Odontology

, Volume 103, Issue 2, pp 117–125 | Cite as

Gene networks, occlusal clocks, and functional patches: new understanding of pattern and process in the evolution of the dentition

Review Article

Abstract

Our understanding of the evolution of the dentition has been transformed by advances in the developmental biology, genetics, and functional morphology of teeth, as well as the methods available for studying tooth form and function. The hierarchical complexity of dental developmental genetics combined with dynamic effects of cells and tissues during development allow for substantial, rapid, and potentially non-linear evolutionary changes. Studies of selection on tooth function in the wild and evolutionary functional comparisons both suggest that tooth function and adaptation to diets are the most important factors guiding the evolution of teeth, yet selection against random changes that produce malocclusions (selectional drift) may be an equally important factor in groups with tribosphenic dentitions. These advances are critically reviewed here.

Keywords

Occlusion Tribosphenic teeth Evolution Developmental networks 

Introduction

The dentition has become a model system for understanding patterns of processes of evolution. Even though the outlines of dental evolution had already been sketched by the 1970s, including a general understanding of form, function, homology, embryology, and genetic heritability [1, 2, 3, 4, 5, 6, 7], only recently have the detailed mechanisms of dental evolution been revealed. Evolution is a hierarchical process with mechanisms that operate at many levels from genes, biochemical pathways, cells, and tissues to functional morphology, population genetics, macroevolution, and evolutionary ecology. Advances in molecular developmental genetics of teeth, computational modeling, functional morphology, and field experimentation have connected these hierarchical links allowing data from histology to paleontology to be integrated into a cohesive evolutionary framework [8, 9]. Here I review advances that are key to our understanding of the mechanisms that underpin the variation and evolution of the dentition.

Developmental genetic underpinnings

Selection and drift, the primary mechanisms of evolutionary change, operate at the level of the individual because differences between the reproductive legacies of individuals determine which phenotypes are inherited by descendant generations. Nevertheless, processes operating at the levels of genes, gene networks, and tissue interactions are key for understanding how phenotypes are produced and what causes them to vary among individuals. The evolutionary consequences of natural selection and genetic drift thus stem from changes in genetic structure, levels of gene expression, combinations of genes, and the timing and spatial distribution of gene expression that emerge from selection on individuals. Advances in dental morphogenesis have led to a new understanding of the processes that produce variation in tooth crowns and dentitions, of how genetic transformations translate into changes in dental phenotype, and about biases in genetic and phenotypic transformations that make some changes more likely than others.

Developmental genetic research has demonstrated that tooth crown development is largely controlled by iterative molecular signaling between primary and secondary enamel knots, which moderates a signaling cascade between the ectodermal dental epithelium and the underlying mesenchymal dental papilla [10, 11, 12, 13]. The spatial relationships between the folding tissue layers in the tooth germ and the concentration and diffusion of signaling molecules create a morphodynamic system that can generate a vast range of crown types from simple uni-cusped structures like mammalian canines to complex multi-cusped teeth like those of the extinct rodent-like Multituberculata [14, 15]. Interestingly, the enamel knot cascade appears to be a derived feature of mammals that is not found in lizards or crocodilians, even those with multi-cusped teeth [16, 17, 18, 19]. Modifications of the expression of genes involved in the enamel knot cascade are the primary mechanism for transforming one crown type into another [12, 20].

The dentition as a whole is patterned by homeobox genes and other signaling molecules that affect the number and spacing of teeth and the forms of their crowns. Differentiation between incisor, canine, premolar, and molar fields is largely mediated by expression of homeobox genes such as Barx1, Dlx2, Msx1, and Msx2 and their regulators [21, 22, 23]. Differentiation of teeth in different fields is in part controlled by downstream effects of gene expression within the homeobox domains on the gene networks involved in the enamel knot cascade resulting in different tooth types within the same dentition. In species with strongly differentiated teeth, the homeobox fields typically correspond to patterns of phenotypic and genetic integration [24, 25, 26, 27, 28]. Within the fields, diffusion processes of activator and inhibitor molecules influence the relative size of teeth within the field and the gain and loss of teeth [29, 30]. Some genes blur the spatial patterning of homeobox domains by affecting the morphology of the entire dentition, such as Eda expression which influences cusp number [31]. Quantitative genetic parameters like heritability of tooth size and shape [4, 7] arise from parent-to-offspring transmission of the underlying molecular developmental network of individual teeth and the dentition as a whole [8, 32]. The evolution of the dentition is thus achieved by modifications to genes or levels of regulatory gene expression within and across the spatial domains [9, 21]. The regulatory networks are modified by evolutionary processes to make the dentition more homogeneous or differentiated, to acquire or lose individual teeth or entire tooth fields, or to alter the morphology of teeth within fields or across the entire dentition.

These developmental and genetic breakthroughs now provide a broad framework for understanding how tooth form is controlled and the mechanisms by which it differentiates and changes. Nevertheless, many details are still only dimly understood, such as the precise mechanisms by which differences between adjacent teeth within a series are controlled or by which differentiation of tooth types is produced in some taxa but not in others. Even the mechanisms by which teeth are gained and lost are incompletely understood. Much remains to be done.

Form, function, fitness, and environment

A better understanding of the role of natural selection in dental evolution has also been achieved in recent years. Dental form is closely related to masticatory efficiency and dietary function [33, 34, 35, 36, 37, 38]. The correspondence between form and function has long suggested that selection must play a role in optimizing a species’ dentition for its diet (or vice versa) [39], but very few studies of natural selection in the wild of the effects of dentition on reproductive fitness had been made until recently.

The effect of dental form and function on reproductive fitness, and thus natural selection, was recently studied in Malagasy lemur populations over the course of two decades [40, 41, 42]. Dental senescence (lifetime wear and degradation of the dentition) resulted in decreased masticatory efficiency as lemurs aged and their teeth became more worn. Older individuals were still capable of processing tender vegetation, but had increasing difficulty with tougher foodstuffs. This change did not affect fertility, which remained high in older individuals, but it did increase infant mortality in dry years by decreasing an older mothers’ ability to nourish young offspring via lactation. Older mothers could not process tougher foodstuffs during dry years efficiently enough to meet the nutritional needs of both themselves and their dependants. Females with longer lasting dentitions thus contribute more offspring to subsequent generations during times of drought, providing a mechanism by which arid conditions can trigger natural selection for more durable dentitions.

Teeth and nutrition are involved in many aspects of an individual’s health, longevity, and reproductive potential, which means that rate of wear is unlikely to be the only factor linked to natural selection. Dental functions that have the potential to impact fitness include precision of occlusal fit, which can affect food processing efficiency [37, 38, 43, 44]; proportional size of the upper and lower arches, which can also impact occlusal fit [45, 46, 47]; duration of dental development, which determines the age at which an individual can start processing food [48]; and physiological cost of dental development, which can compete with physiological processes such as growth, bone formation, reproduction, and lactation [49, 50, 51, 52]; and risk of infection or other health problems due to tooth impacts, periodontal damage, and other dental problems [53, 54]. Presumably all of these factors affect reproductive fitness with different frequencies and strengths, creating a selective landscape in which dental variation is filtered by a weighted combination of factors. The selective landscape of the dentition is further complicated by tooth wear. The effect of wear on dental function varies from taxon to taxon, with some taxa maintaining the same functional properties despite wear-driven changes in form and other taxa undergoing a wear-based change in tooth function [55]. No absolute relationship between wear and dental senescence therefore exists.

As environments change, the links between dentition, environment, fitness, and selection are expected to cause the average form of the dentition to evolve. This process occurs through time, but it is mirrored spatially within environments that vary geographically creating spatially different selective optima. Tooth form is, in fact, known to vary geographically among populations of the same species and between closely related species that have arisen by allopatric differentiation [25, 56, 57, 58, 59, 60, 61]. Dental differences between such populations tend to be small, however, and whether they arise from selection or drift is not always obvious, as discussed below. Over longer evolutionary timescales dental evolution is more obviously linked to environmentally related changes in diet, exemplified by changes in tooth crown height in mammalian herbivores in relation to aridity and plant abrasiveness. The crowns of herbivore species are, on average, higher in arid regions or grasslands than in moist and forested areas [62, 63]. This correlation between environment and dentition likely arises from a combination of local selection for high crowned and consequently durable teeth and from diet-based sorting of species into regions where herbaceous growth is compatible with their tooth form [63, 64].

Dental microevolution: selection or drift?

The relative importance of natural selection and genetic drift in dental evolution, including the small differences in teeth observed between populations of the same species, is unclear to some extent; however, growing evidence suggests that selection predominates because evolutionary change in tooth form observed in the fossil record or in phylogenetic comparisons of living taxa is often faster than expected from drift alone. Drift consists of random, functionless changes in morphology that occur when certain dental features are coincidentally associated with the individuals that contribute offspring to the next generation [65]. The process of drift is a form of sampling error that results in change in the average teeth from one generation to the next. The rate of drift is a function of effective population size, phenotypic variance, and heritability and can be estimated if these parameters are known [66, 67]. Drift is fastest in very small, highly variable populations and slower in larger populations.

Studies of variation in tooth, mandibular, and maxillary shape in the Common shrew, Sorex araneus, and other taxa have shown that dental evolution is usually faster than can be explained by drift alone. The Common shrew is a widespread Eurasian species that is fragmented into more than 70 local karyotypic races, each with a unique arrangement of chromosomes that frequently interfere with reproduction between populations, thus making it a model system for studying gene flow and microevolutionary differentiation in the wild [68]. Tooth and mandibular shape differences among the karyotypic groups and their sister species, which varies in a broad geographic cline that stretches across Eurasia from Britain to Baikal, is too great to be attributed to drift alone [56, 58, 69]. Adjacent (peripatric) karyotypic groups of the Common shrew are known to hybridize, presumably after coming back in geographic contact after expanding from isolated glacial refugia [68, 70]. Drift is sufficient to explain differences observed between populations across such hybrid zones, but whether the seemingly small differences measured at the present time arose due to drift or whether they are remnants of historically larger differences that have already been lost through gene flow, thus erasing the effects of past selection during refugial isolation, is unclear [71]. Fossil evidence suggests the latter [56, 72].

Dental changes also track environmental changes through time within a population, even over short timescales. One study measured change in mandibular morphology in a population of Yellow-necked mouse in which boom-bust cycles in population size tracked cycles of mast in an oak, linden, and hornbeam forest over a period of about seven generations [73]. The changes in mandible size and shape were too rapid to be explained by drift compared to a control of non-functional traits in the skull that did evolve by drift. Another study on dentition in a high-latitude population of common shrews over about 25–50 generations showed rates of change that were too rapid for drift and which were correlated with local variation in summer temperatures and precipitation over the same time period [74].

All of these comparative observations are consistent with the field-based study of dental senescence in lemurs in suggesting that environmentally driven selection on teeth has a measureable effect on dental morphology even over short timescales.

An ‘occlusal clock’ for evolution?

Despite the preponderance of evidence that natural selection rather than drift drives the evolution of dental morphology, the pattern of evolutionary divergence in teeth often appears to be random. Stochastic processes, such as Brownian motion, have statistically predictable outcomes that allow random patterns to be distinguished statistically from directional or stabilizing selection [75, 76]. In shrews, for example, which have tightly interlocking tribosphenic dentitions, dental divergence among populations and species fits a model of random evolution [69, 72]. Random evolutionary patterns are usually interpreted as evidence for drift, but natural selection that arises from random changes in environment can cause seemingly neutral changes in the direction and magnitude of evolution in a process known as selective drift [77, 78, 79]. Selective drift appears to explain evolution of the tightly interlocking teeth of shrews and bats [69, 80] (Fig. 1a, b), and perhaps also the lower crowned teeth of marmots and humans, the latter of which were more constrained in their divergence as would be expected from clade-wide stabilizing selection, which is an Ornstein–Uhlenbeck mode of evolution [28, 57]. These clades are all relatively recent in geological terms, having last common ancestors within the last 5–20 million years. Despite their random patterns of dental evolution, the rates of evolution observed in these groups are too high to arise from drift unless population sizes are unrealistically small, which suggests that evolution is driven by selective drift in which tooth morphology has selectively tracked an unknown and randomly changing factor. Interestingly, however, diet does not seem to be the factor. Dietary differences within the shrews and bats are negligible, marginal with the marmots, and larger within hominins [58, 59, 81, 82]. If not diet, then what factor is driving selection on tooth shape?
Fig. 1

Upper (a) and lower (b) tribosphenic cheek teeth of the bat Eptesicus fuscus showing the tightly interlocking crown features. P upper premolar, M upper molar, p lower premolar, m lower molar. The fit between uppers and lowers in different individuals becomes linearly worse the more distantly related they are (c). [after 80]

Occlusal fit may be the answer. Tribosphenic molars, like those in shrews and bats, interlock tightly and their ability to process food and maintain sharp shearing blades depends on the fit between upper and lower teeth [37, 38, 83, 84]. The match between upper and lower counterparts in the dentition is so precise that it has been used not only to study functional transitions in dental evolution [85, 86], but also to literally associate isolated upper and lower teeth in the fossil record [87, 88]. Occlusion in high-relief carnivorous or insectivorous teeth is likely to affect fitness because tight fits between their shearing blades is critical to prey capture and processing; indeed, malocclusion could severely interfere with mastication if it prevented shearing blades from sliding past one another. If the inefficiency of food processing impacted fitness, as it might well do given the example of dental selection in lemurs, then selection for precise occlusion is expected to be strong. Change in morphology of an upper or lower tooth is likely to interfere with occlusion and lower the individual’s fitness unless it is accompanied by a corresponding change in the counterparts in the opposite dental arch. Selection should therefore favor either a directional change in the counterpart teeth or a stabilizing reversal in the first tooth. If variation in tooth shape is independent, or even semi-independent, in the two arches, then drift in tooth morphology will drive selection to maintain occlusion, an example of Kimura’s selective drift [77].

Evolution of occlusal fit in bats suggests this might be the case. Occlusal fit between upper and lower molars in bats has a linear relationship with phylogenetic divergence [80]. In that study, occlusal fit was measured with geometric morphometrics [89] by placing landmarks on occluding surfaces of the upper and lower molars. Procrustes superimposition was used to lock the two together as tightly as possible. In this way, the fit of upper and lower teeth belonging to the same individual could be measured and compared to uppers and lowers from different individuals in the same population, from different populations, and from different species. The fit becomes linearly worse the more distantly related the two individuals are (Fig. 1c). The linearity of this pattern suggests both a stochastically constant process like drift and a selection-based coevolution between counterparts, consistent with selective drift. All of the bat species studied were insectivorous and differ more in the mode of prey capture, and therefore more in the flight specializations than the material properties of the insects they eat [90]. Selection in this case therefore does not appear to be optimizing the teeth for new dietary functions, but simply maintaining optimization for an insectivorous diet by preserving occlusal precision. Rapid divergence in shrews of the phenotypic covariance pattern of the tooth crowns, which are a measure of the relationships of one tooth cusp to another, support the hypothesis that selectional drift plays a role because the covariance evolution is neither associated with dietary changes nor is it closely related to the covariances imparted by the developmental cascade that patterns the spacing of cusps [91].

Occlusion in non-mammals

Mammals have long been considered unique because of their complex occlusion, but recent advances have refined our understanding of the evolution of tooth-on-tooth movements in vertebrates. Wear striations on fossil teeth demonstrate that dental occlusion evolved independently in ten or more clades of amniote vertebrates, many of them are herbivores like the sail-backed synapsids of the Edaphosauridae [92, 93, 94, 95, 96]. Even conodonts, tiny jawless lamprey-like animals that were common in Paleozoic seas, have sophisticated tooth-on-tooth feeding movements [97, 98]. Ornithopod and ceratopsian dinosaurs used transverse jaw movements, facilitated in some taxa by cranial kinesis, to chew with batteries of herbivorous teeth in ways that are analogous to mammalian ungulates [99, 100, 101]. And an explosion of new fossil finds of early mammals and closely related synapsids has added complexity to the history of the interlocking teeth and bi-phasic masticatory cycle that characterize mammals [102, 103, 104].

Avoiding fitness risks associated with malocclusion

Despite the existence of occlusal relationships in non-mammalian teeth, the precision and complexity of interlocking patterns in mammalian teeth is far greater than in other taxa. The evolutionary ratchet that is implied by the selectional drift hypothesis suggests that the tightly interlocking mammalian patterns are less likely to convey fitness in a given environmental context than teeth whose occlusal pattern is simpler and more forgiving. Mammals have a number of mechanisms that may mitigate the fitness risks that come with malocclusion. In all mammals, the periodontal ligament and alveolar bone allow for a certain amount of plastic readjustment that can help align occlusal relationships. Many herbivores and some omnivores have occlusal contacts that ordinarily develop via wear, creating a good fit between uppers and lowers in the process [105, 106, 107, 108]. Other, less intuitive mechanisms add plasticity to the development of occlusion. For example, wear on tightly locking shearing crests in carnivores helps maintain their sharpness [83], which combined with carnassial rotation in which the tooth’s orientation changes as the occlusal surfaces on the blades wear [109] can maintain a precise shearing function even as the tooth crown is abraded. Zalambdodont dentitions, which have interlocking v-shaped teeth, typically require less occlusal precision than the complex interdigitizing shearing blades of tribosphenic teeth [110].

These mechanisms help maintain functional occlusion without relying purely on development and genetics to match the forms and placements of occluding upper and lower teeth. In doing so, they provide a buffer on selection because they make allowances for otherwise imperfectly occluding tooth morphologies to meet masticatory needs. The quadrate teeth of omnivores and herbivores, which have more such mechanisms than the ancestral tribosphenic dentition, have evolved independently in more than 20 lineages, a key feature that is associated with increased diversification [111].

New techniques for studying functional evolution in teeth

Our understanding of the evolution of the dentition has also been improved by new quantitative analytical techniques. Three-dimensional scans allow skulls and dentitions to be manipulated in silico to explore hypotheses about how patterns of mandibular movements, occlusal surfaces of teeth, and muscular moment arms contributed to masticatory patterns, even in long extinct species [37, 38, 100, 112, 113]. New tools developed for the analysis of 3D data, like occlusal fingerprint analysis (OFA), have been adapted from methods used to study human occlusion to understand ancient fossil dentitions [114, 115, 116]. Extensions of OFA using applications from engineering, like finite element analysis (FEA), have allowed not only dynamic occlusal patterns, but also masticatory stresses and strains to be modeled [117]. Tools for shape measurement, including geometric morphometrics, have also been applied to understand processes of dental form, occlusion, and diet in the evolution of dental form and function [28, 59, 118, 119, 120, 121]. Other techniques, like orientation patch count (OPC), have been innovatively synthesized from general principles of occlusal function and topographic analyses developed for geographic analysis [122, 123]. OPC is a seemingly abstract, yet theoretically grounded count of the number of contiguous patches of crown surface that have a unique spatial orientation. Teeth with large shearing blades from hypercarnivores like cats, for example, tend to have a few number of large surfaces that are oriented in parallel, whereas the granivorous or herbivorous of mice, rats, and their relatives tend to have many small cusps and crests have a larger number of smaller patches. OPC provides a means for estimating the diet of animals, both living and fossil, and for quantitatively comparing their occlusal complexity and has now been used in several studies to assess evolutionary changes in dental function [124, 125, 126, 127].

An integrated framework of dental evolution

The emerging model of dental evolution is both more complicated than previous understandings, yet able to produce major changes in tooth form through seemingly simpler mechanisms. The spatial mosaic of developmental genetic factors within the dental arches allows for complex functional and evolutionary dynamics [9, 128]. Within-field diffusive effects can homogenize or differentiate teeth along the dental arch [29] and cross-field effects of genes like Eda can induce parallel changes in the morphology of many teeth [31]. Furthermore, the physical dynamics of developing tooth germs, signaling centers, and tissue layers can fundamentally affect morphological outcomes independent of the developmental genetics of the signal molecules themselves [14, 15]. As a consequence, evolutionary change in the dentition can involve morphological jumps that emerge from continuous changes in the underlying developmental genetic apparatus, as well as rapid convergent evolution in the overall form of the dentition or in specific features and asymmetries in the direction of evolutionary change [20]. These complex dynamics can pose special challenges for phylogenetic or morphometric studies of the dentition, many of which remain analytically unsolved, because the morphological transitions that arise from genetic changes are not necessarily independent, continuous, or linear [31, 129]. Most interestingly, the developmental genetic factors that are responsible for changes in the dentition can be relatively high level in the regulatory network or low level in individual genes. The gain of new dental features or parallel acquisitions in distantly related clades is likely to involve the higher levels, whereas their loss is likely to involve changes at low levels [130].

Notes

Acknowledgments

Thanks to the editors of Odontology for inviting this review, to M. Fortelius and J. Jernvall for providing references, and for two anonymous reviewers whose comments improved the text. Philip Myers of the University of Michigan Museum of Zoology provided access to the bat specimen in Fig. 1. This paper is dedicated to Percy M. Butler, who pioneered the study of dental evolutionary developmental biology and who passed away at the age of 102, still engaged in active research on teeth, while this review was being prepared.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Osborn HF. In: Gregory WK, editor. Evolution of mammalian molar teeth to and from the triangular type. New York: Macmillan; 1907.Google Scholar
  2. 2.
    Kurtén B. On the variation and population dynamics of fossil and recent mammal populations. Acta Zool Fenn. 1953;76:1–122.Google Scholar
  3. 3.
    Butler PM. The ontogeny of molar pattern. Biol Rev. 1956;31:30–70.Google Scholar
  4. 4.
    Grüneberg H. Genes and genotypes affecting the teeth of the mouse. J Embryol Exp Morphol. 1965;14:137–59.PubMedGoogle Scholar
  5. 5.
    Peyer B. Comparative odontology. Chicago: University of Chicago Press; 1968.Google Scholar
  6. 6.
    Crompton AW. The origin of the tribosphenic molar. In: Kermack DM, Kermack KA, editors. Early Mammals. London: Academic Press; 1971. p. 65–88.Google Scholar
  7. 7.
    Alvesalo L, Tigerstedt PMA. Heritabilities of tooth dimensions. Hereditas. 1974;77:311–8.PubMedGoogle Scholar
  8. 8.
    Zhao Z, Weiss KM, Stock DW. Development and evolution of dental patterns and their genetic basis. In: Teaford MF, Smith MM, Ferguson MWJ, editors. Development, function, and evolution of teeth. Cambridge: Cambridge University Press; 2000. p. 152–72.Google Scholar
  9. 9.
    Jernvall J, Thesleff I. Tooth shape formation and tooth renewal: evolving with the same signals. Development. 2012;139:3487–97.PubMedGoogle Scholar
  10. 10.
    Jernvall J, Kettunen P, Keränen S, Thesleff I. Evidence for the role of the enamel knot as a control center in the mammalian tooth cusp formation: non-dividing cells express growth stimulating Fgf-4 gene. Int J Dev Biol. 1994;38:463–9.PubMedGoogle Scholar
  11. 11.
    Jernvall J, Åberg T, Kettunen P, Keränen S, Thesleff I. The life history of an embryonic signaling center: bmp-4 induces p21 and is associated with apoptosis in the mouse tooth enamel knot. Development. 1998;125:161–9.PubMedGoogle Scholar
  12. 12.
    Jernvall J. Mammalian molar cusp patterns: developmental mechanisms of diversity. Acta Zool Fenn. 1995;198:1–61.Google Scholar
  13. 13.
    Thesleff I, Sahlberg C. Growth factors as inductive signals regulating tooth morphogenesis. Sem Cell Dev Biol. 1996;7:185–93.Google Scholar
  14. 14.
    Salazar-Ciudad I, Jernvall J. A gene network model accounting for development and evolution of mammalian teeth. Proc Natl Acad Sci USA. 2002;99:8116–20.PubMedCentralPubMedGoogle Scholar
  15. 15.
    Salazar-Ciudad I, Jernvall J. A computational model of teeth and the developmental origins of morphological variation. Nature. 2010;464:583–6.PubMedGoogle Scholar
  16. 16.
    Trapani J, Yamamoto Y, Stock DW. Ontogenetic transition from unicuspid to multicuspid oral dentition in a teleost fish: Astyanax mexicanus, the Mexican tetra (Ostariophysi,: Characidae). Zool J Linn Soc. 2005;145:523–38.Google Scholar
  17. 17.
    O’Connor PM, Sertich JJ, Stevens NJ, Roberts EM, Gottfried MD, Hieronymus TL, Jinnah ZA, Ridgely R, Ngasala RS, Temba J. The evolution of mammal-like crocodyliforms in the Cretaceous period of Gondwana. Nature. 2010;466:748–51.PubMedGoogle Scholar
  18. 18.
    Handrigan GR, Richman JM. Unicuspid and bicuspid tooth crown formation in squamates. J Exp Biol. 2011;316B:171–86.Google Scholar
  19. 19.
    Richman JM, Handrigan GR. Reptilian tooth development. Genesis. 2011;49:247–60.PubMedGoogle Scholar
  20. 20.
    Harjunmaa E, Seidel K, Häkkinen T, Renvoisé E, Corfe IJ, Kallonen A, Zhang ZQ, Evans AR, Mikkola ML, Salazar-Ciudad I, Klein OD, Jernvall J. Replaying evolutionary transitions from the dental fossil record. Nature. 2014;512:44–8.PubMedGoogle Scholar
  21. 21.
    Tucker AS, Matthews KL, Sharpe PT. Transformation of tooth type induced by inhibition of BMP signaling. Science. 1998;282:1136–8.PubMedGoogle Scholar
  22. 22.
    Ferguson CA, Tucker AS, Sharpe PT. Temperospatial cell interactions regulating mandibular and maxillary arch patterning. Development. 2000;124:4811–8.Google Scholar
  23. 23.
    Tucker AS, Sharpe PT. The cutting edge of mammalian development; how the embryo makes teeth. Nat Rev Genet. 2004;5:499–508.PubMedGoogle Scholar
  24. 24.
    Gingerich PD, Winkler DA. Patterns of variation and correlation in the dentition of the Red Fox, Vulpes vulpes. J Mamm. 1979;60:691–704.Google Scholar
  25. 25.
    Szuma E. Variation and correlation patterns in the dentition of the Red fox from Poland. Ann Zool Fenn. 2000;37:113–27.Google Scholar
  26. 26.
    Meiri S, Dayan T, Simberloff D. Variability and correlations in carnivore crania and dentition. Funct Ecol. 2005;19:337–43.Google Scholar
  27. 27.
    Hlusko LJ, Sage RD, Mahaney MC. Modularity in the mammalian dentition: mice and monkeys share a common dental genetic architecture. J Exp Zool B Mol Dev Evol. 2011;316B:21–49.Google Scholar
  28. 28.
    Gómez-Robles A, Polly PD. Morphological integration in the hominin dentition: evolutionary, developmental, and functional factors. Evolution. 2012;66:1024–43.PubMedGoogle Scholar
  29. 29.
    Kavanagh KD, Evans AR, Jernvall J. Predicting evolutionary patterns of mammalian teeth from development. Nature. 2007;449:427–32.PubMedGoogle Scholar
  30. 30.
    Polly PD. Evolutionary biology: development with a bite. Nature. 2007;449:413–5.PubMedGoogle Scholar
  31. 31.
    Kangas AT, Evans AR, Thesleff I, Jernvall J. Nonindependence of mammalian dental characters. Nature. 2004;432:211–4.PubMedGoogle Scholar
  32. 32.
    Hlusko LJ, Maas ML, Mahaney MC. Statistical genetics of molar cusp patterning in pedigreed baboons: implications for primate dental development and evolution. J Exp Zool B Mol Dev Evol. 2004;302B:268–83.Google Scholar
  33. 33.
    Biknevicius AR. Dental function and diet in the Carpolestidae (Primates, Plesiadapiformes). Am J Phys Anthropol. 1986;71:157–71.PubMedGoogle Scholar
  34. 34.
    Butler PM. The evolution of tooth shape and tooth function in primates. In: Teaford MF, Smith MM, Ferguson MJJ, editors. Development, function, and evolution of teeth. Cambridge: Cambridge University Press; 2000. p. 201–11.Google Scholar
  35. 35.
    Lucas PW, Peters CR. Function of postcanine tooth crown shape in mammals. In: Teaford MF, Smith MM, Ferguson MWJ, editors. Development, function, and evolution of teeth. Cambridge: Cambridge University Press; 2000. p. 282–9.Google Scholar
  36. 36.
    Teaford MF. Primate dental function and morphology revisited. In: Teaford MF, Smith MM, Ferguson WMJ, editors. Development, Function, and Evolution of Teeth. Cambridge: Cambridge University Press; 2000. p. 290–304.Google Scholar
  37. 37.
    Evans AR, Sanson GD. The tooth of perfection: functional and spatial constraints on mammalian tooth shape. Biol J Linn Soc. 2003;78:173–91.Google Scholar
  38. 38.
    Evans AR, Sanson GD. Spatial and functional modeling of carnivore and insectivore molariform teeth. J Morphol. 2006;267:649–62.PubMedGoogle Scholar
  39. 39.
    Simpson GG. Major features of evolution. New York: Columbia University Press; 1953.Google Scholar
  40. 40.
    King SJ, Arrigo-Nelson SJ, Pochron ST, Semprebon GM, Godfrey LR, Wright PC, Jernvall J. Dental senescence in a long-lived primate links infant mortality to rainfall. Proc Nat Acad Sci USA. 2004;102:16579–83.Google Scholar
  41. 41.
    King SJ, Boyer DM, Tecot S, Strait SG, Zohdy S, Blanco MB, Wright PC, Jernvall J. Lemur habitat and dental senescence in Ranomafana National Park, Madagascar. Am J Phys Anthropol. 2012;148:228–37.PubMedGoogle Scholar
  42. 42.
    Ungar PS. Reproductive fitness and tooth wear: milking as much as possible out of dental topographic analysis. Proc Natl Acad Sci USA. 2005;102:16533–4.PubMedCentralPubMedGoogle Scholar
  43. 43.
    Bolton WA. Disharmony in tooth size and its relation to the analysis and treatment of malocclusion. Angle Orthod. 1958;28:113–30.Google Scholar
  44. 44.
    Othman S, Harradine N. Tooth size discrepancies in an orthodontic population. Angle Orthod. 2007;77:668–74.PubMedGoogle Scholar
  45. 45.
    Mills JRE. Occlusion and malocclusion of the teeth in Primates. In: Brothwell DR, editor. Dental Anthropology, vol. 5. Oxford: Pergamon Press; 1963. p. 29–51.Google Scholar
  46. 46.
    Molnar S, Molnar IM. Dental arch shape and tooth wear variability. Am J Phys Anthropol. 1990;82:385–95.PubMedGoogle Scholar
  47. 47.
    Eguchi S, Townsend GC, Richards LC, Hughes T, Kasai K. Genetic contribution to dental arch size variation in Australian twins. Arch Oral Biol. 2004;49:1015–24.PubMedGoogle Scholar
  48. 48.
    Godfrey LR, Samonds KE, Jungers WL, Sutherland MR. Dental development and Primate life histories. In: Kappeler PM, Pereira ME, editors. Primate Life Histories and Socioecology. Chicago: University of Chicago Press; 2003. p. 177–203.Google Scholar
  49. 49.
    Smith BH. Dental development as a measure of life history in primates. Evolution. 1989;43:683–8.Google Scholar
  50. 50.
    Smith BH. Life history and the evolution of human maturation. Evol Anthropol. 1992;1:134–42.Google Scholar
  51. 51.
    Dirks W, Reid DJ, Jolly CJ, Phillips-Conroy JE, Brett FL. Out of the mouths of baboons: stress, life history, and dental development in the Awash National Park hybrid zone, Ethiopia. Am J Phys Anthropol. 2002;118:239–52.PubMedGoogle Scholar
  52. 52.
    Rountrey AN, Fisher DC, Tikhonov AN, Kosintsev PA, Lazarev PA, Boeskorov G, Buigues B. Early tooth development, gestation, and season of birth in mammoths. Quat Int. 2012;255:196–205.Google Scholar
  53. 53.
    Flynn TR, Shanti RM, Levi MH, Adamo AR, Kraut RA, Trieger N. Severe odontogenic infections, Part 1: prospective report. J Oral Maxillo Surg. 2006;64:1093–103.Google Scholar
  54. 54.
    Pavlica Z, Petelin M, Juntes P, Eržen D, Crossley DA, Kalarič U. Periodontal disease burden and pathological changes in organs of dogs. J Vet Dent. 2008;25:97–105.PubMedGoogle Scholar
  55. 55.
    Ungar PS, M’kirera F. A solution to the worn tooth conundrum in primates. Proc Natl Acad Sci USA. 2006;100:3874–7.Google Scholar
  56. 56.
    Polly PD. Paleophylogeography of Sorex araneus: molar shape as a morphological marker for fossil shrews. Mammalia. 2003;68:233–43.Google Scholar
  57. 57.
    Polly PD. Paleophylogeography: the tempo of geographic differentiation in marmots (Marmota). J Mamm. 2003;84:369–84.Google Scholar
  58. 58.
    Polly PD. Phylogeographic differentiation in Sorex araneus: morphology in relation to geography and karyotype. Russ J Theriol. 2007;6:73–84.Google Scholar
  59. 59.
    Caumul R, Polly PD. Phylogenetic and environmental components of morphological variation: skull, mandible and molar shape in marmots (Marmota, Rodentia). Evolution. 2005;59:2460–72.PubMedGoogle Scholar
  60. 60.
    White TA, Searle JB. Mandible asymmetry and genetic diversity in island populations of the common shrew, Sorex araneus. J Evol Biol. 2008;21:636–41.PubMedGoogle Scholar
  61. 61.
    McGuire JL. Geometric morphometrics of vole (Microtus californicus) dentition as a new paleoclimatic proxy: shape change along geographic and climatic clines. Quat Int. 2010;212:198–205.Google Scholar
  62. 62.
    Fortelius M, Eronen JT, Jernvall J, Liu L, Pushkina D, Rinne J, Tesakov A, Vislobokova I, Zhang Z, Zhou L. Fossil mammals resolve regional patterns of Eurasian climate change over 20 million years. Evol Ecol Res. 2002;4:1005–16.Google Scholar
  63. 63.
    Eronen JT, Puolamäki K, Liu L, Lintulaakso K, Damuth J, Janis C, Fortelius M. Precipitation and large herbivorous mammals II: estimates from present-day communities. Evol Ecol Res. 2010;12:217–33.Google Scholar
  64. 64.
    Janis CM, Fortelius M. On the means whereby mammals achieve increased functional durability of their dentitions with special reference to limiting factors. Biol Rev. 1988;63:197–230.PubMedGoogle Scholar
  65. 65.
    Wright S. The evolution of dominance. Am Nat. 1929;63:556–61.Google Scholar
  66. 66.
    Lande R. Natural selection and random genetic drift in phenotypic evolution. Evolution. 1976;30:314–34.Google Scholar
  67. 67.
    Endler JA. Geographic variation, speciation, and clines. Princeton: Princeton University Press; 1977.Google Scholar
  68. 68.
    Searle JB, Wójcik JM. Chromosomal evolution, the case of Sorex araneus. In: Wójcik JM, Wolsan M, editors. Evolution of Shrews. Białowieża: Mammal Research Institute of the Polish Academy of Sciences; 1998. p. 173–218.Google Scholar
  69. 69.
    Polly PD. On the simulation of the evolution of morphological shape: multivariate shape under selection and drift. Palaeontol Electr. 2004;7(7A):1–28.Google Scholar
  70. 70.
    Hausser J. The Sorex of the araneus-arcticus group: do they really speciate? In: Merrit JF, Kirkland GL Jr, Rose RK editors. Advances in the Biology of Shrews. Carn Mus Nat Hist Sp Publ. 1994; 8: 295–306.Google Scholar
  71. 71.
    Polly PD, Polyakov AV, Ilyashenko VB, Onischenko SS, White TA, Bulatova NS, Pavlova S, Borodin PM, Searle JB. Phenotypic variation across chromosomal hybrid zones of the Common shrew (Sorex araneus) indicates reduced gene flow. PLoS One. 2013;8:e67455.PubMedCentralPubMedGoogle Scholar
  72. 72.
    Polly PD. On morphological clocks and paleophylogeography: toward a timescale for Sorex hybrid zones. Genetica. 2001;112–113:339–57.PubMedGoogle Scholar
  73. 73.
    Wójcik AM, Polly PD, Sikorski MD, Wójcik JM. Selection in a cycling population: differential response among skeletal traits. Evolution. 2006;60:1925–35.PubMedGoogle Scholar
  74. 74.
    Poroshin EA, Polly PD, Wójcik JM. Climate and morphological change on decadal scales: multiannual variation in the common shrew Sorex araneus in northeast Russia. Acta Theriol. 2010;55:193–202.Google Scholar
  75. 75.
    Bookstein FL. Random walk and the existence of evolutionary rates. Paleobiology. 1987;13:446–64.Google Scholar
  76. 76.
    Felsenstein J. Phylogenies and quantitative characters. Ann Rev Ecol Syst. 1988;19:445–71.Google Scholar
  77. 77.
    Kimura M. Process leading to quasi-fixation of genes in natural populations due to random fluctuations of selection intensities. Genetics. 1954;39:280–95.PubMedCentralPubMedGoogle Scholar
  78. 78.
    Cavalli-Sforza LL, Edwards AWF. Phylogenetic analysis: models and estimation procedures. Am J Hum Genet. 1967;19:233–57.PubMedCentralPubMedGoogle Scholar
  79. 79.
    Felsenstein J. Inferring Phylogenies. Sunderland: Sinauer Associates; 2003.Google Scholar
  80. 80.
    Polly PD, Le Comber SC, Burland TM. On the occlusal fit of tribosphenic molars: Are we underestimating species diversity in the Mesozoic? J Mamm Evol. 2005;12:285–301.Google Scholar
  81. 81.
    Ungar PS, Grine FE, Teaford MF. Diet in early Homo: a review of the evidence and a new model of adaptive versatility. Ann Rev Anthropol. 2006;35:209–28.Google Scholar
  82. 82.
    Ungar PS, Grine FE, Teaford MF. Dental microwear and diet of the Plio-Pleistocene hominin Paranthropus boisei. PLoS One. 2008;3:e2004.Google Scholar
  83. 83.
    Popowics TE, Fortelius M. On the cutting edge: tooth blade sharpness in herbivorous and faunivorous mammals. Ann Zool Fenn. 1997;34:73–88.Google Scholar
  84. 84.
    Anderson PSL, LaBarbera M. Functional consequences of tooth design: effects of blade shape on energetics of cutting. J Exp Biol. 2008;211:3619–26.PubMedGoogle Scholar
  85. 85.
    Crompton AW, Hiiemae KM. Molar occlusion and mandibular movements during occlusion, Didelphis marsupialis. Zool J Linn Soc. 1970;49:21–47.Google Scholar
  86. 86.
    Kay RF, Hiiemae KM. Jaw movement and tooth use in recent and fossil Primates. J Phys Anthropol. 1974;40:227–56.Google Scholar
  87. 87.
    Wood CB, Conroy GC, Lucas SG. New discoveries of fossil primates from the type Torrejonian (Middle Paleocene) of New Mexico. Folia Primatol. 1979;32:1–7.PubMedGoogle Scholar
  88. 88.
    Wood CB, Clemens WA. A new specimen and a functional reassociation of the molar dentition of Batodon tenuis (Placentalia: Incertae sedis), latest Cretaceous (Lancian), North America. Bull Mus Comp Zool. 2001;156:99–118.Google Scholar
  89. 89.
    Bookstein FL. Morphometric Tools for Landmark Data. Cambridge: Cambridge University Press; 1991. p. 435.Google Scholar
  90. 90.
    Vaughan N. The diets of British bats (Chiroptera). Mamm Rev. 1997;27:77–94.Google Scholar
  91. 91.
    Polly PD. Development, Geography, and Sample Size in P matrix evolution: molar-shape change in island populations of Sorex araneus. Evol Dev. 2005;7:29–41.PubMedGoogle Scholar
  92. 92.
    Weishampel DB, Norman DB. Vertebrate herbivory in the Mesozoic; jaws, plants, and evolutionary metrics. Geol Soc Am Spec Pap. 1989;238:87–100.Google Scholar
  93. 93.
    Rybczynski N, Reisz RR. Earliest evidence for efficient oral processing in a terrestrial herbivore. Nature. 2001;411:684–7.PubMedGoogle Scholar
  94. 94.
    Reisz RR. Origin of dental occlusion in tetrapods: signal for terrestrial vertebrate evolution? J Exp Zool Mol Dev Evol. 2006;306B:177–261.Google Scholar
  95. 95.
    Fröbisch J. On dental occlusion and saber teeth. Science. 2011;331:1525–8.PubMedGoogle Scholar
  96. 96.
    Young MT, Brusatte SL, Beatty BL. Brandalise de Andrade M, Desojo JB. Tooth-on-tooth interlocking occlusion suggests macrophagy in the Mesozoic marine crocodylomorph Dakosaurus. Anat Rec. 2012;295:1147–58.Google Scholar
  97. 97.
    Purnell MA. Microwear on conodont elements and macrophagy in the first vertebrates. Nature. 1995;374:798–800.Google Scholar
  98. 98.
    Donoghue PCJ, Purnell MA. Mammal-like occlusion in conodonts. Paleobiology. 1999;25:58–74.Google Scholar
  99. 99.
    Weishampel DB. Evolution of jaw mechanisms in ornithopod dinosaurs. Adv Anat Embryol Cell Biol. 1984;87:1–109.PubMedGoogle Scholar
  100. 100.
    Rybczynski N, Tiarabasso A, Bloskie P, Cutherbertson R, Holliday C. A three-dimensional animation model of Edmontosaurus (Hadrosauridae) for testing chewing hypotheses. Palaeontol Electr. 2008;11(9A):1–14.Google Scholar
  101. 101.
    Barrett PM. Paleobiology of herbivorous dinosaurs. Ann Rev Earth Plan Sci. 2012;42:207–30.Google Scholar
  102. 102.
    Luo ZX. Transformation and diversification in early mammal evolution. Nature. 2007;450:1011–9.PubMedGoogle Scholar
  103. 103.
    Luo ZX, Ji Q, Yuan CX. Convergent dental adaptations in pseudo-tribosphenic and tribosphenic mammals. Nature. 2007;450:93–7.PubMedGoogle Scholar
  104. 104.
    Kielan-Jaworowska Z, Cifelli RL, Luo ZX. Mammals from the age of dinosaurs: origin, evolution, and structure. New York: Columbia University Press; 2013.Google Scholar
  105. 105.
    Rensberger JM. Occlusion model for mastication and dental wear in herbivorous mammals. J Paleontol. 1973;47:515–28.Google Scholar
  106. 106.
    Fortelius M. Functional aspects of occlusal cheek-tooth morphology in hypsodont, non-ruminant ungulates. In: Martinell J, editor. International Symposium on Concept and Methods in Paleontology; 1981. p. 153–62.Google Scholar
  107. 107.
    Fortelius M. The functional significance of wear-induced change in the occlusal morphology of herbivore cheek teeth, exemplified by Dicerorhinus etruscus upper molars. Acta Zool Fenn. 1985;170:157–8.Google Scholar
  108. 108.
    Ungar PS, Williamson M. Exploring the effects of tooth wear on functional morphology: a preliminary study using dental topographic analysis. Palaeontol Electr. 2000;3(1A):1–18.Google Scholar
  109. 109.
    Mellet JS. Carnassial rotation in a fossil carnivore. Am Mid Nat. 1969;82:287–9.Google Scholar
  110. 110.
    Asher RJ, Sánchez-Villagra MR. Locking yourself out: diversity among dentally zalambdodont theiran mammals. J Mamm Evol. 2005;12:26–282.Google Scholar
  111. 111.
    Hunter JP, Jernvall J. The hypocone as a key innovation in mammalian evolution. Proc Nat Acad Sci USA. 1995;92:10718–22.PubMedCentralPubMedGoogle Scholar
  112. 112.
    Smith NE, Strait SG. PaleoView3D: from specimen to online digital model. Palaeontol Electr. 2004;11(11A):1–17.Google Scholar
  113. 113.
    Jones D, Evans AR, Siu K, Rayfield EJ, Donoghue PCJ. The sharpest tools in the box? Quantitative analysis of conodont element functional morphology. Proc R Soc B. 2012;279:2849–54.PubMedCentralPubMedGoogle Scholar
  114. 114.
    Kullmer O, Banazzi S, Fiorenza L, Schulz D, Bacso S, Winzen O. Technical note: occlusal fingerprint analysis: quantification of tooth wear pattern. Am J Phys Anthropol. 2009;139:600–5.PubMedGoogle Scholar
  115. 115.
    Kullmer O, Benazzi S, Schulz D, Gunz P, Kordos L, Begun DR. Dental arch restoration using tooth macrowear patterns with application to Rudapithecus hungaricus from the Late Miocene of Rudabánya, Hungary. Hung J Hum Evol. 2013;64:151–60.Google Scholar
  116. 116.
    Schultz JA, Martin T. Function of the pretribosphenic and tribosphenic mammalian molars inferred from 3D animation. Naturwiss. 2014;101:771–81.PubMedGoogle Scholar
  117. 117.
    Benazzi S, Kullmer O, Grosse IR, Weber GW. Using occlusal wear information and finite element analysis to investigate stress distributions in human molars. J Anat. 2011;219:259–72.PubMedCentralPubMedGoogle Scholar
  118. 118.
    Gómez-Robles A, Martinón-Torres M, Bermúdez de Castro JM, Margvelashvili A, Bastir M, Arsuaga JL, Pérez-Pérez A, Estebaranz F, Martinez LM. A geometric morphometric analysis of hominin upper first molar shape. J Hum Evol. 2007;53:272–85.PubMedGoogle Scholar
  119. 119.
    Gómez-Robles A, Bermúdez de Castro JM, Arsuaga JL, Carbonell E, Polly PD. No known hominin species matches the expected dental morphology of the last common ancestor of Neanderthals and modern humans. Proc Natl Acad Sci USA. 2013;110:18196–201.PubMedCentralPubMedGoogle Scholar
  120. 120.
    Grossnickle DM, Polly PD. Mammal disparity decreases during the Cretaceous angiosperm radiation. Proc R Soc B. 2013;280:20132110.PubMedCentralPubMedGoogle Scholar
  121. 121.
    Wilson GP. Mammals across the K/Pg boundary in northeastern Montana, USA: dental morphology and body-size patterns reveal extinction selectivity and immigrant-fueled ecospace filling. Paleobiology. 2013;39:429–69.Google Scholar
  122. 122.
    Evans AR, Wilson GP, Fortelius M, Jernvall J. High-level similarity of dentitions in carnivorans and rodents. Nature. 2007;445:78–81.PubMedGoogle Scholar
  123. 123.
    Smits PD, Evans AR. Functional constraints on tooth morphology in carnivorous mammals. BMC Evol Biol. 2012;12:146.PubMedCentralPubMedGoogle Scholar
  124. 124.
    Boyer DM. Relief index of second mandibular molars is a correlate of diet among prosimian primates and other euarchontan mammals. J Hum Evol. 2008;55:1118–37.PubMedGoogle Scholar
  125. 125.
    Boyer DM, Evans AR, Jernvall J. Evidence of dietary differentiation among Late Paleoeocene-Early Eocene plesiadapids (Mammalia, Primates). Am J Phys Anthropol. 2010;142:194–210.PubMedGoogle Scholar
  126. 126.
    Santana SE, Strait S, Dumont ER. The better to eat you with: functional correlates of tooth structure in bats. Funct Ecol. 2011;25:839–47.Google Scholar
  127. 127.
    Wilson GP, Evans AR, Corfe IJ, Smits PD, Fortelius M, Jernvall J. Adaptive radiation of multituberculate mammals before the extinction of dinosaurs. Nature. 2012;483:457–60.PubMedGoogle Scholar
  128. 128.
    Weiss KW, Stock DW, Zhao Z. Dynamic interactions and the evolutionary genetics of dental patterning. Crit Rev Oral Biol Med. 1998;9:369–98.PubMedGoogle Scholar
  129. 129.
    Polly PD. Developmental dynamics and G-matrices: Can morphometric spaces be used to model evolution and development? Evol Biol. 2008;35:83–96.Google Scholar
  130. 130.
    Salazar-Ciudad I, Jernvall J. The causality horizon and developmental bases of morphological evolution. Biol Theory. 2013;8:286–92.Google Scholar

Copyright information

© The Society of The Nippon Dental University 2015

Authors and Affiliations

  1. 1.Department of Geological SciencesIndiana UniversityBloomingtonUSA
  2. 2.Department of BiologyIndiana UniversityBloomingtonUSA
  3. 3.Department of AnthropologyIndiana UniversityBloomingtonUSA

Personalised recommendations