Bat teeth illuminate the diversification of mammalian tooth classes

Abstract

Tooth classes are an innovation that has contributed to the evolutionary success of mammals. However, our understanding of the mechanisms by which tooth classes diversified remain limited. We use the evolutionary radiation of noctilionoid bats to show how the tooth developmental program evolved during the adaptation to new diet types. Combining morphological, developmental and mathematical modeling approaches, we demonstrate that tooth classes develop through independent developmental cascades that deviate from classical models. We show that the diversification of tooth number and size is driven by jaw growth rate modulation, explaining the rapid gain/loss of teeth in this clade. Finally, we mathematically model the successive appearance of tooth buds, supporting the hypothesis that growth acts as a key driver of the evolution of tooth number and size. Our work reveal how growth, by tinkering with reaction/diffusion processes, drives the diversification of tooth classes and other repeated structure during adaptive radiations.

Periodic pattern formation during embryonic development

“…It is only over the last couple of decades that it has been possible to experimentally test whether Turing RD systems can produce embryonic periodic patterns. Turing RD systems have now been implicated in the formation of a diverse array of embryonic periodic patterns including the digits of the limb [ 3 , 17 ], hair follicles [ 4–6 ], intestinal villi [ 11 ], and palatal rugae [ 18 ], as well as playing a role in tooth morphogenesis [ 19 ], the left–right patterning of the embryo [ 20 , 21 ], and lung branching [ 22 ].…”

“…Both RD-like systems [ 19 , 66–68 ] and MC models [ 69 , 70 ] have been reported to explain various aspects of tooth morphogenesis during embryogenesis. For instance, a RD system with WNT, SHH, and the WNT/BMP inhibitor Sostdc1 serving as the activator, mediator, and inhibitor, respectively, is capable of generating the spacing of mammalian teeth [ 67 ].…”

“…Turing-like RD systems involving EDAR signalling can also explain how differences in tooth morphology between animals [ 68 , 71 ], particularly molar cusp shape and number, have evolved. More recently, it was also suggested that the differential jaw growth between closely related species of bats directly perturbs the underlying Turing mechanism leading to modulation of the size and spacing of teeth, which likely has enabled these animals to adapt to different dietary requirements [ 19 ].…”

Comparative transcriptomics in serial organs uncovers early and pan-organ developmental changes associated with organ-specific evolutionary novelty

“…Theoretical studies propose that the patterning of teeth and cusps are determined dynamically at two levels: the parameters of a Turing system (activator, inhibitor and their interaction) and the field size (control of growth and/or competence) (Morita et al, 2022;Sadier et al, 2019;Salazar-Ciudad, 2008). In tooth and other systems, many examples of evolutionary changes targeting one (Harjunmaa et al, 2014;Salazar-Ciudad & Jernvall, 2010;Thiery et al, 2022) or the other (Bailleul et al, 2019;Pantalacci et al, 2008;Sadier et al, 2023) have been suggested. Here we propose that the mouse upper molar innovation relied on three complementary developmental changes at these two levels (Figure 6B).…”