Evolutionary trends and stasis in carnassial teeth of European Pleistocene wolf Canis lupus (Mammalia, Canidae)
Introduction
Morphometric variations and evolutionary trends through time in Pleistocene species have been investigated in recent years by several authors using different statistical strategies (Lacombat, 2009, Piras et al., 2009, Piras et al., 2012, Magniez, 2010, Desantis et al., 2011, Nishioka et al., 2011, Pandolfi et al., 2011, Raymond and Prothero, 2011, Stefaniak et al., 2012, Lozano–Fernandez et al., 2013, Mazza and Bertini, 2013, Meachen et al., 2014, O'Keefe et al., 2014, van der Made et al., 2014). Several works focused on sequences of fossil populations in order to investigate phenotypic changes and their causes during a time span, the Pleistocene, characterized by important climatic changes (Pandolfi et al., 2011, Mazza and Bertini, 2013, van der Made et al., 2014). Several contributions revealed stasis in time series-oriented paleontological studies (cfr. Piras et al., 2009). Since 1972, palaeontologists investigated on the importance of stasis during evolution (Eldredge and Gould, 1972). Stasis is a central point inside the Punctuated Equilibria Theory (Eldredge and Gould, 1972, Gould and Eldredge, 1977, Gould, 2002, Eldredge et al., 2005). The major focus of this evolutionary model is that the phenotypes are stable through time and no directional trends are observable. The causes of the stasis could be: a) absence of variability; b) balancing selection; c) developmental constriction; d) habitat tracking; e) population structure: a species being structured in semi-isolated metapopulations. Different isolated populations experience different selective pressure thus returning a no neat phenotypic change in time (Wright, 1932, Eldredge and Gould, 1972, Gould and Eldredge, 1977, Gould, 2002, Eldredge et al., 2005).
Most paleontological studies set apart between patterns of stasis, random walk, and directional evolution. Stasis sensu strictu can be defined as when the variance of the total time series sample is not significantly larger than that of a single population in a time lapse (Wood et al., 2007, Piras et al., 2009, Piras et al., 2012). The random walk could be considered as a stasis sensu latu, defined as no neat change in successive steps of population mean values across a discrete ordered time sequence (Hunt and Carrano, 2010). Directional evolution is characterized by a significant trend in population means during the considered time intervals (Wood et al., 2007, Piras et al., 2009, Piras et al., 2012). A particular case of directional evolution for an evolutionary process with selection or drift is the Ornstein–Uhlenbeck model (Hansen, 1997, Butler and King, 2004, Piras et al., 2012), which represents a random walk with a general tendency to an adaptive optimum.
Morphometric variations in the wolf (Canis lupus) have been investigated by several authors but without testing for any evolutionary trend (Boudadi–Maligne, 2010, Boudadi–Maligne, 2012, Brugal and Boudadi–Maligne, 2011, Flower, 2012, Flower and Schreve, 2014, van der Made et al., 2014). The oldest fossil record of the modern wolf is reported in the Olyor fauna (Siberia) and in the Cripple Creek Sump (Alaska) during the Middle Pleistocene. Several authors have proposed an origin of C. lupus in Beringia (Sher, 1986, Tedford et al., 2009; among others). In Europe, the first occurrence of the modern wolf, with the subspecies C. lupus lunellensis (Bonifay, 1971), is reported at Lunel-Viel (France), chronologically referred to MIS 11–10 (0.4–0.35 Ma: Argant and Mallye, 2005, Mallye, 2007, Croitor et al., 2008, Boudadi–Maligne, 2010). Other subspecies of wolf have been described in France during the Pleistocene: C. lupus santenaisensis (Santenay site, MIS 6–5), C. lupus mediterraneus and C. lupus maximus (Jaurens Cave, MIS 3) (Bonifay, 1971, Argant, 1991, Brugal and Boudadi–Maligne, 2011, Boudadi–Maligne, 2012). In the Italian peninsula, the first record of the modern wolf is at La Polledrara di Cecanibbio (late Middle Pleistocene; Gliozzi et al., 1997, Petronio et al., 2011, Anzidei et al., 2012, Sardella et al., 2014). The morphology of C. lupus remains collected at La Polledrara di Cecanibbio is very similar to that of the modern wolf (Sardella et al., 2014). The modern wolf from the Apennine area is referred to the subspecies C. lupus italicus upon phenotypic (Altobello, 1921), morphometric (Nowak and Federoff, 2002, Nowak, 2003) and genetic features (Randi et al., 2000, Fabbri et al., 2007, Pilot et al., 2010). No subspecies of C. lupus have been described in Italy through the Pleistocene.
In this paper, we investigated evolutionary models in the carnassial teeth of C. lupus from the Pleistocene of Southern Europe. Within canids, premolars and molars are used for slicing and for grinding, respectively (Ewer, 1973, Ungar, 2010). The upper carnassials, within all carnivores, are used only for slicing (Butler, 1946), whereas the lower carnassials play both functions in canids: the trigonid is used to slice and the talonid to grind (Ewer, 1973, Ungar, 2010). The ratio between trigonid and talonid is a valid indicator of the dietary habits (Ewer, 1973, Van Valkenburgh and Wayne, 1994, Ungar, 2010). The lower carnassial length can be used to estimate carnivore body size (Van Valkenburgh, 1990, Van Valkenburgh, 1991, Van Valkenburg, 2007) due to its low variability and because tooth size is fixed upon eruption (Gingerich, 1974).
We focused on two questions: does exist an evolutionary trend in carnassial teeth of the wolf through the Pleistocene‒Holocene? Does exist a relationship between climate change and carnassial teeth through time? We used linear measurements of European wolves to explore and better understand the evolutionary dynamics of the carnassial morphology during the Pleistocene using modern statistical tools.
Section snippets
Materials
We collected 486 and 491 linear measurements (in mm) on the first lower molar and fourth upper premolar, respectively, i.e. the carnassial teeth (Fig. 1).
Data of extant and fossil C. lupus are from Argant (1991), Malez and Turk (1991), Ziegler (1996), Fladerer (1997), Fladerer and Einwögerer (1997), Pacher and Döppes (1997), Boudadi–Maligne, 2010, Boudadi–Maligne, 2012, Bertè (2013), Bertè and Pandolfi (2014) and Sardella et al. (2014). All of these authors strictly followed the morphometric
Results
ANOVAs performed on the several datasets (global sample of length and width of M1, and length, width and maximum width of P4) reveal significant differences of carnassials in space (if comparing the teeth dimensions with the different geographical areas) and in time (if comparing teeth dimension with the different time ranges: recent to 0.38 Ma) among the several C. lupus populations (p-value < 0.05, see Table 2). The evolutionary models resulting from the analyses on entire sample are reported
Discussion and conclusions
The overall results reported above show two different evolutionary patterns of the carnassials within C. lupus. M1 is characterized by a phenotypic fluctuation during Middle–Late Pleistocene and Holocene towards an adaptive optimum. However, investigating the phenotypic patterns within Italian and French wolves separately, have revealed how an absence of directionality describes the lower carnassial through time. When considering French and Italian wolves as a single dataset, a directional
Acknowledgments
We thank the editor Prof. J. Carrión and two anonymous reviewers for insightful suggestions on an earlier draft of the manuscript. We are grateful to C. Petronio, A. Vigna Taglianti, L. Boitani, R. Sardella (Sapienza, Università di Roma), A. Tagliacozzo (Museo Nazionale Preistorico-Etnografico “L. Pigorini”, Roma), R. Zorzin and A. Vaccari (Museo Civico di Storia Naturale di Verona), M. Pavia (Museo Regionale di Scienze Naturali di Torino), C. Violani and S. Maretti (Università degli Studi di
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