Gene expression supports a single origin of horns and antlers in hoofed mammals.

Horns, antlers, and other bony cranial appendages of even-toed hoofed mammals (ruminant artiodactyls) challenge traditional morphological homology assessments. Cranial appendages all share a permanent bone portion with family-specific integument coverings, but homology determination depends on whether the integument covering is an essential component or a secondary elaboration of each structure. To enhance morphological homology assessments, we tested whether juvenile cattle horn bud transcriptomes share homologous gene expression patterns with deer antlers relative to pig outgroup tissues, treating the integument covering as a secondary elaboration. We uncovered differentially expressed genes that support horn and antler homology, potentially distinguish them from non-cranial-appendage bone and other tissues, and highlight the importance of phylogenetic outgroups in homology assessments. Furthermore, we found differentially expressed genes that could support a shared cranial neural crest origin for horns and antlers and expression patterns that refine our understanding of the timing of horn and antler differentiation.

Vole genomics links determinate and indeterminate growth of teeth.

Continuously growing teeth are an important innovation in mammalian evolution, yet genetic regulation of continuous growth by stem cells remains incompletely understood. Dental stem cells responsible for tooth crown growth are lost at the onset of tooth root formation. Genetic signaling that initiates this loss is difficult to study with the ever-growing incisor and rooted molars of mice, the most common mammalian dental model species, because signals for root formation overlap with signals that pattern tooth size and shape (i.e., cusp patterns). Different species of voles (Cricetidae, Rodentia, Glires) have evolved rooted and unrooted molars that have similar size and shape, providing alternative models for studying roots. We assembled a de novo genome of Myodes glareolus, a vole with high-crowned, rooted molars, and performed genomic and transcriptomic analyses in a broad phylogenetic context of Glires (rodents and lagomorphs) to assess differential selection and evolution in tooth forming genes. We identified 15 dental genes with changing synteny relationships and six dental genes undergoing positive selection across Glires, two of which were undergoing positive selection in species with unrooted molars, Dspp and Aqp1. Decreased expression of both genes in prairie voles with unrooted molars compared to bank voles supports the presence of positive selection and may underlie differences in root formation. Bulk transcriptomics analyses of embryonic molar development in bank voles also demonstrated conserved patterns of dental gene expression compared to mice, with species-specific variation likely related to developmental timing and morphological differences between mouse and vole molars. Our results support ongoing evolution of dental genes across Glires, revealing the complex evolutionary background of convergent evolution for ever-growing molars.

Tissue Mechanical Forces and Evolutionary Developmental Changes Act Through Space and Time to Shape Tooth Morphology and Function.

Efforts from diverse disciplines, including evolutionary studies and biomechanical experiments, have yielded new insights into the genetic, signaling, and mechanical control of tooth formation and functions. Evidence from fossils and non-model organisms has revealed that a common set of genes underlie tooth-forming potential of epithelia, and changes in signaling environments subsequently result in specialized dentitions, maintenance of dental stem cells, and other phenotypic adaptations. In addition to chemical signaling, tissue forces generated through epithelial contraction, differential growth, and skeletal constraints act in parallel to shape the tooth throughout development. Here recent advances in understanding dental development from these studies are reviewed and important gaps that can be filled through continued application of evolutionary and biomechanical approaches are discussed.

Shape disparity of bovid (Mammalia, Artiodactyla) horn sheaths and horn cores allows discrimination by species in 3D geometric morphometric analyses.

The bony cranial structures of even-toed hoofed mammals are important for understanding ecology and behavior of ruminants. Horns, the cranial appendages of the family Bovidae, are covered in a layer of keratin that is often not preserved in the fossil record; however, this keratin sheath is intimately involved in the processes that influence horn shape evolution. To understand the relationship between these two components of horns, we quantified both core and sheath shape for four extant species using three-dimensional geometric morphometric analyses in separate, core- and sheath-specific morphospaces as well as a combined morphospace. We assessed correlations between the horn and sheath morphospaces using two-block partial least squares regression, a Mantel test of pairwise distances between species, and Procrustes ANOVA. We measured disparity in the combined morphospace as Procrustes distances between mean shapes of cores and sheaths within and between species and as Procrustes variance. We also tested whether core and sheath shapes could be discriminated by taxon with a canonical variate analysis. Results show that horn core and sheath morphospaces are strongly correlated. The differences in shape between a species' core and sheath were statistically significant, but not as great as those between the cores and sheaths of different species when close relatives were not considered, and core and sheath Procrustes variances are not significantly different within species. Cores and sheath shapes were highly identifiable and were assigned to the correct clade 93% of the time in the canonical variate analysis. Based on these tests, horn cores are distinguishable in geometric morphometric analyses, extending the possibility of using geometric morphometrics to study the ecology and evolution of bovid horns to the fossil record.

Sexual maturity and shape development in cranial appendages of extant ruminants.

Morphological disparity arises through changes in the ontogeny of structures; however, a major challenge of studying the effect of development on shape is the difficulty of collecting time series of data for large numbers of taxa. A proxy for developmental series proposed here is the age at sexual maturity, a developmental milestone potentially tied to the development of structures with documented use in intrasexual competition, such as cranial appendages in Artiodactyla. This study tested the hypothesis that ruminant cranial appendage shape and size correlate with onset of sexual maturity, predicting that late sexual maturity would correlate with larger, more complicated cranial appendages. Published data for cranial appendage shape and size in extant taxa were tested for correlations with sexual maturity using linear mixed-effect models and phylogenetic generalized least-squares analyses. Ancestral state reconstructions were used to assess correlated variables for developmental shifts indicative of heterochrony. These tests showed that phylogeny and body mass were the most common predictors of cranial appendage shape and sexual maturity was only significant as an interaction with body mass. Nevertheless, using developmental milestones as proxies for ontogeny may still be valuable in targeting future research to better understand the role of development in the evolution of disparate morphology when correlations exist between the milestone and shape.