Late Cenozoic Evolution of the Macropodoid Dentition

Author: Aidan Couzens

Couzens, Aidan, 2017 Late Cenozoic Evolution of the Macropodoid Dentition, Flinders University, School of Biological Sciences

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Dietary adaptation has played an important role in the 200 million year diversification of mammals. Changes in the dentition are a critical component of dietary adaptation because teeth influence how efficiently food can be processed. Because mammals have only limited capacity to replace damaged teeth, the ability to build a durable dentition is an important influence on an individual’s evolutionary fitness. Herbivores are under especially strong pressure to maintain dental function, because the tougher and more abrasive plant foods they consume require extended dental processing compared with animal protein. Grasses and shrubs growing in open habitats are especially difficult and costly to consume because high concentrations of siliceous plant-cell inclusions (phytoliths) and adhering dust and soil make them highly abrasive. The resultant deterioration of tooth function arising from dental wear can significantly impact an individual’s fitness. Open habitats, where herbivores are subject to elevated levels of dental wear, became common during the late Cenozoic as decreasing atmospheric CO2 concentrations and lower global temperatures prompted the spread of grasses and shrubs. Expansion of these habitats was associated with the diversification of herbivore groups like artiodactyl ungulates, horses, and kangaroos. To deal with higher levels of dental wear many herbivore groups increased dental durability by increasing the size of the tooth crown, continuously replacing chewing teeth , increasing tooth area, increasing enamel thickness, or altering enamel microstructure.

The most diverse marsupial herbivores are the macropodoids (kangaroos and relatives) which are often considered ecological analogues of artiodactyls because they acquired parallel adaptations for grazing and locomotion in open habitats. From at least the late Miocene macropodoids evolved within progressively drier and more open terrestrial ecosystems dominated by shrubs and grasses. During the Miocene–Pliocene transition, macropodine and sthenurine kangaroos diversified to become Australia’s dominant terrestrial herbivores. However, unlike ungulate herbivores, macropodoids never evolved very high-crowned prismatic molars, suggesting that they must have acquired a different set of adaptations to increase dental durability. Thus far no systematic attempt has been made to examine what types of dental adaptations these may have been.

In this study I examine how macropodoids responded to dietary change over the past 25 million years. I show that across extant macropodoids molar crown height variation is positively correlated with increased level of dietary abrasion but not habitat openness. The pattern of fossil and reconstructed molar crown height shows an asymmetric increase in disparity, consistent with either a bounded diffusion model, or a multiple trait optimum model. A phylogenetic comparative analysis reveals that the best-fitting models of crown height evolution are adaptive. A four-peak Ornstein–Uhlenbeck model is favoured over simpler models with fewer optima. Initial increases in molar crown-height during the early Neogene are linked with the evolution of bilophodont molars that were better able to process tough foods like dicot leaves than lower-crowned cusps. Molar crown-height disparity more than doubled across the Miocene–Pliocene transition, primarily in response to the expansion of macropodine kangaroos into grass-dominated Pliocene ecosystems.

However, the increase in molar crown-height amongst Pliocene macropodids remained significantly below levels attained by contemporaneous artiodactyl ungulates and equids. Using high-resolution micro-computed tomography, I tested whether variation in molar enamel thickness allowed macropodoids to diversify despite their low-crowned dentitions. Computation of three-dimensional relative enamel thickness scores reveals that there is an approximately three-fold range of enamel thickness amongst macropodoids. The macropodine genera Macropus, Petrogale and Wallabia are characterised by possessing amongst the thickest molar enamel of any mammal yet examined; comparable to primates with ‘hyper-thick’ enamel like Australopithecus, Paranthropus and Homo. In contrast, the relative molar enamel thickness of the giant sthenurine kangaroos is extremely thin, comparable to hominoids like Gorilla which consume large quantities of leaves. Spatial mapping of enamel thickness and linear measurements from seven molar regions suggest that, structurally, bilophodont molars are differentiated from bunodont molars by thick enamel between the buccal and lingual cusps. Linear enamel thickness measurements suggest that Pliocene macropodines co-opted this pattern to build bladed dentitions with thicker molar enamel, better able to resist high levels of wear. Increases in enamel thickness along the blade edge and relief surface are likely adaptive because they help maintain a trenchant lophid, and offset dentine exposure. These results provide strong evidence that thick molar enamel is an adaptive response to high rates of dental wear.

The capacity of dental traits to vary through time is an important determinant of rates and directions of adaptive change. Some functionally and phylogenetically important macropodoid traits show evidence for reevolution after long intervals of absence, but the reasons for this have been unclear. One such trait is the posthypocristid, a longitudinal molar crest bounding a crushing basin on the rear face of basal macropodoid lower molars. Based on a reassessment of the homology of talonid features, and an ancestral state reconstruction analysis, I show that the posthypocristid reevolved separately in the Sthenurinae and Macropodinae, each after more than 15 million years of absence. I examined whether high levels of reversibility in the posthypocristid and other talonid traits were linked to developmental processes regulating tooth proportionality and cusp number. Based on an activation–inhibition model of tooth development, I show that the same statistically significant deviation from the inhibitory cascade leads to posthypocristid reversal in both Sthenurinae and Macropodinae. Based on morphological similarities to mouse dental phenotypes, increased responsiveness of the molar talonid to ectodysplasin dosage may have been an important enabler of posthypocristid reversibility. These results bolster the view that reversals are possible after long periods of absence and show how developmental factors promote homoplasy.

Overall this work shows how major changes in macropodoid dental evolution during the past 25 million years were influenced by both environmental change and developmental factors. In the future, simulations of dental evolution within developmental morphospace will potentially improve our understanding of how natural selection, drift, and constraints, shape transitions between adaptive zones. Significant questions remain about how enamel thickness functions and how its variation at population and macroevolutionary scales is influenced by genetic–developmental processes. The expanded virtual analysis of dental morphology holds great promise for improving our understanding of adaptation and will play an important role in attempts to build a quantitative genotype–phenotype map.

Keywords: Marsupial, adaptation, Neogene, environmental change, kangaroo, teeth, reversal

Subject: Biological Sciences thesis

Thesis type: Doctor of Philosophy
Completed: 2017
School: School of Biological Sciences
Supervisor: Gavin Prideaux