
F School of Biological Sciences, Faculty of Sciences, The University of Adelaide, SA 5005, Australia.
G Corresponding author. Email: bill.breed@adelaide.edu.au
Reproduction, Fertility and Development 30(11) 1434-1442 https://doi.org/10.1071/RD17431
Submitted: 17 October 2017 Accepted: 5 April 2018 Published: 18 May 2018
Abstract
It is widely accepted that in mammals a causal relationship exists between postcopulatory sexual selection and relative testes mass of the species concerned, but how much it determines sperm size and shape is debatable. Here we detailed for the largest murine rodent tribe, the Rattini, the interspecific differences in relative testes mass and sperm form. We found that residual testes mass correlates with sperm head apical hook length as well as its angle, together with tail length, and that within several lineages a few species have evolved highly divergent sperm morphology with a reduced or absent apical hook and shorter tail. Although most species have a relative testes mass of 1–4%, these derived sperm traits invariably co-occur in species with much smaller relative testes mass. We therefore suggest that high levels of intermale sperm competition maintain a sperm head with a long apical hook and long tail, whereas low levels of intermale sperm competition generally result in divergent sperm heads with a short or non-existent apical hook and shorter tail. We thus conclude that sexual selection is a major selective force in driving sperm head form and tail length in this large tribe of murine rodents.
Additional keywords: Murid rodents, sexual selection, sperm evolution.
References
Achmadi, A. S., Esselstyn, J. A., Rowe, K. C., Maryanto, I., and Abdullah, M. T. (2013). Phylogeny, diversity, and biogeography of Southeast Asian spiny rats (Maxomys). J. Mammal. 94, 1412–1423.| Phylogeny, diversity, and biogeography of Southeast Asian spiny rats (Maxomys).Crossref | GoogleScholarGoogle Scholar |
Achmadi, A. S., Rowe, K. C., and Esselstyn, J. A. (2014). New records of two rarely encountered, endemic rats (Rodentia: Muridae: Murinae) from Gunung Gandangdewata, West Sulawesi Province. Treubia. 41, 51–60.
| New records of two rarely encountered, endemic rats (Rodentia: Muridae: Murinae) from Gunung Gandangdewata, West Sulawesi Province.Crossref | GoogleScholarGoogle Scholar |
Bedford, J. M. (2004). Enigmas of mammalian gamete form and function. Biol Rev Camb Philos Soc 79, 429–460.
| Enigmas of mammalian gamete form and function.Crossref | GoogleScholarGoogle Scholar |
Bedford, J. M. (2014). Singular features of fertilization and their impact on the male reproductive system in eutherian mammals. Reproduction 147, R43–R52.
| Singular features of fertilization and their impact on the male reproductive system in eutherian mammals.Crossref | GoogleScholarGoogle Scholar |
Bergstrom, C. T., and Dugatkin, L. A. (2012). ‘Evolution’. (W. W. Norton & Company: New York.)
Birkhead, T. R., and Møller, A. P. (Eds) (1998). ‘Sperm Competition and Sexual Selection’. (Academic Press: San Diego, California.)
Birkhead, T. R., Hosken, D. J., and Pitnick, S. (Eds) (2009). ‘Sperm Biology: An Evolutionary Perspective’. (Academic Press: Amsterdam.)
Breed, W. G. (1993). Novel organization of the spermatozoon in two species of murid rodents from southern Asia. J. Reprod. Fertil. 99, 149–158.
| Novel organization of the spermatozoon in two species of murid rodents from southern Asia.Crossref | GoogleScholarGoogle Scholar |
Breed, W. G. (1998). Interspecific variation in structural organisation of the spermatozoon in the Asian bandicoot rats, Bandicota species (family Muridae). Acta Zool. 79, 277–285.
| Interspecific variation in structural organisation of the spermatozoon in the Asian bandicoot rats, Bandicota species (family Muridae).Crossref | GoogleScholarGoogle Scholar |
Breed, W. G. (2004). The spermatozoon of Eurasian murine rodents: its morphological diversity and evolution. J. Morphol. 261, 52–69.
| The spermatozoon of Eurasian murine rodents: its morphological diversity and evolution.Crossref | GoogleScholarGoogle Scholar |
Breed, W. G., and Musser, G. G. (1991). Sulawesi and Philippine rodents (Muridae): a survey of spermatozoal morphology and its significance for phylogenetic inference. Am. Mus. Novit. 3003, 1–15.
Breed, W. G., and Taylor, J. (2000). Body mass, testes mass, and sperm size in murine rodents. J. Mammal. 81, 758–768.
| Body mass, testes mass, and sperm size in murine rodents.Crossref | GoogleScholarGoogle Scholar |
Burgin, C. J., Colella, J. P., Kahn, P. L., and Upham, N. S. (2018). How many species of mammals are there? J. Mammal. 99, 1–11.
| How many species of mammals are there?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 |
Cummins, J. M., and Woodall, P. F. (1985). On mammalian sperm dimensions. J. Reprod. Fertil. 75, 153–175.
| On mammalian sperm dimensions.Crossref | GoogleScholarGoogle Scholar |
Dorman, F., Balsamo, P., Leigh, C., and Breed, W. G. (2014). Co-evolution of gametes of the greater bandicoot rat, Bandicota indica – a murine rodent from South-East Asia. Acta Zool. 95, 392–396.
| Co-evolution of gametes of the greater bandicoot rat, Bandicota indica – a murine rodent from South-East Asia.Crossref | GoogleScholarGoogle Scholar |
Drew, S., Leigh, C., and Breed, W. G. (2014). Spermatozoa of the old endemic rodents of Australia – the possible functional significance of their ventral processes. Reprod. Fertil. Dev. 26, 1183–1187.
| Spermatozoa of the old endemic rodents of Australia – the possible functional significance of their ventral processes.Crossref | GoogleScholarGoogle Scholar |
Esselstyn, J. A., Achmadi, A. S., and Rowe, K. C. (2012). Evolutionary novelty in a rat with no molars. Biol. Lett. 8, 990–993.
| Evolutionary novelty in a rat with no molars.Crossref | GoogleScholarGoogle Scholar |
Esselstyn, J. A., Achmadi, A. S., Handika, H., and Rowe, K. C. (2015). A hog-nosed shrew rat (Rodentia: Muridae) from Sulawesi Island, Indonesia. J. Mammal. 96, 895–907.
| A hog-nosed shrew rat (Rodentia: Muridae) from Sulawesi Island, Indonesia.Crossref | GoogleScholarGoogle Scholar |
Fabre, P.-H., Hautier, L., Dimitrov, D., and Douzery, E. J. P. (2012). A glimpse on the pattern of rodent diversification: a phylogenetic approach. BMC Evol. Biol. 12, 88–106.
| A glimpse on the pattern of rodent diversification: a phylogenetic approach.Crossref | GoogleScholarGoogle Scholar |
Fabre, P. H., Pages, M., Musser, G. G., Fitriana, Y. S., Fjeldsa, J., Jennings, A., Jonsson, K. A., Kennedy, J., Michaux, J., Semiadi, G., Supriatna, N., and Helgen, K. M. (2013). A new genus of rodent from Wallacea (Rodentia: Muridae: Murinae: Rattini), and its implication for biogeography and Indo–Pacific Rattini systematics. Zool. J. Linn. Soc. 169, 408–447.
| A new genus of rodent from Wallacea (Rodentia: Muridae: Murinae: Rattini), and its implication for biogeography and Indo–Pacific Rattini systematics.Crossref | GoogleScholarGoogle Scholar |
Ferres, K. M., McPherson, N. O., Lane, M., Bakos, H. W., Kind, K. L., and Breed, W. G. (2018). Gamete cryopreservation of Australian “old endemic” rodents – spermatozoa from the plains mouse (Pseudomys australis) and the spinifex hopping mouse (Notomys alexis). Aust. Mammal. 40, 76–83.
| Gamete cryopreservation of Australian “old endemic” rodents – spermatozoa from the plains mouse (Pseudomys australis) and the spinifex hopping mouse (Notomys alexis).Crossref | GoogleScholarGoogle Scholar |
Gage, M. J. G. (1998). Mammalian sperm morphometry. Proc. R. Soc. Lond. B 265, 97–103.
| Mammalian sperm morphometry.Crossref | GoogleScholarGoogle Scholar |
Gage, M. J., and Freckleton, R. P. (2003). Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length. Proc. R. Soc. Lond. B 270, 625–632.
| Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length.Crossref | GoogleScholarGoogle Scholar |
Gomendio, M., and Roldan, E. R. S. (1991). Sperm competition influences sperm size in mammals. Proc. R. Soc. Lond. B 243, 181–185.
| Sperm competition influences sperm size in mammals.Crossref | GoogleScholarGoogle Scholar |
Gomendio, M., and Roldan, E. R. S. (2008). Implications of diversity in sperm size and function for sperm competition and fertility. Int. J. Dev. Biol. 52, 439–447.
| Implications of diversity in sperm size and function for sperm competition and fertility.Crossref | GoogleScholarGoogle Scholar |
Gómez Montoto, L., Magaña, C., Tourmente, M., Martín-Coello, J., Crespo, C., Luque-Larena, J. J., Gomendio, M., and Roldan, E. R. S. (2011a). 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 |
Gómez Montoto, L., Sánchez, M. V., Tourmente, M., Martín-Coello, J., Luque-Larena, J. J., Gomendio, M., and Roldan, E. R. S. (2011b). Sperm competition differentially affects swimming velocity and size of spermatozoa from closely related muroid rodents: head first. Reproduction 142, 819–830.
| Sperm competition differentially affects swimming velocity and size of spermatozoa from closely related muroid rodents: head first.Crossref | GoogleScholarGoogle Scholar |
Harcourt, A. H., Harvey, P. H., Larson, S. G., and Short, R. V. (1981). Testis weight, body weight and breeding system in primates. Nature 293, 55–57.
| Testis weight, body weight and breeding system in primates.Crossref | GoogleScholarGoogle Scholar |
Hosken, D. J. (1997). Sperm competition in bats. Proc. R. Soc. Lond. B 264, 385–392.
| Sperm competition in bats.Crossref | GoogleScholarGoogle Scholar |
Humphries, S., Evans, J. P., and Simmons, L. W. (2008). Sperm competition: linking form to function. BMC Evol. Biol. 8, 319.
| Sperm competition: linking form to function.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 |
Immler, S., Pitnick, S., Parker, G. A., Durrant, K. L., Lupold, S., Calhim, S., and Birkhead, T. R. (2011). Resolving variation in the reproductive tradeoff between sperm size and number. Proc. Natl. Acad. Sci. USA 108, 5325–5330.
| Resolving variation in the reproductive tradeoff between sperm size and number.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 |
Kenagy, G. J., and Trombulak, S. C. (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 |
Lalli, M., and Clermont, Y. (1981). Structural changes of the head components of the rat spermatid during late spermiogenesis. Am. J. Anat. 160, 419–434.
| Structural changes of the head components of the rat spermatid during late spermiogenesis.Crossref | GoogleScholarGoogle Scholar |
Lecompte, E., Aplin, K., Denys, C., Catzeflis, F., Chades, M., and Chevret, P. (2008). Phylogeny and biogeography of African Murinae based on mitochondrial and nuclear gene sequences, with a new tribal classification of the subfamily. BMC Evol. Biol. 8, 199.
| Phylogeny and biogeography of African Murinae based on mitochondrial and nuclear gene sequences, with a new tribal classification of the subfamily.Crossref | GoogleScholarGoogle Scholar |
Lüpold, S., Linz, G. M., Rivers, J. W., Westneat, D. F., and Birkhead, T. R. (2009). Sperm competition selects beyond relative testes size in birds. Evolution 63, 391–402.
| Sperm competition selects beyond relative testes size in birds.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 |
(a) Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘Gateway Computing Environments Workshop (GCE)’. pp. 1–8. (Institute of Electrical and Electronics Engineers.)
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. (2014). A systematic review of Sulawesi Bunomys (Muridae, Murinae) with the description of two new species. Bull. Am. Mus. Nat. Hist. 392, 1–313.
| A systematic review of Sulawesi Bunomys (Muridae, Murinae) with the description of two new species.Crossref | GoogleScholarGoogle Scholar |
Musser, G. G., and Carleton, M. D. (2005). Superfamily Muroidea. In ‘Mammal Species of the World: A Taxonomic and Geographic Reference Vol. 2’. 3rd edn. (Eds D. E. Wilson and D. M. Reeder.) pp. 894–1531. (Johns Hopkins University Press: Baltimore.)
Oko, R., and Clermont, Y. (1988). Isolation, structure and protein composition of the perforatorium of rat spermatozoa. Biol. Reprod. 39, 673–687.
| Isolation, structure and protein composition of the perforatorium of rat spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Pagès, M., Chaval, Y., Herbreteau, V., Waengsothorn, S., Cosson, J. F., Hugot, J. P., Morand, S., and Michaux, J. (2010). Revisiting the taxonomy of the Rattini tribe: a phylogeny-based delimitation of species boundaries. BMC Evol. Biol. 10, 184.
| Revisiting the taxonomy of the Rattini tribe: a phylogeny-based delimitation of species boundaries.Crossref | GoogleScholarGoogle Scholar |
Pagès, M., Fabre, P. H., Chaval, Y., Mortelliti, A., Nicolas, V., Wells, K., Michaux, J. R., and Lazzari, V. (2016). Molecular phylogeny of South-East Asian arboreal murine rodents. Zool. Scr. 45, 349–364.
| Molecular phylogeny of South-East Asian arboreal murine rodents.Crossref | GoogleScholarGoogle Scholar |
Parker, G. A. (1970). Sperm competition and its evolutionary consequences in insects. Biol. Rev. Camb. Philos. Soc. 45, 525–567.
| Sperm competition and its evolutionary consequences in insects.Crossref | GoogleScholarGoogle Scholar |
Parker, G. A. (1990). Sperm competition games: raffles and roles. Proc. R. Soc. Lond. B Biol. Sci. 242, 120–126.
| Sperm competition games: raffles and roles.Crossref | GoogleScholarGoogle Scholar |
Parker, G. A. (2016). The evolution of expenditure on testes. J. Zool. 298, 3–19.
| The evolution of expenditure on testes.Crossref | GoogleScholarGoogle Scholar |
Ramm, S. A., and Stockley, P. (2010). Sperm competition and sperm length influence the rate of mammalian spermatogenesis. Biol. Lett. 6, 219–221.
| Sperm competition and sperm length influence the rate of mammalian spermatogenesis.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. R. Soc. B 272, 949–955.
| Sperm competition and the evolution of male reproductive anatomy in rodents.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2017). ‘R: A Language and Environment for Statistical Computing, Version 3.4.1’. (R Foundation for Statistical Computing: Vienna.)
Robins, J. H., McLenachan, P. A., Phillips, M. J., McComish, B. J., Matisoo-Smith, E., and Ross, H. A. (2010). Evolutionary relationships and divergence times among the native rats of Australia. BMC Evol. Biol. 10, 375.
Rowe, K. C., Reno, M. L., Richmond, D. M., Adkins, R. M., and Steppan, S. J. (2008). Pliocene colonization 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 colonization and adaptive radiations in Australia and New Guinea (Sahul): multilocus systematics of the old endemic rodents (Muroidea: Murinae).Crossref | GoogleScholarGoogle Scholar |
Rowe, K. C., Aplin, K. P., Baverstock, P. R., and Moritz, C. (2011). Recent and rapid speciation with limited morphological disparity in the genus Rattus. Syst. Biol. 60, 188–203.
| Recent and rapid speciation with limited morphological disparity in the genus Rattus.Crossref | GoogleScholarGoogle Scholar |
Rowe, K. C., Achmadi, A. S., and Esselstyn, J. A. (2014). Convergent evolution of aquatic foraging in a new genus and species (Rodentia: Muridae) from Sulawesi Island, Indonesia. Zootaxa 3815, 541–564.
| Convergent evolution of aquatic foraging in a new genus and species (Rodentia: Muridae) from Sulawesi Island, Indonesia.Crossref | GoogleScholarGoogle Scholar |
Rowe, K. C., Achmadi, A. S., and Esselstyn, J. A. E. (2016a). A new genus and species of omnivorous rodent (Muridae: Murinae) from Sulawesi, nested within a clade of endemic carnivores. J. Mammal. 97, 978–991.
| A new genus and species of omnivorous rodent (Muridae: Murinae) from Sulawesi, nested within a clade of endemic carnivores.Crossref | GoogleScholarGoogle Scholar |
Rowe, K. C., Achmadi, A. S., and Esselstyn, J. A. (2016b). Repeated evolution of carnivory among Indo–Australian rodents. Evolution 70, 653–665.
| Repeated evolution of carnivory among Indo–Australian rodents.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 |
Smith, T. T., and Yanagimachi, R. (1990). The viability of hamster spermatozoa stored in the isthmus of the oviduct: the importance of sperm–epithelium contact for sperm survival. Biol. Reprod. 42, 450–457.
| The viability of hamster spermatozoa stored in the isthmus of the oviduct: the importance of sperm–epithelium contact for sperm survival.Crossref | GoogleScholarGoogle Scholar |
Snook, R. R. (2005). Sperm in competition: not playing by the numbers. Trends Ecol. Evol. 20, 46–53.
| Sperm in competition: not playing by the numbers.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 |
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
| RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Crossref | GoogleScholarGoogle Scholar |
Steppan, S. J., Adkins, R. M., Spinks, P. Q., and Hale, C. (2005). Multigene phylogeny of the Old World mice, Murinae, reveals distinct geographic lineages and the declining utility of mitochondrial genes compared to nuclear genes. Mol. Phylogenet. Evol. 37, 370–388.
| Multigene phylogeny of the Old World mice, Murinae, reveals distinct geographic lineages and the declining utility of mitochondrial genes compared to nuclear genes.Crossref | GoogleScholarGoogle Scholar |
Suarez, S. S. (1987). Sperm transport and motility in the mouse oviduct: observations in situ. Biol. Reprod. 36, 203–210.
| Sperm transport and motility in the mouse oviduct: observations in situ.Crossref | GoogleScholarGoogle Scholar |
Thitipramote, N., Suwanjarat, J., and Breed, W. G. (2009). Reproductive biology of the greater bandicoot rat Bandicota indica (Rodentia: Muridae) in the rice fields of southern Thailand. Curr. Zool. 55, 48–55.
Thitipramote, N., Suwanjarat, J., Leigh, C., and Breed, W. G. (2011). Variation in sperm morphology of a murine rodent from South-East Asia: the greater bandicoot rat, Bandicota indica. Acta Zool. 92, 201–205.
| Variation in sperm morphology of a murine rodent from South-East Asia: the greater bandicoot rat, Bandicota indica.Crossref | GoogleScholarGoogle Scholar |
Tourmente, M., Gomendio, M., and Roldan, E. R. (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 |
Tourmente, M., Zarka Trigo, D., and Roldan, E. R. S. (2016). Is the hook of muroid rodent’s sperm related to sperm train formation? J. Evol. Biol. 29, 1168–1177.
| Is the hook of muroid rodent’s sperm related to sperm train formation?Crossref | GoogleScholarGoogle Scholar |
Varea-Sánchez, M., Tourmente, M., Bastir, M., and Roldan, E. R. (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 |