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Testing a Long-Standing Hypothesis on the Relation Between the Auditory Mammalia 2014; aop Fatemeh Tabatabaei Yazdi * , Paolo Colangelo and Dominique Adriaens Testing a long-standing hypothesis on the relation between the auditory bulla size and environmental conditions: a case study in two jird species (Muridae: Meriones libycus and M. crassus ) Abstract: Variation in mammalian auditory bulla size Keywords: geoclimatic variation; geometric morphomet- has been linked to environmental conditions, and has rics; rodent; skull; two-block partial least squares. even been claimed to provide a habitat-specific survival value. Enlarged bullae are typically shared among species DOI 10.1515/mammalia-2013-0043 adapted to living in arid habitats. Previous studies suggest Received March 12 , 2013 ; accepted May 27 , 2014 that jirds also exhibit this adaptive enlargement of the bulla. However, such claims are based on the observation on a limited number of specimens, and thus they provide no quantitative support for this hypothesis. Therefore, we tested this hypothesis using a combination of geometric Introduction morphometrics and multivariate statistical techniques on a large sample of two jird species that exhibit a wide and A strong relationship between the environment and mor- partially overlapping geographical (and hence climatic) phological variation in animals has long been recognized, range, i.e., Meriones crassus (Sundevall, 1842) and M. with several studies showing associations of geoclimatic libycus (Lichtenstein, 1823). A total of 485 intact skulls of variation with inter- and intraspecific morphological vari- populations originating from Africa to the eastern Iranian ations (e.g., Ashton et al. 2000 , Meiri and Dayan 2003 , Plateau were analysed. The covariation between auditory Rychlik et al. 2006 , Cardini et al. 2007 , Colangelo et al. 2010 , bulla shape and several geoclimatic variables was explored Pavlinov et al. 2010 ). A marked variation in bulla size is using the two-block partial least-squares method. To some one of the phenomena that has been identified in several degree, the results seem to support the hypothesis that mammalian species, such as armadillos ( Squarcia et al. morphological variation in the auditory bulla is, indeed, 2007 ) and vervet monkeys ( Cardini et al. 2007 ). In rodents, correlated with geoclimatic variation. However, this find- enlarged bullae even have been considered to be adaptive ing cannot be generalised at several levels, hence refuting for living in drier environments (e.g., Petter 1961 , Pavli- the hypothesis of convergent correlations between geocli- nov 1979, 2001 , Chevret and Dobigny 2005, Momenzadeh matic conditions and bulla morphology. Species-specific et al. 2008, Darvish 2009 ). The enlargement is claimed to differences were found at different levels, suggesting that increase hearing performance, especially within the low- if local responses are present, they may reflect interac- frequency sound range, as well as to increase sound ampli- tions with phylogenetic constraints. fication that improves predator detection ( Burda et al. 1999 , Mason 2001, 2003 , Huang et al. 2002 , Schleich and Vasallo 2003 ). Both features would clearly have a habitat-specific survival value in a desert environment, which could explain *Corresponding author: Fatemeh Tabatabaei Yazdi, Faculty of a selective pressure towards bulla enlargement ( Lay 1972 , Natural Resources and Environment, Ferdowsi University of Webster and Webster 1984 , Sheets 1989 , Van der Straeten Mashhad, Azadi Square, 91735 Mashhad, Iran, and Dieterlen 1992 , Webster and Plassmann 1992 , Huang e-mail: [email protected] , [email protected] et al. 2002 ). However, these claims on environmentally cor- Paolo Colangelo: Department of Biology and Biotechnologies “ Charles Darwin ” , University of Rome “ La Sapienza ” , Roma, Italy related bulla enlargement are based on observations with a Dominique Adriaens: Evolutionary Morphology of Vertebrates, K.L. limited quantification of both the morphological and geo- Ledeganckstraat 35, 9000 Gent, Belgium climatic variation, and thus remain to be tested rigorously. Brought to you by | Universiteit Gent Authenticated Download Date | 12/15/14 12:12 AM 2 F. Tabatabaei Yazdi et al.: Morphological variation in jirds linked to environmental conditions Although geographically linked environmental con- on the basis of external (e.g., tail morphology) and cranial ditions have traditionally been studied using spatial criteria, including several features related to the audi- descriptors, such as latitude and elevation, current access tory bulla (e.g., suprameatal triangle), using published to more extensive environmental data with advanced mor- identification keys ( Chaworth-Musters and Ellerman 1947 , phometric techniques allow more complex multifactorial Osborn and Helmy 1980 ). Information on collection labels analyses. These techniques allow to discover patterns of was used as additional information for the identification. phenotypic responses to environmental changes, as well Moreover, to be able to assign the specimens to nominal as to identify habitat-specific factors constraining pheno- taxa, the available type specimens of both species in these typic evolution ( Reis et al. 2002a,b , Monteiro et al. 2003 , museums were examined and included in the analyses Cardini et al. 2007 ). (Appendix 2). Juvenile specimens, identified based on the Previous studies on jird species showed that cranial eruption and amount of wear on the molars (M2; Petter shape variation mainly involved variation at the level 1959, Tong 1989 , Pavlinov 2008 ) were excluded from the of the tympanic bulla ( Chaworth-Musters and Ellerman analyses to avoid confounding phenotypic variation that 1947 , Misonne 1959 , Pavlinov 2008 , Darvish 2009 , Pavli- was due to ontogenetic allometry. nov et al. 2010 ). Therefore, we tested the hypothesis that Sampling localities are depicted in Figure 1 , with the climatic conditions explain part of the phenotypic varia- abbreviated locality names (as used in the plots in Figures tion in the auditory bulla, and especially whether aridity 3 – 7) explained in Appendix 3. is the most predictive environmental variable, both at The ventral side of the skull of the specimens was intra- and interspecific levels. Such patterns have already photographed in a standardised manner using a Nikon been observed in rodents by, for example, Misonne (1959) , D70 digital reflex camera (5-megapixel resolution), Petter (1961) , Darvish (2009) , and Pavlinov (2008) . Hence, equipped with a Sigma 105 mm macro lens manner. The this study attempts to answer the following questions: (1) camera was placed on a tripod parallel to the ground which geoclimatic variables, and at what level, affect the plane. The intact and cleaned skulls were mounted in a tympanic bulla size and shape; and (2) to what degree is box with glass pearls. Left-right symmetry in a ventral the relation between geoclimatic conditions and bulla view and perfect overlap at the level of bullae, teeth rows, morphology species-specific. and the optic canals on the lateral side were the most To test the hypotheses on environmentally driven phe- important criteria to position the skulls in a standardised notypic divergences in two sympatric Meriones species, way. Millimetre paper was included in the images to allow namely, M. crassus (Sundevall, 1842) and M. libycus the acquisition of a scaling factor. Landmark configura- (Lichtenstein, 1823), spanning a broad geographic and tions were digitised using the software TpsDig 2.12 ( Rohlf environmental range, a covariance analysis was done on 2004 ). Given that testing left-right asymmetry in the phe- the skull morphology and geoclimatic data. notypic variation was not the focus of this study, remov- ing redundant bilateral landmarks would increase the statististical power of the analyses. Hence, we tested for Materials and methods left-right differences in the ventral face of 20 specimens of both species. A Monte Carlo randomization (based on partial warp scores, see below) showed that skulls were Samples and data acquisition on size and symmetrical (p ≥ 0.726). For this reason, only one side (left shape variation side) of the skulls was further digitised for the analyses. As a result, specimens that were broken on one side could A total of 485 intact skulls (271 for Meriones crassus and 214 still be included ( Elewa 2004 ), where in case the left side for M. libycus ) were analysed. Specimens were obtained was broken, the right side was digitised after which the from the collections of the Smithsonian Natural Museum coordinates were mirrored along the midline. of Natural History (Washington D.C. USA), the Field As a reference for overall skull size and shape, 10 Museum of Natural History (Chicago, USA), the British landmarks were collected from the ventral cranium Museum of Natural History (London, UK), the Mus é e ( Figure 2 A), as described in Appendix 4. The four land- national d ’ Histoire naturelle (Paris, France), the Natural marks used to describe bulla size and shape (Figure 2B) History Museum of Ferdowsi University (Mashhad, Iran), are (1) the most caudal point at the level of the auditory and the Royal Belgian Institute of Natural Sciences (Brus- meatus, (2) rostral curvature point at the level of the audi- sels, Belgium). A list of specimens with their catalogue tory meatus, (3) the most rostral point of the tympanic number is given in Appendix 1. Specimens were identified bulla, and (4) the most caudal point of the tympanic bulla. Brought to you
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