Mandible Variation in the Dwarf Fat-Tailed Jerboa, Pygeretmus Pumilio (Rodentia: Dipodidae)
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Canadian Journal of Zoology Phenotypic plasticity under desert environment constraints: mandible variation in the dwarf fat-tailed jerboa, Pygeretmus pumilio (Rodentia: Dipodidae) Journal: Canadian Journal of Zoology Manuscript ID cjz-2019-0029.R1 Manuscript Type: Article Date Submitted by the 17-Apr-2019 Author: Complete List of Authors: Krystufek, Boris; Slovenian Museum of Natural History Janzekovic, Franc; Faculty of Natural Sciences and Mathematics, University of Maribor Shenbrot, DraftGeorgy; Ben-Gurion University of the Negev, Mitrani Department of Desert Ecology Ivajnsic, Danijel; Faculty of Natural Sciences and Mathematics, University of Maribor Klenovsek, Tina; Faculty of Natural Sciences and Mathematics, University of Maribor Is your manuscript invited for consideration in a Special Not applicable (regular submission) Issue?: Bergmann’s rule, desert ecology, ecomorphology, geometric Keyword: morphometrics, dwarf fat-tailed jerboa, Pygeretmus pumilio, resource availability https://mc06.manuscriptcentral.com/cjz-pubs Page 1 of 46 Canadian Journal of Zoology Phenotypic plasticity under desert environment constraints: mandible variation in the dwarf fat-tailed jerboa, Pygeretmus pumilio (Rodentia: Dipodidae) B. Kryštufek, F. Janžekovič, G. Shenbrot, D. Ivajnšič, and T. Klenovšek B. Kryštufek. Slovenian Museum of Natural History, Prešernova 20, 1000 Ljubljana, Slovenia, email: [email protected] F. Janžekovič, D. Ivajnšič, and T. Klenovšek. Faculty of Natural Sciences and Mathematics, University of Maribor, Koroška 160, 2000 Maribor, Slovenia, emails: [email protected]; [email protected]; [email protected] G. Shenbrot. Mitrani Department ofDraft Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, Israel, email: [email protected] Correspondence: T. Klenovšek Address: Faculty of Natural Sciences and Mathematics, Koroška 160, 2000 Maribor, Slovenia. Telephone: +386 41 808 366 Fax: +386 2 25 18 180 E-mail: [email protected] 1Supplementary tables are available with the article through the journal Web site at 1 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 2 of 46 Phenotypic plasticity under desert environment constraints: mandible variation in the dwarf fat-tailed jerboa, Pygeretmus pumilio (Rodentia: Dipodidae) B. Kryštufek, F. Janžekovič, G. Shenbrot, D. Ivajnšič, and T. Klenovšek Abstract: Arid areas have a comparatively narrow range of habitat types, with restricted variation in environmental parameters, leaving narrow boundaries for phenotypic variation to correlate with ecological variables. To test this presumption, we explored variation in size and shape of the mandible in the dwarf fat-tailed jerboa Pygeretmus pumilio (Kerr, 1792) under the constraints of a rigorous desert environment. Size varied significantly and predictably with geographic position and demonstrated a strong, non-linear longitudinal pattern. Moreover, size was associated withDraft several other climatic variables, but not with soil properties or with proxies for primary productivity. Our results suggest that, for rodents exposed to rapid and extreme changes, larger size may have multiple advantages, i.e. in maintaining euthermia during cold nights and efficient water metabolism under aridity stress; in accumulating fat reserves for hibernation; and digging deeper burrows, better protected from surface extremes. Shape varied clinally along the longitudinal transect, and the pattern was affected more by temperature than by precipitation. We conclude that the success of dwarf fat-tailed jerboa in occupying an extensive geographic range relies on their ability to meet environmental heterogeneity through cohesive and diverse responses, including physiology, behaviour, life-history traits, and morphological plasticity. Keywords: Bergmann’s rule, desert ecology, ecomorphology, geometric morphometrics, dwarf fat-tailed jerboa, Pygeretmus pumilio, resource availability. 1Supplementary tables are available with the article through the journal Web site at 2 https://mc06.manuscriptcentral.com/cjz-pubs Page 3 of 46 Canadian Journal of Zoology Introduction Interest in ecotypic morphometric variation of endothermic vertebrates goes back to the mid-19th century. Size has been in the focus ever since Bergmann’s (1847) generalization of the association between body size and latitude. The emerging third universal response to anthropogenic warming (i.e. reduction in body size alongside global temperature increases) is adding new significance to an old interest (Millien et al. 2006). Such attention is understandable, given that the size of an organism affects virtually every aspect of its existence (Calder 1984). Various hypotheses were proposed in the past to explain the functional association between the size of an animal and its environment (Millien et al. 2006; Yom-Tov and Geffen 2011). The traditional reason for the negative relation between body size and temperature (Bergmann’s rule) invokes the heat conservation gained through a decreased surface-area-to-volume ratioDraft (heat conservation hypothesis; Bergmann 1847; Gür 2010). While the low ratio of a larger endotherm better conserves energy in a cold environment, the high ratio in its smaller counterpart dissipates heat more effectively, which is advantageous in a warm, humid environment (heat dissipation hypothesis; Aldrich and James 1991). Since energy (fat) reserves increase with body size faster than the metabolic rate, a larger animal will endure (fast) for longer during periods of resource shortage (seasonality hypothesis; Gür 2010). A key predictor in determining body size can be food availability during postnatal growth, when the body size of endotherms is largely determined. The resource availability hypothesis therefore predicts a positive correlation between body size and environmental productivity itself, rather than temporal variability of productivity (Mueller and Diamond 2001; Yom-Tov and Geffen 2011). After the early interest in size variation, geographic variation in morphological shape and its association with environmental factors progressed, with the introduction of multivariate statistics in data analysis and particularly benefited from the revolution in 1Supplementary tables are available with the article through the journal Web site at 3 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 4 of 46 geometric morphometrics and analysis of landmarks (Rohlf and Marcus 1993). A number of studies showed that animals were capable of modifying their shape to improve resource use in a changing habitat and to cope with intra-specific competition (Souto-Lima and Millien 2014; Renaud et al. 2015). Deserts are environments of extremes in temperature and water availability. Extensive water shortages and a scarcity of vegetation create serious selective pressure and determine the occurrence, adaptation and distribution of desert animals (Laity 2008). Adaptations to extreme desert conditions have been studied at length in various groups, particularly rodents (for reviews, see MacMillen 1983; Genoways and Brown 1993; Mueller and Diamond 2001). Where body size is concerned, several authors noted that some mammals are smaller in desert environments than they would be in more mesic situations (the desert rule; McNab 2010). Furthermore, trends in size are associatedDraft more closely with precipitation and primary productivity than with temperature (Yom-Tov and Geffen 2006; McNab 2010). The dwarf fat-tailed jerboa Pygeretmus pumilio (Kerr, 1792) is a small (mean body mass = 45 grams), bipedal dipodid (family Dipodidae) from the semideserts and clay deserts of southeastern Europe and Central Asia. The geographic range covers ca. 5350 km in longitude and ca. 1750 km in latitude (Figure 1). It is a nocturnal leaf-eater and a facultative hibernator (Shenbrot et al. 1995). The dwarf fat-tailed jerboa is a promising model for studying ecotypic variation in a desert rodent. It is a ricochet rodent that occupies an extensive desert belt, is abundant, and is polytypic, with five recognized subspecies (Shenbrot et al., 1995 (2008)). We analyzed the morphological variability in P. pumilio by studying the mandible, which is a remarkably flexible structure and reacts actively to various interactions and feedbacks by changing shape (Renaud et al. 2015). Despite its obvious simplicity, the mandible evolved as a mosaic of elements and comprises several morphogenetic regions 1Supplementary tables are available with the article through the journal Web site at 4 https://mc06.manuscriptcentral.com/cjz-pubs Page 5 of 46 Canadian Journal of Zoology (Casanovas-Vilar and van Dam 2013). These regions show dissimilar rates of differentiation, composition, and function, making the mandible a highly informative structure. The mandible is the only movable bone of the skull, effectively acting as a lever through articulation between the condylar process and the temporal bone of the cranium. The main function of the mandible is to produce gnawing and chewing actions. It is nearly flat and it can be effectively analyzed in two dimensions, from a lateral point of view (Renaud et al. 2015). This minimizes error, which is an important issue in studies where any measured differences are naturally subtle. The main aim of this study was to evaluate the effects of different spatial and environmental conditions on the size and shape of the mandible of P. pumilio across its wide geographic range. We