Gene networks, occlusal clocks, and functional patches: new understanding of pattern and process in the evolution of the dentition
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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.
KeywordsOcclusion Tribosphenic teeth Evolution Developmental networks
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 . 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) , 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 ; 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 . 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 . 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 . 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 . 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 . 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 .
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?
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 .
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 . In that study, occlusal fit was measured with geometric morphometrics  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 . 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 .
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 , which combined with carnassial rotation in which the tooth’s orientation changes as the occlusal surfaces on the blades wear  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 .
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 .
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 . 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  and cross-field effects of genes like Eda can induce parallel changes in the morphology of many teeth . 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 . 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 .
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.
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