Morpho-Geometric Analysis of Eight Grass Mouse Species of the Genus Lemniscomys (Rodentia: Muridae)

Imed Ben Salem*, Aymen Ben Ibrahim, M’barek Chetoui and Saïd Nouira

Research Unit “Biodiversité et Biologie des Populations”, Faculty of Sciences of Tunis, University of Tunis El Manar, 2092 Tunis

ABSTRACT

Lemniscomys are exclusively African rodents. This study deals with morphs-genetic analysis of eight species viz. Lemniscomys barbarus, L. bellieri, L. griselda, L. limulus, L. macculus, L. rosalia, L. striatus and L. zebra; which have practically similar external morphologies although they spread in completely different geographical areas. The approach adopted was to identify landmarks on the skulls of all specimens using the tpsDig software, and then analyzing them through the program MorphoJ. Our results show that L. griselda has the largest skull, whereas L. zebra has the smallest. L. griselda and L. rosalia have greater breadth of the braincase, length of the nasals and length of the tympanic bulla, than the other species. This is probably related to a phenotypic evolution due to selective pressure, as is also the case in the genus Gerbillus.

Article Information

Received 14 June 2016

Revised 24 June 2016

Accepted 23 July 2016

Available online 23 September 2016

Authors’ Contributions

IBS and ABI conceived and designed the study. They also acquired, analysed and interpreted the data. MC and SN participated in drafting and revising the article.

Key words

Lemniscomys, Morphometric geometrics, Africa, Rodents, Skull

* Corresponding author: imedbensalem.fst@gmail.com

0030-9923/2016/0004-1161 $ 8.00/0

Copyright 2016 Zoological Society of Pakistan

DOI: http://dx.doi.org/10.17582/journal.pjz/2017.49.1.sc1

Research in systematics has benefited from several new techniques developed in recent years, including geometric morphometric analysis. It was developed to address the problems of systematic relationships and evolution, and made significant contributions to studies related to rodents which constitute the majority of the mammalian biodiversity in Africa (Denys et al., 2003). However, recent studies on genus Lemniscomys (Trouessart, 1881) have exclusively focused on the biogeographical, phylogenetic, chromosomal and molecular analysis (Castaglia et al., 2002; Nicolas et al., 2008; Mboumba et al., 2012) at the expense of morphometric analysis. This genus is one of the more diverse groups of rodents; its distribution is exclusively African and covers much of the continent with the exception of the Sahara which is a major ecological barrier. The genus Lemniscomys includes eleven species (Kingdon et al., 2013), which are characterized by their external appearance, in fact the color of their fur consists of one or more longitudinal stripes hence the term striped mouse. In the present study, we will focus on geometric morpho-metric analysis of eight species, which have close external morphologies despite occurring in different geographic areas (Carlton and Van der Straten, 1997) and possess dissimilar chromosome sets (Castaglia and Oguge, 2008).

Material and methods

A total of 200 adult specimens were analyzed, representing eight species L. barbarus (Linnaeus, 1766), L. bellieri (Van der Straeten, 1975), L. griselda (Thomas, 1904), L. limulus (Thomas, 1910), L. macculus (Thomas and Wroughton, 1910), L. rosalia (Thomas, 1904), L. striatus (Linnaeus, 1758) and L. zebra (Heuglin, 1864). Each species is represented by 25 specimens, they are deposited in Institut Royale des Sciences Naturelles de Belgique (IRSNB), Musé Royal de l’Afrique Centrale (MRAC) and Faculté des Sciences de Tunis (FST) in the Research Unit “Biodiversité et Biologie des Populations” (Supplementary Table I). The deposited specimens in the two museums mentioned above were identified according to Van der Straeten in his previous works (Carlton and Van der Straeten, 1997; Van der Straeten and Verheyen, 1980).

The skulls of all specimens were photographed on the ventral side using a Canon PowerShot A2200 HD camera (14.1 MP resolution). Using the software tpsDig, version 1.40 (Rohlf, 2009) 20 landmarks are identified on the skull images (Fig. 1).

1, tip of the nasal; 2, 15, inferior margin of infraorbital foramen; 3, 14, anterior extremity of molar row; 4, 13, posterior extremity of molar row; 5, 12, back of zygomatic notch; 6, 11, tympanic bulla at the posterior border of the external auditory meatus; 7, 10, posterior extremity of the tympanic bulla; 8, 9, posterior intersection between foramen magnum and occipital condyle; 16, anterior extremity of foramen; 17, posterior extremity of foramen; 18, aAnterior limit of mesopterygoid fossa; 19, 20, junction between tympanic bulla and pterygoid process.

The configurations of landmarks were analyzed by the MorphoJ program version 1.05f (Klingenberg, 2013). The average size of a skull was obtained from the square root of the sum of squared distances between landmarks and the center of gravity (or centroid) of the skull (Bookstein, 1991). The difference in average size of skulls between species is visualized by box plots. Differences in the shape of skulls between species are visualized through the Canonical Variate Analysis (CVA). Finally, Unweighted Pair Group Method with Average (UPGMA) was computed from the Procrustes distances obtained through ventral side configurations. All statistical analyses were performed using the PAST software, version 2.17 (Rohlf, 2009).

Results

We noticed a significant variation in the size of skulls (Fig. 2), Turkey HSD test suggests that L. griselda have the largest skulls (P <0.001) whereas L. zebra presents the smallest ones (P <0.001). The other species L. barbarus, L. bellieri, L. limulus, L. macculus, L. rosalia and L. striatus show intermediate sizes.

The variation in the shape of skulls is not related to the size of the skulls. The Canonical Variate Analysis (CVA; Fig. 3) corresponding to the ventral side configuration shows us a significant difference in the shape of skulls between species (Manova: Wilks’ λ = 0.0063; F = 14.29; P <0.001), the first 2 axes of the CVA absorbing 73.024% of variances, axis 1 (55.456%) allows discrimination of L. griselda, L. linulus and L. rosalia which are located in the positive part of the first axis, L. barbarus, L. macculus, and L. zebra are located in the negative part, whereas L. bellieri and L. striatus are located in the intermediate part with a substantial overlap. Axis 2 (17.568%) of the CVA shows significant overlapping between species, however it allows the discrimination between L. barbarus and L. zebra.

The variation on the axis 1 of the CVA focuses on landmarks n° 1, 16, 6, 11, 19 and 20 (Fig. 4), which menas that the most discriminating factors are the breadth of the braincase (landmarks n° 6 and 11), length of nasals (landmarks n° 1 and 16) and length of tympanic bulla (landmarks n° 19 and 20). The latter is more developed among L. rosalia and L. griselda than among the other species.

The UPGMA tree (Fig. 5) computed from the obtained Procrustes distances reveals the existence of two groups: the first consists of L. barbarus; L. bellieri; L. macculus and L. zebra, the second is formed by L. linulus and L. rosalia; L. striatus has a central position, whereas L. griselda has a basal position in the UPGMA tree.

Discussion

Geometric morphometric analysis is used for the first time on the genus Lemniscomys. Our results are close to those found by Van der Straeten and Verheyen (1980), despite having used multivariate analysis methods based on cranial measurements. However, recent molecular studies of the genus Lemniscomys show that L. rosalia, L. striatus and L. zebra have the same ancestry (Castaglia et al., 2002), which differs from the results found by morphometric analysis mentioned above and the present analysis. The difference, in this case, between molecular and morphometric analysis can be explained by a high rate of phenotypic evolution, this suggests the action of different selective pressures or functional constraints in the morphological evolution of the genus Lemniscomys, as in the case of the genus Gerbillus (Abiath, 2002; Abiath et al., 2010). Our results show that

close species morphologically on the cranial level are more or less sympatric species such as L. macculus and L. zebra (Eastern Africa) or L. griseldaand L. rosalia (Zambia) covering the same geographical areas (Kingdon et al., 2013).

Conclusion

The morpho-geometric approach applied on eight species of the genus Lemniscomys shows that the closest species on a cranial level can have dissimilar cytogenetic sets. It is due to a high rate of phenotypic evolution that can surpass the molecular counterpart. It would be interesting to explore this difference between morpho-geometric and cytogenetic results with further molecular studies of this genus.

Acknowledgements

The present study has been carried out in the Research Unit “Biodiversité et Biologie des Populations” at the “Faculté des Sciences de Tunis” (FST). It would have never been possible without the collaboration of many people we want to thank. We express our greatest gratitude to Mr. George LENGLET, curator at the “Institut Royale des Sciences Naturelles de Belgique” (IRSNB), who welcomed us at the Institute, and Mr. Wim WENDELEN, curator at the “Musé Royal de l’Afrique Centrale” (MRAC).

Conflict of interest statement

The authors declare that there is no conflict of interests regarding the publication of the manuscript.

Supplementary material

There is supplementary material associated with this article. Access the material online at: http://dx.doi.org/10.17582/journal.pjz/2017.49.1.sc1

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