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Testing the inhibitory cascade model in Mesozoic and Cenozoic mammaliaforms - PubMed

  • ️Tue Jan 01 2013

Testing the inhibitory cascade model in Mesozoic and Cenozoic mammaliaforms

Thomas J D Halliday et al. BMC Evol Biol. 2013.

Abstract

Background: Much of the current research in the growing field of evolutionary development concerns relating developmental pathways to large-scale patterns of morphological evolution, with developmental constraints on variation, and hence diversity, a field of particular interest. Tooth morphology offers an excellent model system for such 'evo-devo' studies, because teeth are well preserved in the fossil record, and are commonly used in phylogenetic analyses and as ecological proxies. Moreover, tooth development is relatively well studied, and has provided several testable hypotheses of developmental influences on macroevolutionary patterns. The recently-described Inhibitory Cascade (IC) Model provides just such a hypothesis for mammalian lower molar evolution. Derived from experimental data, the IC Model suggests that a balance between mesenchymal activators and molar-derived inhibitors determines the size of the immediately posterior molar, predicting firstly that molars either decrease in size along the tooth row, or increase in size, or are all of equal size, and secondly that the second lower molar should occupy one third of lower molar area. Here, we tested the IC Model in a large selection of taxa from diverse extant and fossil mammalian groups, ranging from the Middle Jurassic (~176 to 161 Ma) to the Recent.

Results: Results show that most taxa (~65%) fell within the predicted areas of the Inhibitory Cascade Model. However, members of several extinct groups fell into the regions where m2 was largest, or rarely, smallest, including the majority of the polyphyletic "condylarths". Most Mesozoic mammals fell near the centre of the space with equality of size in all three molars. The distribution of taxa was significantly clustered by diet and by phylogenetic group.

Conclusions: Overall, the IC Model was supported as a plesiomorphic developmental system for Mammalia, suggesting that mammal tooth size has been subjected to this developmental constraint at least since the divergence of australosphenidans and boreosphenidans approximately 180 Ma. Although exceptions exist, including many 'condylarths', these are most likely to be secondarily derived states, rather than alternative ancestral developmental models for Mammalia.

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Figures

Figure 1
Figure 1

High level phylogeny of mammals, including all groups used in this study. Dotted lines represent possible affinities or where groups may be polyphyletic. Italicised taxonomic names are extinct groups, some of which are likely polyphyletic. Tree topology modified from Asher and Helgen [48], with extinct group placement based on various recent analyses or compilations [18,21-23,27,29,30,40,41]. This tree is intended to be illustrative of the diversity of groups covered in this analysis, and is not derived from any single phylogenetic analysis.

Figure 2
Figure 2

Lower molar area ratios plotted for 132 mammalian genera, with regression line. The black line represents the IC Model as predicted by Kavanagh et al. [8], with the white areas representing the predicted possible areas under the strict IC Model. Grey regions are outside the predicted areas of the model, and represent regions of the graph where m2 is either the largest lower molar (bottom-right) or the smallest (top-left). 65.2% of sampled taxa fall within the predicted area. The thin red line is the reduced major axis regression line, with 95% confidence bands in blue on either side.

Figure 3
Figure 3

Minimum area polygons for the ten taxonomic groupings. Only groups with more than five genera were included in this analysis. Carnivora and Creodonta have been grouped together as possibly closely-related carnivorous placentals; Primates and Plesiadapiformes are also grouped together. Non-parametric MANOVA results in a highly significant clustering by taxonomic group (p<0.001), even when removing the most extreme members of Artiodactyla. The only group to overlap with the range of the carnivorous placental grouping is Cimolesta. “Condylarths” and Acreodi are clustered together in an area distinct from that occupied by Artiodactyla and Perissodactyla, with only three “condylarths” overlapping in range with the extant ungulate groups, showing that “archaic” and extant ungulates possess clearly distinct tooth morphologies.

Figure 4
Figure 4

Morphospace positions for Mesozoic mammals and the extant and “archaic” ungulates. Mesozoic mammals (coloured in blue) are found near the centre (1,1) of the morphospace, closer to the plesiomorphic conditions of equal-sized molars. “Condylarths”, coloured black, are found mostly in the region of the morphospace where m2 is the largest molar, and are separate from Artiodactyla (dark green) and Perissodactyla (light green), with the exceptions of Hyopsodus, Anisonchus and Lambertocyon, all of which possess molars that increase in size posteriorly. Artiodactyla show the most extreme increase in molar size, with Uintacyon, Elomeryx and Merycoidodon exhibiting six-fold or more increases in molar area from m1 to m3.

Figure 5
Figure 5

Minimum area polygons for 132 genera divided into six dietary types. The data show a similarity to the predicted distribution from Kavanagh et al.[8], with more faunivorous dietary types placed in the bottom left of the morphospace, and more herbivorous dietary types in the top right.

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