Elsevier

Zoology

Volume 140, June 2020, 125779
Zoology

Geometric morphometric analysis of the plateau zokor (Eospalax baileyi) revealed significant effects of environmental factors on skull variations

https://doi.org/10.1016/j.zool.2020.125779Get rights and content

Highlights

  • Plateau zokors are subterranean rodents destroying the grasslands in the Qinghai-Tibetan Plateau.

  • Morphology of the plateau zokors’ skull changes among different populations.

  • Variations in the skull shape were associated with ecological factors.

Abstract

The plateau zokor (Eospalax baileyi) is employed as an ideal model for examining the relationships between phenotypic and ecological adaptations to the underground conditions in which the skull morphology evolves to adapt to tunnel environment. We evaluated the influence of environmental factors (altitude, temperature, and precipitation) and geographical distance on the variations in skull morphology of a native subterranean rodent plateau zokor population. Thin-plate spline showed that the trend of morphological changes along the CV1 axis was as follows: the two zygomatic arch and the two postorbital processes moved down, the two mastoid processes and the tooth row moved upward, and the tympanic bulla grew longer. The changes along the CV2 axis were as follows: the nasal bone and the tooth row became longer, the distance between the two anterior tips of zygomatic arch lengthened, the infraorbital foramen became smaller, the whole posterior part of the skull became shorter, the zygomatic bone and the two posterior tips of zygomatic arch moved down, and the foramen magnum became bigger. Thus we found significant differences in the skull shape among the seven populations studied. Along with the reduction in the altitude and increase in the mean annual temperature and mean annual precipitation, the nasal bone became shorter, the distance between the two anterior tips of the zygomatic arch became shorter, the whole posterior part of the skull lengthened, the infraorbital foramen became smaller, the two mastoid processes moved upward, and the occipital bone moved down on the dorsal surface of the skull. On the ventral surface of the skull, with an increase in the altitude, mean annual temperature, and mean annual precipitation, the tympanic bulla became shorter, the tooth row moved down, and the foramen magnum became smaller. The morphological changes in the skull were significantly positively correlated with environmental factors. Finally, there was a significant positive correlation between the Procrustes distance matrix of the skull and the geographic distance matrix, which indicates that the evolution of the plateau zokor follows the distance isolation model, but it needs to be further explored from genetic perspectives.

Introduction

The daily activities of rodents are constantly jeopardized with a myriad of threats in their natural environment; therefore, a series of adaptive mechanisms are undertaken either in a short-term (e.g., changes in foraging, feeding, general activity, and shelter-seeking behavior) (Busch et al., 2000; Leussis and Bolivar, 2006; Marcy et al., 2013) or in a systematic manner (e.g., change in physical characteristics) (Barnett and Dickson, 1989; Smith et al., 1998; Hoffmann and Sgrò, 2011). Adaptation is a phenotypic variation that in a given environment has the highest fitness for a particular set of variants (Reeve and Sherman, 1993). The phenotypic variant is beneficial for species fitness and survival under adverse environmental conditions. In a relatively stable environment, the evolution of organisms is relatively slow. However, in extremely unstable environments, organisms rapidly differentiate into different geographical branches, leading to the continuous accumulation of variation between populations or subspecies, thus forming new species (Krimbas and Loukas, 1984; Huntley and Webb, 1989; Khadem and Krimbas, 1991; Reeve and Sherman, 1993).

Skull is the point of direct interaction between mammals and the environment, and its morphological changes are directly related to environmental factors (Yom-Tov et al., 1999). In the process of species differentiation, it usually bears the effect of natural selection, and its morphological differences can elucidate the diversity across different species (Carrasco, 2000; González et al., 2002; Luna and Pacheco, 2002; Garnier et al., 2004). When environmental and genetic factors influence the skull, certain geographical, and intra- and inter-specific differences in the skull morphology and structures can be observed. These variations are extremely important to discuss the process of population diversity and speciation, including both intra- and inter-specific distinction and comparison, which is an important basis for species identification and classification (Ventura and Gosalbez, 1992). In rodents, skull morphology is of great significance for their survival and fitness as its structure enables the individuals to execute several functions including feeding, attacking, and digging besides the common sensory mechanisms, such as hearing, olfaction, and vision (Mora et al., 2003; Samuels, 2009). Furthermore, the skull is also directly related to the development of the brain in mammals.

The root, rhizome, young twig, and leaf are the favorite food of subterranean rodents. This has changed their tooth shape and helped develop a powerful masticatory muscle, and these changes have also affected the skull-related structures (Agrawal, 1967). Environmental factors may also play a pivotal role in the development of skull morphology during the different growth phases (Burnett, 1983; Yom-Tov and Nix, 1986). By analyzing the morphological differences and similarities in animal skulls under different environmental conditions, we may unravel the selective forces that govern the morphological and geographical variations in different populations and the direction of its evolution (Lu, 2003).

The plateau zokor (Eospalax baileyi) is a typical subterranean rodent species inhabiting the Qinghai–Tibetan Plateau (Su et al., 2015). It shows seasonal activities during spring and autumn at an altitude of 2800–4200 m with high adaption to the underground life, and it has great ecological and economic significance. Due to its special underground niche, it is highly dependent on its forelimbs, incisors, and head. These parts are used to dig holes and eat plant roots and stems (Zhang and Liu, 2003). Furthermore, its unique way of living makes it push the soil and build mounds in the grassland, which seriously damages the grassland plants and ecosystem (Zhang et al., 2003). In addition, due to a complex environment of high humidity, limited oxygen and high carbon dioxide atmosphere, low temperature, and lack of food (Shao et al., 2015), the plateau zokor has become a good model to study differentiation, selection, and species formation. Under this harsh environment, the body structure of the plateau zokor may evolve to adapt to the underground tunnel system. Thus, combined with geometric skull morphology of the plateau zokor, the measurement and analysis of its geographical differentiation features are of great value to master its intraspecific variation and understand its ecological characteristics, which can provide an important reference for research on their geographical evolution, developmental biology, and evolutionary ecology.

Zhang et al. (2012) investigated the relationship between body size of the plateau zokor and some environmental factors in the Qinghai–Tibetan Plateau. The results showed that the plateau zokor follows the Bergmann’s rule on the latitude, but based on the altitude, it is contrary to the Bergman rule. Furthermore, after assessing 19 morphological traits and the evolutionary mechanisms underlying sexual size dimorphism in the plateau zokor, Su et al. (2018) reported the individual variations in sexual size dimorphism and body size of the plateau zokors depending on sex. Natural underground habitats and behavioral differences between different genders can exert selective pressure on male traits and promote the evolution of sexual size dimorphism in the plateau zokors. However, to the best of our knowledge, there is almost no information on the skull morphology of the plateau zokor, especially the geometric morphology, which makes this worthwhile to study. Geometric morphometrics is the statistical analysis of form based on Cartesian landmark coordinates. After separating shape from overall size, position, and orientation of the landmark configurations, the resulting Procrustes shape coordinates can be used for statistical analysis. Procrustes distance can be used to estimate the average shape and describe the shape variation (Mitteroecker and Gunz, 2009). The variations in intraspecific morphology of rodents are increasingly assessed using geometric morphological methods that allow independent examination of shape and size variations (Alhajeri, 2019). Fornel et al. (2018) have confirmed the hypothesis that there is a link between chromosomal polymorphism and skull shape and size variation. Habitat heterogeneity may influence the evolution of the skull morphology in Ctenomys.

In the present study, we aimed to analyze the morphological differences and factors influencing them in the skull of seven populations of the plateau zokor in Gansu province, China, using geometric morphometrics. We combined related ecological factors to explore the correlation between the morphological variations of the skull and analyzed the correlation between the Procrustes distance matrix and geographic distance matrix of the skull.

Section snippets

Study location and sample collection

With the help of local rodent control and prevention authorities in Gansu province, we trapped and killed seven populations of wild-caught plateau zokors. One hundred and ten (n = 210) skulls of adult plateau zokors were used in this study (Fig. 1). Sampling distribution was as follows: Maqu County (n = 30), Meiwu Village (n = 30), Tianzhu County (n = 30), Zecha Village (n = 30), Gahai Town (n = 30), Guomang Village (n = 30), and Lintan County (n = 30). The individual rodents were matched based

Dorsal side

The results of MANOVA (Table 3, P < 0.01) revealed significant differences in the morphology of the dorsal side of the skull among the different geographical populations. The results of the canonical variable analysis on the dorsal side showed that the first three canonical variables explained 76.99% of the differences in the morphology; the first canonical variable accounted for 43.50%, the second accounted for 22.45%, and the third accounted for 11.05% (Table 4). Scatter plots (Fig. 2) of the

Discussion

Different geographical locations encompass various environmental pressures, and after long-term adaptation, the small mammals in these locations undergo morphological changes either between or within species, acclimatizing them to the diverse habitats (Kaneko, 2002; Salvucci et al., 2002; Yom-Tov and Yom-Tov, 2004). These adaptive changes are reflected by modifications in different body parts, such as the sense organs (Webster and Webster, 1980), limbs, and even bone structures (Yom-Tov, 2001;

Conclusions

Our research indicates that the geographic variation in skull occurs in different geographical populations of the plateau zokor. By combining three ecological factors, there was a significant relationship between the morphological changes in the skull and the ecological factors. Different ecological factors formed different habitats, which led to different evolutionary directions of the plateau zokor. This also provided a reference for the adaptive evolution of underground rodents. In addition,

Declaration of Competing Interest

The authors have no competing interests to declare.

Acknowledgements

This study was supported by the National Natural Science Foundation of China (31760706 and 31460566), Innovation Funds (GSAU-XKJS-2018-003) and “Fuxi Talent” Plan (Gaufx-02J03) of Gansu Agricultural University, Gansu Provincial Natural Science Foundation for Distinguished Young Scholars (1606RJDA314) and the Program for Longyuan Youth Innovation Talents of Gansu Province of China.

References (63)

  • F.L. Bookstein

    Principal warps: thin-plate splines and the decomposition of deformations

    IEEE Trans. Pattern Anal. Mach. Intell.

    (1989)
  • C.D. Burnett

    Geographic and climatic correlates of morphological variation in Eptesicus fuscus

    J. Mammal.

    (1983)
  • C. Busch et al.

    Population ecology of subterranean rodents

  • A. Cardini et al.

    Post-natal ontogeny of the mandible and ventral cranium in marmota species (Rodentia, Sciuridae): allometry and phylogeny

    Zoomorphology

    (2005)
  • A. Cardini et al.

    Patterns of morphological evolution in marmota (Rodentia, Sciuridae): geometric morphometrics of the cranium in the context of marmot phylogeny, ecology and conservation

    Biol. J. Linn. Soc.

    (2004)
  • A. Cardini et al.

    Morphological evolution in marmots (Rodentia, Sciuridae): size and shape of the dorsal and lateral surfaces of the cranium

    J. Zool. Syst. Evol. Res.

    (2005)
  • M.A. Carrasco

    Species discrimination and morphological relationships of kangaroo rats (Dipodomys) based on their dentition

    J. Mammal.

    (2000)
  • L.C.C.S. Dumbá et al.

    Cranial geometric morphometric analysis of the genus Tapirus (mammalia, perissodactyla)

    J. Mamm. Evol.

    (2019)
  • R. Fornel et al.

    Skull shape and size variation within and between mendocinus and torquatus groups in the genus Ctenomys (Rodentia: Ctenomyidae) in chromosomal polymorphism context

    Genet. Mol. Biol.

    (2018)
  • S. Garnier et al.

    When morphometry meets genetics: inferring the phylogeography of Carabus solieri using Fourier analyses of pronotum and male genitalia

    J. Evol. Biol.

    (2004)
  • S. González et al.

    Morphometric differentiation of endangered pampas deer (Ozotoceros bezoarticus), with description of new subspecies from Uruguay

    J. Mammal.

    (2002)
  • A.A. Hoffmann et al.

    Climate change and evolutionary adaptation

    Nature

    (2011)
  • B. Huntley et al.

    Migration: species’ response to climatic variations caused by changes in the earth’s orbit

    J. Biogeogr.

    (1989)
  • Y. Kaneko

    Morphological variation and geographical and altitudinal distribution in Eothenomys melanogaster and E. mucronatus (Rodentia, Arvicolinae) in China, Taiwan, Burma, India, Thailand, and Vietnam

    Mamm. Study

    (2002)
  • M. Khadem et al.

    Studies of the species barrier between Drosophila madeirensis and Drosophila subobscura

    Hereditas

    (1991)
  • C.P. Klingenberg

    MorphoJ: an integrated software package for geometric morphometrics

    Mol. Ecol. Resour.

    (2010)
  • O. Kott et al.

    Light propagation in burrows of subterranean rodents: tunnel system architecture but not photoreceptor sensitivity limits light sensation range

    J. Zool.

    (2014)
  • O. Kott et al.

    Light perception in two strictly subterranean rodents: life in the dark or blue?

    Plos One

    (2010)
  • C.B. Krimbas et al.

    Evolution of the obscura group drosophila species. I. Salivary chromosomes and quantitative characters in D. Subobscura and two closely related species

    Heredity

    (1984)
  • D.M. Lay

    The anatomy, physiology, functional significance and evolution of specialized hearing organs of gerbilline rodents

    J. Morphol.

    (1972)
  • X. Lu

    Postnatal growth of skull linear measurements of Cape hare Lepus capensis in northern China: an analysis in an adaptive context

    Biol. J. Linn. Soc.

    (2003)
  • Cited by (17)

    • Novel genotypes of Cryptosporidium and Enterocytozoon bieneusi detected in plateau zokors (Myospalax baileyi) from the Tibetan Plateau

      2022, International Journal for Parasitology: Parasites and Wildlife
      Citation Excerpt :

      The plateau zokor (Myospalax baileyi) is a small subterranean rodent endemic to China that lives alone year-round in sealed burrows underground at altitudes of 2000–4200 m on the Tibetan Plateau (Kang et al., 2020a; Pu et al., 2019).

    • Plateau zokors (Eospalax baileyi) respond to secondary metabolites from the roots of Stellera chamaejasme by enhancing hepatic inflammatory factors and metabolic pathway genes

      2022, Comparative Biochemistry and Physiology Part - C: Toxicology and Pharmacology
      Citation Excerpt :

      The plateau zokor (Eospalax baileyi) is a typical subterranean herbivore that lives on the QTP. It survives in burrows most of the year under harsh environmental conditions characterized by freezing temperatures, low oxygen, and poor soil conditions (Kang et al., 2020). To adapt to long periods of underground survival, the plateau zokor must dig for food that is found underground, which requires a lot of energy.

    • Pleistocene climate-driven diversification of plateau zokor (Eospalax baileyi) in the eastern Qinghai-Tibet Plateau

      2022, Ecological Indicators
      Citation Excerpt :

      A typical subterranean rodent, the plateau zokor (Eospalax baileyi) is native to the QTP (Su et al., 2015). Plateau zokors are highly adapted to underground life, exhibit seasonal activities at altitudes of 2,800–4,200 m throughout the year, and have considerable economic and ecological value (Kang et al., 2020). When constructing complicated burrow systems, they move loose soil to the surface and deposit it into mounds (Zhang, 2007; Zhang and Liu, 2002).

    • Effect of plateau zokor on soil carbon and nitrogen concentrations of alpine meadows

      2021, Catena
      Citation Excerpt :

      Therefore, a possible optimal approach is to completely estimate soil carbon and soil nitrogen in relation to the disturbance effect of small subterranean mammals in grasslands by quantifying soil carbon and soil nitrogen in mound, edge vegetation zone and undisturbed vegetation areas. The plateau zokor (Myospalax fontanierii) is a small subterranean mammal commonly found in alpine meadows on the Qinghai-Tibetan Plateau (Niu et al., 2020), and its habitat ranges in elevation from 2800 to 4200 m (Kang et al., 2020). The intensive burrowing activities of this small subterranean mammal often produce many fresh mounds of soil (Zhang and Liu, 2003; Zhang et al., 2004), contributing to alpine meadow degradation.

    View all citing articles on Scopus
    View full text