Geometric differences between the crania of Australian hopping mice (Notomys, Murinae, Rodentia)
Bader H. AlhajeriA Department of Biological Sciences, Kuwait University, Safat, 13060, Kuwait. Email: bader.alhajeri@ku.edu.kw
Australian Mammalogy 44(1) 24-38 https://doi.org/10.1071/AM20067
Submitted: 17 November 2020 Accepted: 25 January 2021 Published: 1 March 2021
Abstract
Half of the ten Australian hopping mice (Notomys) species have become extinct following the European colonisation of Australia, and most of the rest are threatened. This makes the study of their present diversity paramount. Although recent molecular phylogenies improved our understanding of the relationships among the species, detailed interspecific phenotypic comparisons are still lacking. This is the aim of the present study. Geometric morphometric methods were used to compare the crania of all five extant species (N. alexis, N. aquillo, N. cervinus, N. fuscus, and N. mitchellii) along with the extinct N. longicaudatus. Although previous work (based on traditional approaches) find intragenerically conserved crania, the present study discovers significant differences in cranial size and shape among Notomys species, with the ventral view being more distinct than the dorsal view. There was no evidence of sexual dimorphism in cranial size nor shape, and only a weak allometric effect. Most aspects of cranial shape differed among the species. The extant species pair that differed in cranial shape the most was N. aquilo – N. cervinus, differing in the foramen magnum, tympanic bulla, orbit, incisive foramen, and rostrum, along with cranial width, potentially a consequence of N. cervinus’ phylogenetic position, and N. aquilo’s s ecological uniqueness.
Keywords: Australia, cranial variation, geometric morphometrics, hopping mouse, murine (Murinae), Notomys, rodent, skull.
References
Adams, D., Collyer, M., and Kaliontzopoulou, A. (2020). geomorph: Geometric Morphometric Analyses of 2D/3D Landmark Data. Available at https://cran.r-project.org/package=geomorph/Alhajeri, B. H. (2016). A phylogenetic test of the relationship between saltation and habitat openness in gerbils (Gerbillinae, Rodentia). Mammal Research 61, 231–241.
| A phylogenetic test of the relationship between saltation and habitat openness in gerbils (Gerbillinae, Rodentia).Crossref | GoogleScholarGoogle Scholar |
Alhajeri, B. H. (2018). Craniomandibular Variation in the Taxonomically Problematic Gerbil Genus Gerbillus (Gerbillinae, Rodentia): Assessing the Influence of Climate, Geography, Phylogeny, and Size. Journal of Mammalian Evolution 25, 261–276.
| Craniomandibular Variation in the Taxonomically Problematic Gerbil Genus Gerbillus (Gerbillinae, Rodentia): Assessing the Influence of Climate, Geography, Phylogeny, and Size.Crossref | GoogleScholarGoogle Scholar |
Alhajeri, B. H. (2019). Cranial variation in geographically widespread dwarf gerbil Gerbillus nanus (Gerbillinae, Rodentia) populations: Isolation by distance versus adaptation to local environments. Journal of Zoological Systematics and Evolutionary Research 57, 191–203.
| Cranial variation in geographically widespread dwarf gerbil Gerbillus nanus (Gerbillinae, Rodentia) populations: Isolation by distance versus adaptation to local environments.Crossref | GoogleScholarGoogle Scholar |
Alhajeri, B. H. (2020). A Geometric Morphometric Analysis of Geographic Mandibular Variation in the Dwarf Gerbil Gerbillus nanus (Gerbillinae, Rodentia). Journal of Mammalian Evolution , .
| A Geometric Morphometric Analysis of Geographic Mandibular Variation in the Dwarf Gerbil Gerbillus nanus (Gerbillinae, Rodentia).Crossref | GoogleScholarGoogle Scholar |
Alhajeri, B. H., and Steppan, S. J. (2018a). A phylogenetic test of adaptation to deserts and aridity in skull and dental morphology across rodents. Journal of Mammalogy 99, 1197–1216.
| A phylogenetic test of adaptation to deserts and aridity in skull and dental morphology across rodents.Crossref | GoogleScholarGoogle Scholar |
Alhajeri, B. H., and Steppan, S. J. (2018b). Community structure in ecological assemblages of desert rodents. Biological Journal of the Linnean Society 124, 308–318.
| Community structure in ecological assemblages of desert rodents.Crossref | GoogleScholarGoogle Scholar |
Alhajeri, B. H., and Steppan, S. J. (2018c). Disparity and Evolutionary Rate Do Not Explain Diversity Patterns in Muroid Rodents (Rodentia: Muroidea). Evolutionary Biology 45, 324–344.
| Disparity and Evolutionary Rate Do Not Explain Diversity Patterns in Muroid Rodents (Rodentia: Muroidea).Crossref | GoogleScholarGoogle Scholar |
Balčiauskienė, L. (2007). The growth of captive bred field mice (Apodemus agrarius). Acta Zoologica Lituanica 17, 313–322.
| The growth of captive bred field mice (Apodemus agrarius).Crossref | GoogleScholarGoogle Scholar |
Beolchini, F., and Corti, M. (2004). The taxonomy of the genus Tachyoryctes: A geometric morphometric approach. Italian Journal of Zoology 71, 35–43.
| The taxonomy of the genus Tachyoryctes: A geometric morphometric approach.Crossref | GoogleScholarGoogle Scholar |
Bivand, R., Keitt, T., and Rowlingson, B. (2020). rgdal: Bindings for the ‘Geospatial’ Data Abstraction Library. Available at https://cran.r-project.org/package=rgdal/
Boroni, N. L., Lobo, L. S., Romano, P. S. R., and Lessa, G. (2017). Taxonomic identification using geometric morphometric approach and limited data: An example using the upper molars of two sympatric species of Calomys (Cricetidae: Rodentia). Zoologia 34, e19864.
| Taxonomic identification using geometric morphometric approach and limited data: An example using the upper molars of two sympatric species of Calomys (Cricetidae: Rodentia).Crossref | GoogleScholarGoogle Scholar |
Breed, W. G. (1983). Sexual Dimorphism in the Australian Hopping Mouse, Notomys alexis. Journal of Mammalogy 64, 536–539.
| Sexual Dimorphism in the Australian Hopping Mouse, Notomys alexis.Crossref | GoogleScholarGoogle Scholar |
Breed, W. G. (1985). Morphological variation in the female reproductive tract of Australian rodents in the genera Pseudomys and Notomys. Journal of Reproduction and Fertility 73, 379–384.
| Morphological variation in the female reproductive tract of Australian rodents in the genera Pseudomys and Notomys.Crossref | GoogleScholarGoogle Scholar | 3989792PubMed |
Collyer, M. L., and Adams, D. C. (2018). RRPP: An R package for fitting linear models to high-dimensional data using residual randomization. Methods in Ecology and Evolution 9, 1772–1779.
| RRPP: An R package for fitting linear models to high-dimensional data using residual randomization.Crossref | GoogleScholarGoogle Scholar |
Crossley, D. A., and del Mar Miguélez, M. (2001). Skull size and cheek-tooth length in wild-caught and captive-bred chinchillas. Archives of Oral Biology 46, 919–928.
| Skull size and cheek-tooth length in wild-caught and captive-bred chinchillas.Crossref | GoogleScholarGoogle Scholar | 11451406PubMed |
Diete, R. L., Meek, P. D., Dickman, C. R., and Leung, L. K. P. (2016). Ecology and conservation of the northern hopping-mouse (Notomys aquilo). Australian Journal of Zoology 64, 21–32.
| Ecology and conservation of the northern hopping-mouse (Notomys aquilo).Crossref | GoogleScholarGoogle Scholar |
Dunnington, D. (2020). ggspatial: Spatial Data Framework for ggplot2. Available at https://cran.r-project.org/package=ggspatial/
Ford, F. (2006). A splitting headache: relationships and generic boundaries among Australian murids. Biological Journal of the Linnean Society 89, 117–138.
| A splitting headache: relationships and generic boundaries among Australian murids.Crossref | GoogleScholarGoogle Scholar |
Gunz, P., Mitteroecker, P., Neubauer, S., Weber, G. W., and Bookstein, F. L. (2009). Principles for the virtual reconstruction of hominin crania. Journal of Human Evolution 57, 48–62.
| Principles for the virtual reconstruction of hominin crania.Crossref | GoogleScholarGoogle Scholar | 19482335PubMed |
Holm, S. (1979). A Simple Sequentially Rejective Multiple Test Procedure. Scandinavian Journal of Statistics 6, 65–70.
| A Simple Sequentially Rejective Multiple Test Procedure.Crossref | GoogleScholarGoogle Scholar |
IUCN (2019). The IUCN Red List of Threatened Species. Version 2019-6.2. Available at https://www.iucnredlist.org/
Li, Y., Li, Y., Li, H., Wang, J., Rong, X., and Li, Y. (2020). Niviventer confucianus sacer (Rodentia, muridae) is a distinct species based on molecular, karyotyping, and morphological evidence. ZooKeys 959, 137–159.
| Niviventer confucianus sacer (Rodentia, muridae) is a distinct species based on molecular, karyotyping, and morphological evidence.Crossref | GoogleScholarGoogle Scholar | 32879614PubMed |
Lindenfors, P., Gittleman, J., and Jones, K. (2007). Sexual size dimorphism in mammals. In ‘Sex, size and gender roles: Evolutionary studies of sexual size dimorphism’. (Eds D. Fairbairn, W. Blanckenhorn, and T. Székely.) pp. 16–26. (Oxford University Press: Oxford, England.)
Mahoney, J. A. (1977). Skull characters and relationships of Notomys mordax Thomas (Rodentia: Muridae), a poorly known Queensland Hopping-mouse. Australian Journal of Zoology 25, 749–754.
| Skull characters and relationships of Notomys mordax Thomas (Rodentia: Muridae), a poorly known Queensland Hopping-mouse.Crossref | GoogleScholarGoogle Scholar |
Mahoney, J. A., Smith, M. J., and Medlin, G. C. (2008). A new species of hopping-mouse, Notomys robustus sp. Nov. (Rodentia: Muridae), from cave deposits in the Flinders and Davenport Ranges, South Australia. Australian Mammalogy 29, 117–135.
| A new species of hopping-mouse, Notomys robustus sp. Nov. (Rodentia: Muridae), from cave deposits in the Flinders and Davenport Ranges, South Australia.Crossref | GoogleScholarGoogle Scholar |
Marcy, A. E., Guillerme, T., Sherratt, E., Rowe, K. C., Phillips, M. J., and Weisbecker, V. (2020). Australian rodents reveal conserved Cranial Evolutionary Allometry across 10 million years of murid evolution. The American Naturalist , .
| Australian rodents reveal conserved Cranial Evolutionary Allometry across 10 million years of murid evolution.Crossref | GoogleScholarGoogle Scholar | 33211559PubMed |
McPhee, M. E. (2004). Morphological Change in Wild and Captive Oldfield Mice Peromyscus polionotus subgriseus. Journal of Mammalogy 85, 1130–1137.
| Morphological Change in Wild and Captive Oldfield Mice Peromyscus polionotus subgriseus.Crossref | GoogleScholarGoogle Scholar |
Mitteroecker, P., Gunz, P., Bernhard, M., Schaefer, K., and Bookstein, F. L. (2004). Comparison of cranial ontogenetic trajectories among great apes and humans. Journal of Human Evolution 46, 679–698.
| Comparison of cranial ontogenetic trajectories among great apes and humans.Crossref | GoogleScholarGoogle Scholar | 15183670PubMed |
Morris, K. D. (2000). The status and conservation of nativea rodents in Western Australia. Wildlife Research 27, 405–419.
| The status and conservation of nativea rodents in Western Australia.Crossref | GoogleScholarGoogle Scholar |
Murray, B. R., Dickman, C. R., Watts, C. H. S., and Morton, S. R. (1999). The dietary ecology of Australian desert rodents. Wildlife Research 26, 421–438.
| The dietary ecology of Australian desert rodents.Crossref | GoogleScholarGoogle Scholar |
Musser, G. G., and Carleton, M. D. (2005). Superfamily Muroidea. In ‘Mammal Species of the World a Taxonomic and Geographic Reference’, 3rd edn’ (Eds D. E. Wilson, and D. M. Reeder.) pp. 894–1531. (Johns Hopkins University Press: Baltimore.)
Nowak, R. M., and Paradiso, J. L. (1983). ‘Walker’s Mammals of the World. Volume II’, 4th edn’ (The Johns Hopkins University Press: Baltimore.)
O’Regan, H. J., and Kitchener, A. C. (2005). The effects of captivity on the morphology of captive, domesticated and feral mammals. Mammal Review 35, 215–230.
| The effects of captivity on the morphology of captive, domesticated and feral mammals.Crossref | GoogleScholarGoogle Scholar |
Paradis, E., and Schliep, K. (2019). ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528.
| ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R.Crossref | GoogleScholarGoogle Scholar | 30016406PubMed |
R Core Team (2020). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.r-project.org/
Ralls, K. (1976). Mammals in Which Females are Larger Than Males. The Quarterly Review of Biology 51, 245–276.
| Mammals in Which Females are Larger Than Males.Crossref | GoogleScholarGoogle Scholar | 785524PubMed |
Robinson, A. C., Kemper, C. M., Medlin, G. C., and Watts, C. H. S. (2000). The rodents of South Australia. Wildlife Research 27, 379–404.
| The rodents of South Australia.Crossref | GoogleScholarGoogle Scholar |
Rohlf, F. J. (2015). The tps series of software. Hystrix 26, 1–4.
| The tps series of software.Crossref | GoogleScholarGoogle Scholar |
Rohlf, F. J., and Slice, D. (1990). Extensions of the Procrustes Method for the Optimal Superimposition of Landmarks. Systematic Biology 39, 40–59.
| Extensions of the Procrustes Method for the Optimal Superimposition of Landmarks.Crossref | GoogleScholarGoogle Scholar |
Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of Image Analysis. Nature Methods 9, 671–675.
| NIH Image to ImageJ: 25 years of Image Analysis.Crossref | GoogleScholarGoogle Scholar | 22930834PubMed |
Smissen, P. J., and Rowe, K. C. (2018). Repeated biome transitions in the evolution of Australian rodents. Molecular Phylogenetics and Evolution 128, 182–191.
| Repeated biome transitions in the evolution of Australian rodents.Crossref | GoogleScholarGoogle Scholar | 30075296PubMed |
South, A. (2017). rnaturalearth: World Map Data from Natural Earth. Available at: https//cran.r-project.org/package=rnaturalearth
Tabatabaei Yazdi, F., and Alhajeri, B. H. (2018). Sexual dimorphism, allometry, and interspecific variation in the cranial morphology of seven Meriones species (Gerbillinae, Rodentia). Hystrix, the Italian Journal of Mammalogy 29, 162–167.
| Sexual dimorphism, allometry, and interspecific variation in the cranial morphology of seven Meriones species (Gerbillinae, Rodentia).Crossref | GoogleScholarGoogle Scholar |
Tate, G. H. H. (1951). Results of the Archbold Expeditions, No. 65. The Rodents of Australia and New Guinea. American Museum of Natural History, New York 97, 183–430.
Turner, J. R. (2004). ‘Mammals of Australia’. (Pensoft: Sofia-Moscow.)
Watts, C. H. S., and Aslin, H. J. (1981). ‘The Rodents of Australia’. (Angus and Robertson: Sydney.)
Watts, C. H. S., and Kemper, C. M. (1989). Muridae. In ‘Fauna of Australia’. (Eds D. W. Walton, and B. J. Richardson.) pp. 1–35. (AGPS: Canberra.)
Wickham, H. (2016). ‘ggplot2: Elegant Graphics for Data Analysis.’ (Springer-Verlag New York: New York.) Available at http://ggplot2.org
Zelditch, M. L., Swiderski, D. L., and Sheets, H. D. (2012). ‘Geometric Morphometrics for Biologists: A Primer’, 2nd edn (Academic Press: Massachusetts.)