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

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.

The earliest Asian bats (Mammalia: Chiroptera) address major gaps in bat evolution

Bats dispersed widely after evolving the capacity for powered flight, and fossil bats are known from the early Eocene of most continents. Until now, however, bats have been conspicuously absent from the early Eocene of mainland Asia. Here, we report two teeth from the Junggar Basin of northern Xinjiang, China belonging to the first known early Eocene bats from Asia, representing arguably the most plesiomorphic bat molars currently recognized. These teeth combine certain bat synapomorphies with primitive traits found in other placental mammals, thereby potentially illuminating dental evolution among stem bats. The Junggar Basin teeth suggest that the dentition of the stem chiropteran family Onychonycteridae is surprisingly derived, although their postcranial anatomy is more primitive than that of any other Eocene bats. Additional comparisons with stem bat families Icaronycteridae and Archaeonycteridae fail to identify unambiguous synapomorphies for the latter taxa, raising the possibility that neither is monophyletic as currently recognized. The presence of highly plesiomorphic bats in the early Eocene of central Asia suggests that this region was an important locus for the earliest, transitional phases of bat evolution, as has been demonstrated for other placental mammal orders including Lagomorpha and Rodentia.

Shape disparity in the blade-like premolars of multituberculate mammals: functional constraints and the evolution of herbivory

Cimolodontan multituberculates were a diverse and long-lived group of mammals characterized by large, blade-like lower fourth premolars (p4). Blade-like (plagiaulacoid) dentitions have evolved numerous times in distantly related mammalian lineages. Here we investigate how p4-shape disparity changed through time in the Cimolodonta. We address two hypotheses: (H1) blade-like dentitions constrain the ability of plagiaulacoid mammals to evolve novel dental morphologies, (H2) cimolodontan dental evolution proceeded gradually along a morphocline during the Late Cretaceous. We quantify functionally important aspects of p4 shape, including ratios reflecting height (H:L), symmetry (L1:L), and mesial-face height (H1:H), in a large sample of cimolodontans spanning the mid-Cretaceous through early Paleogene of North America (ca. 100–35 Mya). Our results do not support the morphocline hypothesis (H2) and, instead, show that cimolodontans evolved a wide range of p4 shapes by the mid-Cretaceous, and that p4-shape disparity remained stable through the Late Cretaceous. We hypothesize that the two-stage cimolodontan chewing cycle (slicing-crushing then grinding) imposed functional constraints on p4 morphology. After the Cretaceous-Paleogene boundary, p4-shape disparity increased sharply, driven by the appearance of the Taeniolabidoidea, Microcosmodontidae, and Eucosmodontidae, in the early Paleocene. We contend that the slicing-crushing functions of the p4 became less important in those taxa, relaxing functional constraints on p4 morphology. Cimolodontans that retained both the slicing-crushing and grinding function of the p4 had a more limited range of p4 morphologies, and probably were largely restricted to animal-dominated omnivory. Taxa that shifted the initial slicing-crushing function from the p4 to the incisors had fewer functional constraints on p4 morphology, and were able to increase their molar grinding capacity to exploit plant-dominated omnivory and herbivory. That the p4 was reduced in herbivorous taxa rather than modified into a broader, multi-cusped tooth lends support to the morphological constraint hypothesis (H1), and this relationship between p4 morphology and function suggests that retaining a large, blade-like p4 might have limited the range of herbivorous diets cimolodontans could exploit. These findings highlight the ecological and evolutionary limitations that specialized dentitions can impose on mammals by restricting their morphological and, in turn, functional diversification.

Tooth replacement in early sarcopterygians

Teeth were an important innovation in vertebrate evolution but basic aspects of early dental evolution remain poorly understood. Teeth differ from other odontode organs, like scales, in their organized, sequential pattern of replacement. However, tooth replacement patterns also vary between the major groups of jawed vertebrates. Although tooth replacement in stem-osteichthyans and extant species has been intensively studied it has been difficult to resolve scenarios for the evolution of osteichthyan tooth replacement because of a dearth of evidence from living and fossil sarcopterygian fishes. Here we provide new anatomical data informing patterns of tooth replacement in the Devonian sarcopterygian fishes Onychodu s, Eusthenopteron and Tiktaalik and the living coelacanth Latimeria based on microfocus- and synchrotron radiation-based X-ray microtomography. Early sarcopterygians generated replacement teeth on the jaw surface in a pattern similar to stem-osteichthyans, with damaged teeth resorbed and replacement teeth developed on the surface of the bone. However, resorption grades and development of replacement teeth vary spatially and temporally within the jaw. Particularly in Onychodus , where teeth were also shed through anterior rotation and resorption of bone at the base of the parasymphyseal tooth whorl, with new teeth added posteriorly. As tooth whorls are also present in more stem-osteichthyans, and statodont tooth whorls are present among acanthodians (putative stem-chondrichthyans), rotational replacement of the anterior dentition may be a stem-osteichthyan character. Our results suggest a more complex evolutionary history of tooth replacement.

Emergence of hystricognathous rodents: Palaeogene fossil record, phylogeny, dental evolution and historical biogeography

Although phylogenetic trees imply Asia as the ancestral homeland of the Hystricognathi clade (Rodentia: Ctenohystrica), curiously the oldest known fossil occurrences of hystricognathous rodents are not from Asia, but from Africa and South America, where they appear suddenly in the fossil record of both landmasses by the Late Middle Eocene. Here we performed cladistic and Bayesian (standard and tip-dating analyses) assessments of the dental evidence documenting early ctenohystricans, including several Asian ‘ctenodactyloids’, virtually all Palaeogene Asian and African hystricognaths known thus far and two representatives of the earliest known South American hystricognaths. Our results provide a phylogenetic context of early hystricognaths (with implications on systematics) and suggest that some Eocene Asian ‘ctenodactyloids’ could be considered as stem hystricognaths and pre-hystricognaths, although they were not recognized as such originally. However, this view does not fill the gap of the Eocene Asian hystricognath record, as the proposed results imply many ghost lineages extending back to the Middle Eocene for several Asian and African taxa. They also imply a complex early historical biogeography of the group, involving multiple dispersal events from Asia to Africa (and possibly from Africa back to Asia) and then to South America sometime during the Middle Eocene. Based on these phylogenetic considerations, we discuss the emergence of hystricognathous rodents from a morpho-anatomical perspective by analysing the differentiation of their masticatory apparatus and chewing movements, notably through the evolution of their dental patterns.