Volume 42 Issue 2
Mar.  2021
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Bader H. Alhajeri. Cranial variation in allactagine jerboas (Allactaginae, Dipodidae, Rodentia): a geometric morphometric study. Zoological Research, 2021, 42(2): 182-194. doi: 10.24272/j.issn.2095-8137.2020.302
Citation: Bader H. Alhajeri. Cranial variation in allactagine jerboas (Allactaginae, Dipodidae, Rodentia): a geometric morphometric study. Zoological Research, 2021, 42(2): 182-194. doi: 10.24272/j.issn.2095-8137.2020.302

Cranial variation in allactagine jerboas (Allactaginae, Dipodidae, Rodentia): a geometric morphometric study

doi: 10.24272/j.issn.2095-8137.2020.302
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  • Corresponding author: E-mail: bader.alhajeri@ku.edu.kw
  • Received Date: 2020-10-15
  • Accepted Date: 2021-03-08
  • Available Online: 2021-03-09
  • Publish Date: 2021-03-18
  • Allactaginae is a subfamily of dipodids consisting of four- and five-toed jerboas (Allactaga, Allactodipus, Orientallactaga, Pygeretmus, Scarturus) found in open habitats of Asia and North Africa. Recent molecular phylogenies have upended our understanding of this group’s systematics across taxonomic scales. Here, I used cranial geometric morphometrics to examine variation across 219 specimens of 14 allactagine species (Allactaga major, A. severtzovi, Orientallactaga balikunica, O. bullata, O. sibirica, Pygeretmus platyurus, P. pumilio, P. shitkovi, Scarturus aralychensis, S. euphraticus, S. hotsoni, S. indicus, S. tetradactylus, S. williamsi) in light of their revised taxonomy. Results showed no significant sexual size or shape dimorphism. Species significantly differed in cranial size and shape both overall and as species pairs. Species identity had a strong effect on both cranial size and shape. Only a small part of cranial shape variation was allometric, with no evidence of unique species allometries, and most specimens fit closely to the common allometric regression vector. Allactaga was the largest, followed by Orientallactaga, Scarturus, and finally Pygeretmus. Principal component 1 (PC1) separated O. bullata+O. balikunica+S. hotsoni (with inflated bullae along with reduced zygomatic arches and rostra) from A. major+A. severtzovi+O. sibirica (with converse patterns), while PC2 differentiated Orientallactaga (with enlarged cranial bases and rostra along with reduced zygomatic arches and foramina magna) from Scarturus+Pygeretmus (with the opposite patterns). Clustering based on the unweighted pair group method with arithmetic mean (UPGMA) contained the four genera, but S. hotsoni clustered with O. bullata+O. balikunica and O. sibirica clustered with A. major+A. severtzovi, likely due to convergence and allometry, respectively.
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  • [1]
    Adams D, Collyer M, Kaliontzopoulou A. 2020(2020-06-12). Geomorph: geometric morphometric analyses of 2D/3D landmark data. https://cran.r-project.org/web/packages/geomorph/.
    [2]
    Alhajeri BH. 2016. A phylogenetic test of the relationship between saltation and habitat openness in gerbils (Gerbillinae, Rodentia). Mammal Research, 61(3): 231−241. doi: 10.1007/s13364-016-0264-2
    [3]
    Alhajeri BH. 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(2): 261−276. doi: 10.1007/s10914-016-9377-2
    [4]
    Alhajeri BH. 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(1): 191−203. doi: 10.1111/jzs.12247
    [5]
    Alhajeri BH, Hunt OJ, Steppan SJ. 2015. Molecular systematics of gerbils and deomyines (Rodentia: Gerbillinae, Deomyinae) and a test of desert adaptation in the tympanic bulla. Journal of Zoological Systematics and Evolutionary Research, 53(4): 312−330. doi: 10.1111/jzs.12102
    [6]
    Alhajeri BH, Steppan SJ. 2018a. Community structure in ecological assemblages of desert rodents. Biological Journal of the Linnean Society, 124(3): 308−318. doi: 10.1093/biolinnean/bly068
    [7]
    Alhajeri BH, Steppan SJ. 2018b. Disparity and evolutionary rate do not explain diversity patterns in muroid rodents (Rodentia: Muroidea). Evolutionary Biology, 45(3): 324−344. doi: 10.1007/s11692-018-9453-z
    [8]
    Alhajeri BH, Steppan SJ. 2018c. A phylogenetic test of adaptation to deserts and aridity in skull and dental morphology across rodents. Journal of Mammalogy, 99(5): 1197−1216. doi: 10.1093/jmammal/gyy099
    [9]
    Allen GM. 1940. The Mammals of China and Mongolia. Part 2. New York: The American Museum of Natural History.
    [10]
    Auffray JC, Blasdell K, Bordes F, Chabé M, Chaisiri K, Charbonnel N, et al. 2011. Protocols for Field and Laboratory Rodent Studies. Thailand: Kasetsart University Press.
    [11]
    Bannikova A, Lebedev V, Dubrovskaya A, Solovyeva E, Moskalenko V, Kryštufek B, et al. 2019. Genetic evidence for several cryptic species within the Scarturus elater species complex (Rodentia: Dipodoidea): when cryptic species are really cryptic. Biological Journal of the Linnean Society, 126(1): 16−39. doi: 10.1093/biolinnean/bly154
    [12]
    Beolchini F, Corti M. 2004. The taxonomy of the genus Tachyoryctes: a geometric morphometric approach. Italian Journal of Zoology, 71(1): 35−43. doi: 10.1080/11250000409356548
    [13]
    Bergmann C. 1847. Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Göttinger Studien, 3(1): 595−708.
    [14]
    Berman SL. 1985. Convergent evolution in the hindlimb of bipedal rodents. Journal of Zoological Systematics and Evolutionary Research, 23(1): 59−77.
    [15]
    Bookstein FL. 1986. Size and shape spaces for landmark data in two dimensions. Statistical Science, 1(2): 181−242. doi: 10.1214/ss/1177013696
    [16]
    Boroni NL, Lobo LS, Romano PSR, 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.
    [17]
    Cheng JL, Xia L, Feijó A, Shenbrot GI, Wen ZX, Ge DY, et al. 2020. Phylogeny, taxonomic reassessment and ‘ecomorph’ relationship of the Orientallactaga sibirica complex (Rodentia: Dipodidae: Allactaginae). Zoological Journal of the Linnean Society. doi: 10.1093/zoolinnean/zlaa102.
    [18]
    Colangelo P, Castiglia R, Franchini P, Solano E. 2010. Pattern of shape variation in the eastern African gerbils of the genus Gerbilliscus (Rodentia, Muridae): environmental correlations and implication for taxonomy and systematics. Mammalian Biology, 75(4): 302−310. doi: 10.1016/j.mambio.2009.05.001
    [19]
    Collyer ML, Adams DC. 2018. RRPP: an R package for fitting linear models to high-dimensional data using residual randomization. Methods in Ecology and Evolution, 9(7): 1772−1779. doi: 10.1111/2041-210X.13029
    [20]
    Collyer ML, Adams DC. 2020(2020-05-28). RRPP: linear model evaluation with randomized residuals in a permutation procedure. https://cran.case.edu/web/packages/RRPP/index.html.
    [21]
    Darvish J, Hajjar T, Moghadam Matin M, Haddad F, Akbary Rad S. 2008. New species of five-toed jerboa (Rodentia: Dipodidae, Allactaginae) from North-East Iran. Journal of Sciences, Islamic Republic of Iran, 19(2): 103−109.
    [22]
    Dianat M, Aliabadian M, Darvish J, Akbarirad S. 2013. Molecular phylogeny of the Iranian Plateau five-toed jerboa, Allactaga (Dipodidea: Rodentia), inferred from mtDNA. Mammalia, 77(1): 95−103.
    [23]
    Dianat MA, Tarahomi M, Darvish J, Aliabadian M. 2010. Phylogenetic analysis of the five-toed Jerboa (Rodentia) from the Iranian Plateau based on mtDNA and morphometric data. Iranian Journal of Animal Biosystematics, 6(1): 49−59.
    [24]
    Dunnington D. 2020(2020-07-12). Ggspatial: spatial data framework for ggplot2. https://cran.r-project.org/web/packages/ggspatial/index.html.
    [25]
    Fadda C, Corti M. 2001. Three-dimensional geometric morphometrics of Arvicanthis: implications for systematics and taxonomy. Journal of Zoological Systematics and Evolutionary Research, 39(4): 235−245. doi: 10.1046/j.1439-0469.2001.00169.x
    [26]
    Goodall C. 1991. Procrustes methods in the statistical analysis of shape. Journal of the Royal Statistical Society: Series B (Methodological), 53(2): 285−339. doi: 10.1111/j.2517-6161.1991.tb01825.x
    [27]
    Google. 2020. Google maps. Version 3.42.
    [28]
    Gunz P, Mitteroecker P, Neubauer S, Weber GW, Bookstein FL. 2009. Principles for the virtual reconstruction of hominin crania. Journal of Human Evolution, 57(1): 48−62. doi: 10.1016/j.jhevol.2009.04.004
    [29]
    Hamidi K, Darvish J, Matin MM. 2016. New records of the William’s Jerboa, Paralactaga cf. williamsi (Thomas, 1897) (Rodentia: Dipodidae) from northeastern Iran with notes on its ecology. Check List, 12(2): 1−6.
    [30]
    Holden ME, Musser GG. 2005. Family dipodidae. In: Wilson DE, Reeder DM. Mammal Species of the World: A Taxonomic and Geographic Reference. 3rd ed. Baltimore: Johns Hopkins University Press, 871–893.
    [31]
    Kryštufek B, Arslan A, Shehab A, Abi-Said MR, Zupan S, Lužnik M. 2013. Mitochondrial sequences point on a cryptic species in five-toed jerboas, subgenus Paralactaga. Mammalia, 77(4): 433−438.
    [32]
    Lay DM. 1972. The anatomy, physiology, functional significance and evolution of specialized hearing organs of gerbilline rodents. Journal of Morphology, 138(1): 41−120. doi: 10.1002/jmor.1051380103
    [33]
    Lebedev VS, Bannikova AA, Pagès M, Pisano J, Michaux JR, Shenbrot GI. 2013. Molecular phylogeny and systematics of Dipodoidea: a test of morphology-based hypotheses. Zoologica Scripta, 42(3): 231−249. doi: 10.1111/zsc.12002
    [34]
    Mares MA. 1975. South American mammal zoogeography: evidence from convergent evolution in desert rodents. Proceedings of the National Academy of Sciences of the United States of America, 72(5): 1702−1706. doi: 10.1073/pnas.72.5.1702
    [35]
    Martin SA, Alhajeri BH, Steppan SJ. 2016. Dietary adaptations in the teeth of murine rodents (Muridae): a test of biomechanical predictions. Biological Journal of the Linnean Society, 119(4): 766−784. doi: 10.1111/bij.12822
    [36]
    Michaux J, Shenbrot G. 2017. Family DIPODIDAE (JERBOAS). In: Wilson DE, Lacher Jr TE, Mittermeier RA. Handbook of the Mammals of the World, Volume 7: Rodents II. Barcelona: Lynx Edicions, 1–20.
    [37]
    Miljutin A. 2008. Trends of specialisation in rodents: the five-toed jerboas, subfamily Allactaginae (Dipodoidea, Rodentia). Acta Zoologica Lituanica, 18(4): 228−239. doi: 10.2478/v10043-008-0033-9
    [38]
    Mitteroecker P, Gunz P, Bernhard M, Schaefer K, Bookstein FL. 2004. Comparison of cranial ontogenetic trajectories among great apes and humans. Journal of Human Evolution, 46(6): 679−698. doi: 10.1016/j.jhevol.2004.03.006
    [39]
    Moore TY, Organ CL, Edwards SV, Biewener AA, Tabin CJ, Jenkins Jr FA, et al. 2015. Multiple phylogenetically distinct events shaped the evolution of limb skeletal morphologies associated with bipedalism in the jerboas. Current Biology, 25(21): 2785−2794. doi: 10.1016/j.cub.2015.09.037
    [40]
    Nowak RM, Paradiso JL. 1983. Walker’s Mammals of the World. Volume II. 4th ed. Baltimore: The Johns Hopkins University Press.
    [41]
    Paradis E, Schliep K. 2019. Ape 5. 0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics, 35(3): 526−528.
    [42]
    Pisano J, Condamine FL, Lebedev V, Bannikova A, Quéré JP, Shenbrot GI, et al. 2015. Out of Himalaya: the impact of past Asian environmental changes on the evolutionary and biogeographical history of Dipodoidea (Rodentia). Journal of Biogeography, 42(5): 856−870. doi: 10.1111/jbi.12476
    [43]
    R Core Team. 2020. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
    [44]
    Rohlf FJ. 2015. The tps series of software. Hystrix, 26(1): 9−12.
    [45]
    Rohlf FJ, Corti M. 2000. Use of two-block partial least-squares to study covariation in shape. Systematic Biology, 49(4): 740−753. doi: 10.1080/106351500750049806
    [46]
    Rohlf FJ, Slice D. 1990. Extensions of the procrustes method for the optimal superimposition of landmarks. Systematic Biology, 39(1): 40−59.
    [47]
    Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9(7): 671−675. doi: 10.1038/nmeth.2089
    [48]
    Shenbrot GI. 2009. On the conspecifity of Allactaga hotsoni thomas, 1920 and Allactaga firouzi womochel, 1978 (Rodentia: Dipodoidea). Mammalia, 73(3): 231−237.
    [49]
    Shenbrot GI, Krasnov BR, Rogovin KA. 1999. Spatial Ecology of Desert Rodent Communities. Berlin, Heidelberg: Springer-Verlag.
    [50]
    Shenbrot GI, Sokolov VE, Heptner VG, Koval'skaya YM. 2008. Jerboas: Mammals of Russia and Adjacent Regions. Enfield: CRC Press.
    [51]
    South A. 2017(2017-03-21). Rnaturalearth: world map data from natural earth. https://cran.r-project.org/web/packages/rnaturalearth/index.html.
    [52]
    Tabatabaei Yazdi F, Adriaens D. 2013. Cranial variation in Meriones tristrami (Rodentia: Muridae: Gerbillinae) and its morphological comparison with Meriones persicus, Meriones vinogradovi and Meriones libycus: a geometric morphometric study. Journal of Zoological Systematics and Evolutionary Research, 51(3): 239−251. doi: 10.1111/jzs.12020
    [53]
    Tarahomi SM, Karami M, Darvish J, Malek M, Jangjoo M. 2010. Geometric morphometric comparison of mandible and skull of five species of genus Allactaga (Rodentia: Dipodidae) from Iran. Iranian Journal of Animal Biosystematics, 6(1): 61−69.
    [54]
    Upham NS, Esselstyn JA, Jetz W. 2019. Inferring the mammal tree: species-level sets of phylogenies for questions in ecology, evolution, and conservation. PLoS Biology, 17(12): e3000494. doi: 10.1371/journal.pbio.3000494
    [55]
    Webster DB, Webster M. 1975. Auditory systems of heteromyidae: functional morphology and evolution of the middle ear. Journal of Morphology, 146(3): 343−376. doi: 10.1002/jmor.1051460304
    [56]
    Wickham H. 2016. ggplot2: Elegant Graphics for Data Analysis. 2nd ed. New York: Springer-Verlag.
    [57]
    Wu SY, Wu WY, Zhang FC, Ye J, Ni XJ, Sun JM, et al. 2012. Molecular and paleontological evidence for a post-cretaceous origin of rodents. PLoS One, 7(10): e46445. doi: 10.1371/journal.pone.0046445
    [58]
    Wu SY, Zhang FC, Edwards SV, Wu WY, Ye J, Bi SD, et al. 2014. The evolution of bipedalism in jerboas (Rodentia: Dipodoidea): origin in humid and forested environments. Evolution, 68(7): 2108−2118. doi: 10.1111/evo.12404
    [59]
    Zelditch ML, Swiderski DL, Sheets HD. 2012. Geometric Morphometrics for Biologists: A Primer. 2nd ed. Boston: Academic Press.
    [60]
    Zhang Q, Xia L, Kimura Y, Shenbrot G, Zhang ZQ, Ge DY, et al. 2013. Tracing the origin and diversification of dipodoidea (Order: Rodentia): evidence from fossil record and molecular phylogeny. Evolutionary Biology, 40(1): 32−44. doi: 10.1007/s11692-012-9167-6
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