Time to synchronize our clocks: Connecting developmental mechanisms and evolutionary consequences of heterochrony.

Heterochrony, defined as a change in the timing of developmental events altering the course of evolution, was first recognized by Ernst Haeckel in 1866. Haeckel's original definition was meant to explain the observed parallels between ontogeny and phylogeny, but the interpretation of his work became a source of controversy over time. Heterochrony took its modern meaning following the now classical work in the 1970-80s by Steven J. Gould, Pere Alberch, and co-workers. Predicted and described heterochronic scenarios emphasize the many ways in which developmental changes can influence evolution. However, while important examples of heterochrony detected with comparative morphological methods have multiplied, the more mechanistic understanding of this phenomenon lagged conspicuously behind. Considering the rapid progress in imaging and molecular tools available now for developmental biologists, this review aims to stress the need to take heterochrony research to the next level. It is time to synchronize the different levels of heterochrony research into a single analysis flow: from studies on organismal-level morphology to cells to molecules and genes, using complementary techniques. To illustrate how to achieve a more comprehensive understanding of phyletic morphological diversification associated with heterochrony, we discuss several recent case studies at various phylogenetic scales that combine morphological, cellular, and molecular analyses. Such a synergistic approach offers to more fully integrate phylogenetic and ontogenetic dimensions of the fascinating evolutionary phenomenon of heterochrony.

Peramorphosis, an evolutionary developmental mechanism in neotropical bat skull diversity.

BACKGROUND: The neotropical leaf-nosed bats (Chiroptera, Phyllostomidae) are an ecologically diverse group of mammals with distinctive morphological adaptations associated with specialized modes of feeding. The dramatic skull shape changes between related species result from changes in the craniofacial development process, which brings into focus the nature of the underlying evolutionary developmental processes. RESULTS: In this study, we use three-dimensional geometric morphometrics to describe, quantify, and compare morphological modifications unfolding during evolution and development of phyllostomid bats. We examine how changes in development of the cranium may contribute to the evolution of the bat craniofacial skeleton. Comparisons of ontogenetic trajectories to evolutionary trajectories reveal two separate evolutionary developmental growth processes contributing to modifications in skull morphogenesis: acceleration and hypermorphosis. CONCLUSION: These findings are consistent with a role for peramorphosis, a form of heterochrony, in the evolution of bat dietary specialists.

Development, metamorphosis, morphology, and diversity: The evolution of chordate muscles and the origin of vertebrates.

Recent findings that urochordates are the closest sister-group of vertebrates have dramatically changed our understanding of chordate evolution and vertebrate origins. To continue to deepen our understanding of chordate evolution and diversity, in particular the morphological and taxonomical diversity of the vertebrate clade, one must explore the origin, development, and comparative anatomy of not only hard tissues, but also soft tissues such as muscles. Building on a recent overview of the discovery of a cardiopharyngeal field in urochordates and the profound implications for reconstructing the origin and early evolution of vertebrates, in this study we focus on the broader comparative and developmental anatomy of chordate cephalic muscles and their relation to life history, and to developmental, morphological and taxonomical diversity. We combine our recent findings on cephalochordates, urochordates, and vertebrates with a literature review and suggest that developmental changes related to metamorphosis and/or heterochrony (e.g., peramorphosis) played a crucial role in the early evolution of chordates and vertebrates. Recent studies reviewed here supported de Beer's "law of diversity" that peramorphic animals (e.g., ascidians, lampreys) are taxonomically and morphologically less diverse than nonperamorphic animals (e.g., gnathostomes), probably because their "too specialized" development and adult anatomy constrain further developmental and evolutionary innovations. Developmental Dynamics 244:1046-1057, 2015. © 2014 Wiley Periodicals, Inc.

Macroevolutionary trends in theropod dinosaur feeding mechanics.

Theropod dinosaurs underwent some of the most remarkable dietary changes in vertebrate evolutionary history, shifting from ancestral carnivory1-3 to hypercarnivory4,5 and omnivory/herbivory,6-9 with some taxa eventually reverting to carnivory.10-12 The mandible is an important tool for food acquisition in vertebrates and reflects adaptations to feeding modes and diets.13,14 The morphofunctional modifications accompanying the dietary changes in theropod dinosaurs are not well understood because most of the previous studies focused solely on the cranium and/or were phylogenetically limited in scope,12,15-21 while studies that include multiple clades are usually based on linear measurements and/or discrete osteological characters.8,22 Given the potential relationship between macroevolutionary change and ontogenetic pattern,23 we explore whether functional morphological patterns observed in theropod mandibular evolution show similarities to the ontogenetic trajectory. Here, we use finite element analysis to study the mandibles of non-avialan coelurosaurian theropods and demonstrate how feeding mechanics vary between dietary groups and major clades. We reveal an overall reduction in feeding-induced stresses along all theropod lineages through time. This is facilitated by a post-dentary expansion and the development of a downturned dentary in herbivores and an upturned dentary in carnivores likely via the "curved bone effect." We also observed the same reduction in feeding-induced stress in an ontogenetic series of jaws of the tyrannosaurids Tarbosaurus and Tyrannosaurus, which is best attributed to bone functional adaptation. This suggests that this common tendency for structural strengthening of the theropod mandible through time, irrespective of diet, is linked to "functional peramorphosis" of bone functional adaptations acquired during ontogeny.