Developmental mechanisms underlying avian morphological evolution

Abstract

Vertebrates have evolved remarkable morphological diversity over millions of years, from the smallest hummingbird to the largest whales, in response to natural selection. These endless forms, generated over the course of evolution, can largely be traced back to changes in embryonic development, where modifications of existing structures and the generation of completely novel structures occurs. A mechanistic understanding of how evolutionary diversity arises thus necessitates a deep understanding of the developmental processes underlying morphological transitions in vertebrate evolution. Birds serve as a particularly useful model for this endeavor as one of the most diverse groups of land vertebrates with a number of evolutionarily novel structures – such as feathers and their vocal organ, the syrinx – and a wide array of morphological adaptations, including webbed feet in aquatic birds and flippers used for diving in penguins. Here I present three case studies for the developmental mechanisms underlying avian morphological evolution. First, I characterize the pathways involved in the formation of the vocal folds in the avian syrinx, an evolutionarily novel vocal organ. We find that the syringeal vocal folds are derived from a distinct developmental source than vocal folds in other tetrapods, which are located in the larynx, but similar developmental pathways are active in both types of vocal folds. We further investigate the morphological evolution of the syrinx and show that the presence of paired sound sources (i.e., two sets of syringeal vocal folds) is likely ancestral to extant birds. Next, I present a characterization of the embryonic development of the penguin flipper, which has a series of remarkable adaptations to underwater diving, including loss of distal forelimb muscles and a flattening of forelimb bones. Surprisingly, both the muscles and bones in the early penguin embryo are patterned similar to other birds but are dramatically remodeled late duringembryogenesis. Forelimb muscles are patterned but fail to proliferate, leading to an apparent reduction in musculature. Bones in the penguin flipper are patterned as round tubes like in flighted birds but undergo a gradual ossification of connective tissue which resembles the formation of bone ridges at tendon-attachment sites which has been characterized in the mouse. This process starts at the epiphysis and extends down the length of the bone during development, which is paralleled by the progressive expansion of bone flattening in the penguin fossil record. Finally, I investigate the developmental and genetic mechanisms underlying the convergent evolution of interdigit webbing in birds. While interdigit webbing has evolved several times in birds, we find little evidence of genome-wide convergence in conserved non-coding regions. We show that conserved early developmental enhancers for the gene Gremlin, which has been shown to inhibit interdigit apoptosis, are accessible in the duck interdigit, but Gremlin is likely activated using a novel pathway. In addition, I perform transcriptomic analysis in developing chick, duck, and penguin interdigit and find that duck and penguins have likely evolved distinct mechanisms for interdigit webbing retention.

Together, these data provide new insights into the developmental mechanisms underlying morphological evolution and underscore the extent to which existing genetic modules and developmental processes are reused to facilitate the evolution of novel and highly modified structures.