Evolution of the sabertooth mandible: A deadly ecomorphological specialization
Introduction
Felids (Mammalia, Carnivora) form a morphologically homogenous, monophyletic clade, including strictly carnivorous species. In contrast to other meat-eating mammals, felids only retain the anterior, slicing portion in their lower molars, while the crushing part (the talonid) is lost (Meloro et al., 2007; Van Valkenburgh, 2007). Felids (Felidae plus Barbourofelidae families) can be ecomorphologically subdivided into two categories: conical-toothed cats and sabertooths (Van Valkenburgh, 2007). The former borrow their name from the shape of their canines in cross section (Martin et al., 2000). They include the modern cat genera such as Felis, Panthera, and Acinonyx. Sabertooth cats were characterized by laterally-compressed, extremely long upper canines, procumbent incisors, reduced coronoid process, and low glenoid fossa (Christiansen, 2008a, Christiansen, 2008b, Christiansen, 2006; Slater and Van Valkenburgh, 2008). All of these features conferred on sabertooths a unique killing behavior. The success of the sabertooth morphology is testified by its iterative evolution among meat eating mammals (Van Valkenburgh, 2007). Sabertooths are known among Thylacosmilidae, an extinct clade of South American marsupials of the Miocene and Pliocene (Antón, 2013), and Creodonta, which lived in North America in the Paleocene and Eocene (Antón, 2013). Within Carnivora, the sabertooth morphology appeared in the Nimravidae family, which emerged in late Eocene (Bryant, 1991), the Barbourofelidae family (known from the early Miocene, Morlo et al., 2004), and in the true cat subfamily Machairodontinae, which radiated between Miocene and Late Pleistocene (Hunt Jr., 1996; Werdelin et al., 2010).
Sabertooths' highly derived cranial morphology (Christiansen, 2008a; McHenry et al., 2007; Wroe et al., 2008), and the extremely long yet fragile upper canines, did not allow the exploitation of a wide prey spectrum (Mondanaro et al., 2017). The peculiar morphology and narrow feeding niche make sabertooths the most specialized among mammalian carnivores (Binder and Van Valkenburgh, 2010; Emerson and Radinsky, 1980; Goswami et al., 2011; Randau et al., 2013). In ecological terms, specialization usually translates in competitive advantages (or reduced competition) over other guild members. Yet, it may also be associated with increased extinction risk (Cardillo et al., 2005; Colles et al., 2009; Kingsolver and Pfennig, 2004; Raia et al., 2016; Slatyer et al., 2013).
Herein, we collected and analyzed the largest felid plus barbourofelid mandible collection to date in order to better understand the evolutionary processes leading to the sabertooth specialization. We used Geometric Morphometrics to retrieve information on mandible shape and mechanical performance. Then, we inferred a felid plus barbourofelid phylogenetic hypothesis (Fig. 1) to compute rates of morphological evolution, and tested for phenotypic rate shifts in the tree, under the hypothesis that the sabertooth character represents a morphological discontinuity in felid evolution. We further presumed that the acquisition of the sabertooth morphology increased extinction rates (Liow, 2004; Van Valkenburgh, 2007; Raia et al., 2011). To test for this hypothesis, for each of the two felid ecotypes (conical-, and saber-toothed) we calculated diversification rates and its components (i.e. rates of speciation and extinction) directly from the fossil record, and contrasted sabertooth's versus conical-toothed's rates.
Section snippets
Data and tree
We assembled an informal, time-calibrated phylogenetic supertree containing 157 species representing all extant and extinct valid taxa, as based on the extensive review of the primary literature on felid systematics and phylogeny (see Table S3 and supplementary material for details about the tree preparation). The tree was later pruned to the 88 species (felids plus barbourofelids taxa) for which we had phenotypic data (Table S1), and including all of the species for which at least one complete
Geometric morphometrics
The first four PCs explain cumulatively 77.7% of total variance. In particular, PC1 captures 44.7% of shape variance. This axis is a good descriptor of the morphological difference between.
sabertoothed and conical-toothed cats. Positive values of this axis are associated with long and slender jaws typically of modern felids and characterized by the absence of the mandibular flange medially to the upper canines, which is typical of a number of sabertooths. Towards negative values the coronoid
Discussion
The mandible is the primary feeding device in carnivores (Meloro and O'Higgins, 2011; Meloro et al., 2008). Hence, understanding its evolution is instrumental to comprehend the evolution of carnivore ecomorphology. Geometric morphometrics indicates a clear separation between sabertoothed and conical toothed cats in mandible shape (Fig. 2), which bears a profound adaptive significance. Sabertooths show a considerable reduction of the coronoid process as compared to other felids (Emerson and
Conclusions
The sabertooth character evolved at least seven times among carnivorous mammals and mammal-like reptiles. Sabertooths shows an exceptionally specialized, highly derived morphology different clades converged upon. While the iterative evolution of the sabertooth character in mammals proves it is an evolutionary success, the extreme craniodental specialization the acquisition of the sabertooth morphology brings about implies increased extinction risk, which probably helps explaining why
Acknowledgments
PyRate analyses were run at the High-performance Computing Center (Vital-IT) from the Swiss Institute of Bioinformatics. D.S. received funding from the Swedish Research Council (2015-04748) and from the Knut and Alice Wallenberg Foundation (Sweden).
Additional information
The authors declare no Competing Financial Interests.
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