Elsevier

Quaternary Science Reviews

Volume 221, 1 October 2019, 105886
Quaternary Science Reviews

Molar shape differentiation during range expansions of the collared lemming (Dicrostonyx torquatus) related to past climate changes

https://doi.org/10.1016/j.quascirev.2019.105886Get rights and content

Abstract

The genus Dicrostonyx (the collared lemming) is undoubtedly the small mammal best adapted to the extreme conditions of the arctic environment. The Palearctic collared lemming has been described in numerous European Late Pleistocene localities up to south of France and Croatia. This species experienced climate-driven changes through time, changes mainly observed as repetitive pulses of pan-continental migration, and it thus became a typical indicator of glacial conditions. Using geometric morphometrics on molars, we evaluate the shape changes occurring during the last 100 ky over some dispersal events in Western Europe. The results point out that Dicrostonyx torquatus has a large intra-population variation with a homogenous morphology, regardless of the origin of the individuals. A temporal trend leading to a more complex tooth with a differentiated anterior loop on the first lower molar was observed. An additional effect of the distance from the core populations was also described with a more peculiar shape for the most western populations of France. These temporal and geographical trends might relate to the different migratory pulses documented from ancient DNA haplotypes.

Introduction

The Arctic is unique among Earth's ecosystems and covers almost ten percent of land area. Restrained to circumpolar locations, north to the timberline, this region is subject to extreme climate conditions associated with strong seasonality. Despite the restrictive environment for plant development and limited available resources, many animals inhabit this region such as among terrestrial mammals, some carnivores (Ursus maritimus, Canis lupus arctos, Vulpes lagopus), some large herbivores (Alces alces, Rangifer tarandus), some lagomorphs (Lepus arcticus) and several small mammals (Sorex arcticus, lemmings and voles). These species exhibit different strategies, as migration or hibernation, to cope with the hard conditions and survive (Blix, 2016). In this ecosystem, rodents constitute the main resources for numerous predators and the cyclic dynamics of these key-species is a major driver of the fluctuations of the tundra food web (e.g., Gilg et al., 2003). The collared lemming (Dicrostonyx) represents an emblematic species-complex of this peculiar landscape. This small mammal is well adapted to these conditions, living in dry and well-drained uplands in high Arctic tundra and forest tundra (Wilson et al., 2017).

The different species of Dicrostonyx have a range covering a nearly circumpolar area from Alaska, Canada, Greenland up to Western Russia and North-East Siberia (Wilson et al., 2017). The Eurasian species, Dicrostonyx torquatus (the Palearctic collared lemming) is divided into five phylogenetic clades (Fedorov et al., 1999; Fregda et al., 1999; Abramson and Tikhonova, 2002), congruent with the geographical distribution of chromosome races (Fedorov et al., 1999). This genetic structure seems to derive from the fragmentation of the species' range in the Late Pleistocene and to bottleneck events during the Holocene thermal maximum. The Late Pleistocene is characterized by many major shifts in climate, with both stadial and interstadial cycles known as abrupt and short Heinrich or Dansgaard-Oeschger events (e.g. Labeyrie et al., 2007). These climate fluctuations led to important contraction, expansion or shift in many species' ranges (Hewitt, 1996, 2000), generating migrations and/or local extinctions. These responses appear mainly individualistic (Stewart, 2009) and thus led to changes in species associations and richness establishing non-analogue communities compared to extant ones (e.g., for small mammal assemblages see Kowalski, 1995; Royer et al., 2016). These transient communities contain novel biotic interactions (Blois et al., 2013) since each species has its own capability to track rapid climate change, capacity that appears at least partly related to its own traits (Angert et al., 2011; MacLean and Beissinger, 2017). The collared lemming experienced these climate-driven changes through time, becoming a typical indicator of glacial conditions in the past literature (e.g., Chaline, 1972; Harlé, 1906; Hinton, 1926; Kowalski, 1995). Indeed, this species was recognized between the middle of 19th and the beginning of the 20th centuries in many different fossil records located far South of its current Arctic range, as in Germany (Hensel, 1855), England (Sanford, 1870), Belgium (Rutot, 1910), France (Harlé, 1893, 1906; Pomel, 1853), or Croatia (Lenardić, 2013). Although, many sub-specific or specific taxa of fossil collared lemmings were described from the Late Pleistocene in Europe (e.g., Friant, 1960; Hinton, 1910, 1926; Sanford, 1870), whose relevance remains highly questionable according to Kowalski (2001), the occurrences of these taxa at least attest repeated colonisations of Western Europe throughout different climatic cycles. Based on ancient DNA, populations appear to have been regularly affected by Dansgaard-Oeschger interstadial events all along their presence in Western Europe (Brace et al., 2012), corroborating assumptions from fossil remains (e.g., Marquet, 1993; Royer et al., 2016; Villa et al., 2010). One expected outcome of these repetitive range shifts and/or expansion with local extinctions and subsequent recolonizations is a reduced genetic divergence among populations (Martin and McKay, 2004). These events are also expected to reduce the within-population genetic diversity in peripheral populations (Eckert et al., 2008) by a series of successive bottlenecks (Hewitt, 1996) and genetic drift enhancing the surfing of peculiar alleles over large geographical areas (Klopfstein et al., 2005) but with sharp differences between areas (Excoffier and Ray, 2008). Increase of mutation load in populations on the expansion front is also expected from the same phenomenon (Peischl et al., 2013; Willi et al., 2018), which led to strong divergences of peripheral populations. Following the Last Glacial Maximum, population declines of the collared lemming have been evidenced and climate changes occurring at that time have thus strongly impacted them, affecting their effective population sizes and their genetic diversity (Prost et al., 2010). The last occurrences of the collared lemming in Western Europe vary from the Bølling-Allerød to the early Holocene according to the latitude (e.g., Cordy, 1991; Kowalski, 1995; Price, 2003; Royer, 2013; Royer et al., 2016).

In this context of past climate changes and major range expansions and contractions, the aim of this study is to evaluate the shape variation of the collared lemming teeth, through time and space, from fossil and extant specimens. Indeed, even if there are some studies describing the morphology through biometrical and morphotype analyses (Abramson et al., 2004; Agadjanian, 1976; Agadjanian and Koenigswald, 1977; Kochev, 1984; Nadachowski, 1982; Nagel, 1997; Ponomarev and Puzachenko, 2015; Smirnov et al., 1986, 1997; Zazhigin, 1976), very few studies have investigated morphological variation of this species at large temporal and spatial scales. In the Palearctic collared lemmings, skull and mandible morphologies vary in agreement to chromosome races and mtDNA clades, relationship congruent with the Late Pleistocene stadial cycles (Abramson and Tikhonova, 2002).

In the current study, we investigate the shape of molar as this anatomical element presents two main advantages. First, it allows the comparison of modern and fossil individuals, as it represents the best-preserved fossil remain that can usually be identified at the species level. Second, teeth harbour less plasticity compared to skull and mandible, and thus are likely to vehicle more information to be compared with haplotype diversities. In lemmings, the upper teeth have mainly been studied for systematics purpose in order to discriminate species or simplex and complex morphotypes. We focused instead on the first lower molar because this dental element is also well studied in voles and lemmings for a very long time in evolutionary studies. Moreover, this molar has the special attractiveness of being recently examined in developmental studies (e.g. Harjunmaa et al., 2012; Peterková et al., 2006; Salazar-Ciudad and Jernvall, 2002; Renvoisé et al., 2018). These interests allow potential comparisons aimed at a better understanding of evolutionary patterns and processes in this rodent group (Kavanagh et al., 2007; Polly, 2007; Renvoisé et al., 2009). Geometric morphometrics of the tooth shape was investigated through a temporal sequence ranging from MIS 6 to MIS 1 and a geographical gradient from Siberia to southwestern France. This unique dataset provides the opportunity to contrast morphological variation with the known genetic differentiation observed in recent paleogenetic studies (Palkopoulou et al., 2016), in order to understand the evolution of the Palearctic collared lemming during its Late Pleistocene geographical expansion in Europe.

Section snippets

Material and methods

A total of 592 first lower molars were sampled from 16 fossil localities and 2 present-day sites (Fig. 1; Table 1). All specimens came from collections of Natural History Museums or research laboratories. The fossil sites are located throughout in Europe, mainly in France, Belgium, Switzerland, Hungary and Poland (Fig. 1). They extended from MIS 6 for the oldest site located in Poland up to the Bølling period (see description of sites in supplementary materials). Fossil populations have been

Results

The two first principal components (PCs) of the molar shape account, respectively, for 18.2% and 14.3% of the total shape variation (Fig. 4A). The variation appears to be quite lowly structured and spreads on many dimensions on the shape space, with 23 PCs accounting for 90% of the variation. The result points out a homogenous morphology for the species, regardless of the origin of the individuals. Fig. 4B shows the mean of the different localities on PC1 and PC2 according to age categories.

Discussion

The geometric morphometrics analysis of the first lower molar based on samples distributed largely across time and space shows that both modern and fossil specimens exhibit a quite variable morphology, but this variation is almost similar among populations. Indeed, this variation is spread on many, if not all, directions of the morphospace and a large intra-population variance has been observed both temporally and geographically. This pattern is frequently observed at the intraspecific level on

Conclusion

In conclusion, the shape of the first lower molar of the collared lemming is highly variable and follows temporal and geographical trends that might relate to the different migratory pulses documented from ancient DNA haplotypes. Whereas each pulse appears to be recorded in shape, their effect is quite small compare to the large variation existing at any one time; morphotype proxies of migratory events could not be identified. Dispersal events led to some differentiation according to the

Author contributions

Conceptualization, S.M., A.R. and N.N.; Methodology, N.N.; Formal analysis, N.N.; Investigations and Data Curation, S.M.; Writing–original draft preparation, S.M., A.R., and N.N.; Writing, Review and Editing, S.M., A.R., N.N., E.D., N.S., A.S., O.G., A.N., A.L.

Acknowledgements

Authors thank, for access to the fossil material from several French localities, J.-C. Marquet (La Roche-Cotard, France), L. Lebreton and S. Soriano (Roc-en-Pail, France), B. Maureille and A. Mann (Les Pradelles, France), S. David (Amange-Grotte des Gorges, France) and J. Primault (Tailles des Coteaux, France). We also thank L. Costeur (Naturhistorisches Museum Basel), A.L. Folie (Royal Belgium Institute of Natural History, Bruxelles) and J. Thomas (as part of the ReColNat Research

References (94)

  • A.K. Agadjanian et al.

    Merkmalsverschiebung an der oberen Molaren von Dicrostonyx (Rodentia, Mammalia) in Jungquätar

    N. Jb. Geol. Paläont, Abh.

    (1977)
  • A.L. Angert et al.

    Do species' traits predict recent shifts at expanding range edges?

    Ecol. Lett.

    (2011)
  • A.D. Barnosky et al.

    Evolution, climatic changes and species boundaries: perspectives from tracing Lemmicus curtatus populations through time and space

    Proc. R. Soc. Lond. B

    (2003)
  • A.S. Blix

    Adaptations to polar life in mammals and birds

    J. Exp. Biol.

    (2016)
  • J.L. Blois et al.

    Climate change and the past, present, and future of biotic interactions

    Science

    (2013)
  • F.L. Bookstein

    Morphometric Tools for Landmark Data. Geometry and Biology

    (1997)
  • S. Brace et al.

    Serial population extinctions in a small mammal indicate Late Pleistocene ecosystem instability

    Proc. Natl. Acad. Sci. U.S.A.

    (2012)
  • P. Brunet-Lecomte

    Les campagnols souterrains (Terricola, Arvicolidae, Rodentia) actuels et fossiles d'Europe occidentale

    (1988)
  • R. Caumul et al.

    Phylogenetic and Environmental Components of Morphological Variation : Skull, Mandible, and Molar Shape in Marmots (Marmota, Rodentia)

    (2005)
  • J. Chaline

    Les rongeurs du Pléistocène moyen et supérieur de France (systématique- biostratigraphie- paléoclimatologie)

    (1972)
  • J.-M. Cordy

    5. Paleoecology of the Late Glacial and early Postglacial of Belgium and neighbouring areas

  • J.-M. Cordy

    Analyse paléoécologique des micromammifères tardiglaciaires de la grotte de Chaleux (Prov. de Namur, Belgique)

  • I.L. Dryden et al.

    Statistical Shape Analysis

    (1998)
  • C.G. Eckert et al.

    Genetic variation across species' geographical ranges: the central-marginal hypothesis and beyond

    Mol. Ecol.

    (2008)
  • L. Excoffier et al.

    Genetic consequences of range expansions

    Annu. Rev. Ecol. Evol. Syst.

    (2009)
  • V.B. Fedorov

    Contrasting mitochondrial DNA diversity estimates in two sympatric genera of Arctic lemmings (Dicrostonyx, Lemmus) indicate different responses to Quaternary environmental fluctuations

    Proc. Roy. Soc. Lond. B Biol.

    (1999)
  • V.B. Fedorov et al.

    The importance of ice ages in diversification of Arctic collared lemmings (Dicrostonyx) evidence from the mitochondrial cytochrome b region

    Hereditas

    (1999)
  • V.B. Fedorov et al.

    Mitochondrial DNA variation and the evolutionary history of chromosome races of collared lemmings (Dicrostonyx) in the Eurasian Arctic

    J. Evol. Biol.

    (1999)
  • O. Fejfar

    Überzwei neue Säugetirre aus dem Altpleistozänvon Böhmen

    N. Jb. Geol. Paläont., Mh.

    (1966)
  • K. Fregda et al.

    Genetic diversity in Arctic lemmings

    Ambio

    (1999)
  • M. Friant

    Le Dicrostonyx henseli Hint. Lemming du Pléistocène, sa répartition dans le temps et dans l'espace

    Soc. Geol. Nord

    (1960)
  • M. Frouin et al.

    Chronologie du site moustérien de type Quina des Pradelles (Marillac-le-Franc, Charente, France)

    Paléo

    (2017)
  • O. Gilg et al.

    Cyclic dynamics in a simple vertebrate predator-prey community

    Science

    (2003)
  • O. Hallastschek et al.

    Gene surfing in expanding populations

    Theor. Popul. Biol.

    (2008)
  • E. Harjunmaa et al.

    On the difficulty of increasing dental complexity

    Nature

    (2012)
  • E. Harlé

    Sur les restes de divers Rongeurs quaternaires du SO de la France et sur le climat de cette région à la fin du Quaternaire

    Bull. Soc. Hist. Nat. Toulouse

    (1893)
  • E. Harlé

    Lemming à collier (Myodes torquatus P.) de Teyjat (Dordogne)

    Bull de la Soc. Géol. Fr.

    (1906)
  • R. Hensel

    Beitrage zur Kenntniss fossiler Saugethiere; Insectenfresser und Nagethiere der Diluvialformation

    Deutsch Geol.

    (1855)
  • G.M. Hewitt

    The genetic legacy of the Quaternary ice ages

    Nature

    (2000)
  • M.A.C. Hinton

    Some new late Pleistocene voles and lemmings

    Ann. Mag. Nat. Hist. Lond.

    (1910)
  • M.A.C. Hinton

    Monograph of Voles and Lemmings. Living and Extinct

    (1926)
  • I. Horáček et al.

    Comments on the Weichselian small mammal assemblages in Czechoslovakia and their stratigraphical interpretation

    N. Jb. Geol. Paläont. Mh.

    (1984)
  • W.F. Hutchinson et al.

    Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability

    Evolution

    (1999)
  • D. Jánossy

    Fossile Microtinen aus dem Karpatenbecken, I, Lemminge

    Ann. Hist. Nat. Mus. Hung. SN

    (1954)
  • K. Kavanagh et al.

    Predicting evolutionary patterns of mammalian teeth for development

    Nature

    (2007)
  • S. Klopfstein et al.

    The fate of mutations surfing on the wave of a range expansion

    Mol. Biol. Evol.

    (2005)
  • V.A. Kochev

    An Estimation of Age of Quaternary Sediments by Fossil Remains of Collared Lemmings

    (1984)
  • Cited by (11)

    • European small mammal faunas during Dnieper (Saale) glaciation and transition to the Mikulino (Eem) interglacial

      2021, Quaternary International
      Citation Excerpt :

      The species were identified based on anterior loop structure on the first lower molar and the structure of upper molars (M1 and M2) (Agadjanian, 2009). Whether those species are entitled to be considered as chronospecies – is still debatable (Montuire et al., 2019). In this text, the collared lemming is commonly denoted as Dicrostonyx sp.

    • The Middle Pleistocene small mammals from the lower layers of Tunel Wielki Cave (Kraków-Częstochowa Upland): An Early Toringian assemblage in Poland

      2021, Quaternary International
      Citation Excerpt :

      to Nadachowski et al., 2009) or D. torquatus (acc. to Montuire et al., 2019) are most probably related to MIS 6. To partially fill the gap in the early Middle Pleistocene faunistic context in Poland, here we present a small mammal assemblage from the lower layers of Tunel Wielki, which represents the first Early Toringian assemblage in Poland.

    View all citing articles on Scopus
    View full text