Ontogenetic Tooth Reduction in Stenopterygius quadriscissus (Reptilia: Ichthyosauria): Negative Allometry, Changes in Growth Rate, and Early Senescence of the Dental Lamina

RESEARCH ARTICLE Ontogenetic Tooth Reduction in Stenopterygius quadriscissus (Reptilia: Ichthyosauria): Negative Allometry, Changes in Growth Rate, and Early Senescence of the Dental Lamina Daniel G. Dick1,2*, Erin E. Maxwell1 1 Department of Paleontology, Staatliches Museum für Naturkunde Stuttgart, Stuttgart, Germany, 2 Department of Geoscience, Eberhard-Karls-Universität Tübingen, Tübingen, Germany * Abstract OPEN ACCESS Citation: Dick DG, Maxwell EE (2015) Ontogenetic Tooth Reduction in Stenopterygius quadriscissus (Reptilia: Ichthyosauria): Negative Allometry, Changes in Growth Rate, and Early Senescence of the Dental Lamina. PLoS ONE 10(11): e0141904. doi:10.1371/journal.pone.0141904 Editor: Brian Lee Beatty, New York Institute of Technology College of Osteopathic Medicine, UNITED STATES Received: June 29, 2015 Accepted: October 14, 2015 Published: November 18, 2015 Copyright: © 2015 Dick, Maxwell. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: The authors were funded by the Staatliches Museum für Naturkunde Stuttgart. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. We explore the functional, developmental, and evolutionary processes which are argued to produce tooth reduction in the extinct marine reptile Stenopterygius quadriscissus (Reptilia: Ichthyosauria). We analyze the relationship between mandible growth and tooth size, shape, and count, to establish an ontogenetic trend. The pattern in S. quadriscissus is consistent with hypotheses of tooth size reduction by neutral selection, and this unusual morphology (a functionally edentulous rostrum) was produced by a series of different evolutionary developmental changes that are known for other taxa showing tooth reduction and loss. Specifically, this species evolved functional edentulism by evolutionary changes in the growth allometry of the dentition and by altering growth rates through ontogeny. This observation supports previous hypotheses that S. quadriscissus underwent ontogenetic tooth reduction. Tooth reduction in S. quadriscissus may be caused by unique selective pressures resulting from prey choice and feeding behavior, expanding our current understanding of the mechanisms producing tooth reduction. Introduction Dentition has been convergently reduced in size or lost completely several times throughout vertebrate evolution, despite its importance in individual survival [1]. Loss of such a critical structure requires a complex interaction of developmental and environmental factors, and most extant species which show evolutionary “tooth reduction” are more accurately described as completely edentulous (and hence we use the term “tooth loss” to refer to this condition). Recent advances have improved our understanding of the processes resulting in either A) replacement of the dentition [1], or B) complete loss of the teeth [2]. However, our understanding of processes producing gradual tooth size reduction (without complete tooth loss) is PLOS ONE | DOI:10.1371/journal.pone.0141904 November 18, 2015 1 / 14 Tooth Reduction in Stenopterygius comparatively limited. We demonstrate the existence of a previously hypothesized ontogenetic trend of increasing tooth reduction in the extinct marine reptile Stenopterygius quadriscissus (Reptilia: Ichthyosauria), and explore a potential mechanism producing gradual tooth reduction related to feeding behavior. In doing so, we expand our understanding of dental morphological evolution to include species which show functional edentulism without complete tooth loss. Tooth Reduction: Definitions and Hypotheses In general, our understanding of the processes affecting dental development is restricted to species which show loss of mineralized tooth tissues [1] or complete loss of the dentition [2]. In these species the process of dental development is stopped or altered in early embryonic stages, before the onset of odontogenesis [2]. In addition to tooth loss of this type, some species show extreme reduction in the size of the teeth, resulting in what is functionally equivalent to tooth loss (as has been suggested for Stenopterygius quadriscissus) [3]. Complications in the literature have led to the term “tooth reduction” becoming problematic, as it is used indiscriminately to refer to a number of different morphological and developmental changes. For example, tooth reduction has been used to describe species which show; A) reduction in the size of the teeth relative to other species in the clade, B) species showing reduction in enamel structure, C) reduction in the number of teeth, due either to early senescence of the dental lamina or size reduction of the tooth bearing elements, and D) species which show A, B, and C in conjunction or some different combination [1,3–5]. For the purposes of this article, we define tooth reduction as a reduction in the size of the individual teeth, relative to other morphologically similar species in the same clade, or relative to an earlier ontogenetic stage. Tooth reduction can be further subdivided into a number of more specific terms; tooth height reduction, tooth crown height reduction, tooth tissue reduction, and functional tooth reduction. Here, we define tooth height reduction as a reduction of the entire exposed height of the tooth, including the crown height, the height of the ring of acellular cementum (where present), and the height of the exposed root. Tooth crown height reduction, which is the type of reduction discussed in this article, refers to reduction only of the height of the enamel crown. Tooth tissue reduction, which is not discussed here, can be defined as a reduction in the thickness, extent, and structure of specific tooth tissues, including the enamel, dentine, and cementum. Functional tooth reduction refers to situations wherein a combination of tooth height or tooth crown height reduction results in teeth too small to perform their ordinary function (specifically, teeth are considered functionally reduced if the teeth did not protrude beyond the dental groove, resulting in what is functionally equivalent to true edentulism). Finally, we use the term tooth count reduction to refer to reduction in the number of teeth. Genetic and Evolutionary Perspectives on Tooth Reduction and Loss In addition to semantic confusion, using tooth reduction to mean different combinations of complete tooth or tissue reduction and loss has also created a problematic understanding of the mechanisms resulting in the different morphologies. Tooth loss is generally understood (...truncated)