Developmental influence on evolutionary rates and the origin of placental mammal tooth complexity

Abstract

Development has often been viewed as a constraining force on morphological adaptation, but its precise influence, especially on evolutionary rates, is poorly understood. Placental mammals provide a classic example of adaptive radiation, but the debate around rate and drivers of early placental evolution remains contentious. A hallmark of early dental evolution in many placental lineages was a transition from a triangular upper molar to a more complex upper molar with a rectangular cusp pattern better specialized for crushing. To examine how development influenced this transition, we simulated dental evolution on “landscapes” built from different parameters of a computational model of tooth morphogenesis. Among the parameters examined, we find that increases in the number of enamel knots, the developmental precursors of the tooth cusps, were primarily influenced by increased self-regulation of the molecular activator (activation), whereas the pattern of knots resulted from changes in both activation and biases in tooth bud growth. In simulations, increased activation facilitated accelerated evolutionary increases in knot number, creating a lateral knot arrangement that evolved at least ten times on placental upper molars. Relatively small increases in activation, superimposed on an ancestral tritubercular molar growth pattern, could recreate key changes leading to a rectangular upper molar cusp pattern. Tinkering with tooth bud geometry varied the way cusps initiated along the posterolingual molar margin, suggesting that small spatial variations in ancestral molar growth may have influenced how placental lineages acquired a hypocone cusp. We suggest that development could have enabled relatively fast higher-level divergence of the placental molar dentition.

Symmetry and Aesthetics in Dentistry

“…A triconodontic tooth scheme, therefore, shows bilateral symmetry to a frontal plane and to a sagittal plane. The three main cusps were rearranged from a line to a triangle in tritubercular molars [58]. With more complex tribosphenic teeth, simple schemes of bilateral symmetry were abandoned, mainly by the evolution of an additional main cusp, the hypocone [59].…”

Stripe and spot selection in cusp patterning of mammalian molar formation

“…The acquisition of the hypocone has evolved more than 20 times convergently among various lineages even though there are several options for adding one cusp during odonotogenesis 27 . In terms of mode doubling, the subsequent cusp appears in mode tripling under the stripe pattern cusp formation, which suggests that the hypocone would not necessarily be derived from a certain cusp or structure, but it was acquired independently in the various species in a various approach 15 , 27 , 49 – 52 . Our hypothesis of switching from spot to stripe in cusp patterning is consistent with an increase in lophedness and the adaptive radiation of mammals with hypocones during the Cenozoic era.…”

Evolvability and Macroevolution: Overview and Synthesis

“…Many aspects of body plans do seem highly resistant to change-hence the anisotropic variation that typifies developmental bias-but the geometry of regulatory pathways and their recursive circuits may be too complex for simple generalizations on evolvability (Deline et al, 2020;Erwin, 2021a: p. 7). As with phenotypic modules, modular organization of developmental processes may help to circumvent burden on specific traits, with the more evolvable ones being those whose regulatory factors are structured such that small developmental changes produce significant shifts in form, as Jernvall (2000) suggested for size and number of cusps in mammalian teeth (see also Burroughs, 2019;Couzens et al, 2021).…”