Birds represent the most successful group of modern land vertebrates. Much of their enormous ecological diversity is driven by evolution of the unique bird face, specifically the beak or bill. A key evolutionary innovation, such as a bird beak, can only be fully explained by examining both its ultimate and proximate causes -- the broad-scale evolutionary patterns of change leading to appearance of beak structure and the developmental processes that must be altered to turn a reptilian face into a bird beak, respectively. This study will trace the transition from a nonavian reptile face to the unique bill of birds by applying quantitative techniques to the fossil record, tracing the sequence and nature of transformations during bird evolution. Using that information, the proximate molecular developmental mechanisms behind each transformation will be dissected using chickens and, as comparative material, embryos of crocodylians (the closest living relatives to birds) and lizards. Experimental support for hypotheses about the significance of changes in gene expression will be provided by replicating 'reptilian' states in chicken embryos, producing an altered phenotype that resembles the ancestral condition. This detailed, integrative study of the evolution of the bird face will provide insight into the fundamental nature and mechanisms of key evolutionary transitions that lead to the major radiations populating the earth today.
Understanding these transformations is at the core of comprehending the driving forces behind biodiversity and biological disparity. Few studies have so comprehensively examined the biology of a major adaptive feature. Moreover, this work will be broadly integrative in that the advanced molecular development investigations will be tied heavily to legacy museum and digital collection based activities. Even embryos used in the developmental work will find a permanent archive in the Harvard museum collections. This close tie to the museum lends itself easily to public communication. Exhibits based on this work will draw in the public using the charismatic study subjects -- birds, dinosaurs, and crocodiles -- and will represent a prime opportunity to tie such classical natural history subjects to cutting-edge molecular science.
The research funded by this grant allowed advances in the understanding of the evolution origins of the unique skull of birds. The bird skull is highly modified in having extensive fusion and reconfiguration of bones, in housing an enormously expanded brain, and in bearing the unique anatomical hallmark of birds, the beak, which has also allowed their diversification into a wide range of ecological niches. Surprisingly, little work had been performed on the overall anatomical changes leading to the bird head, and we set out first to investigate these using both living animals and the fossil record. In particular, we used a type of quantitiative shape analysis to determine overall patterns of shape change over the lineage leading to birds. Moreover, we included in the same analysis the shape changes during the maturation or ontogeny of a single species, using both living animals (birds and alligators, which are closely related to birds) and the fossil record of ontogeny. By doing so we discovered that the heads of adult birds resemble to a great degree the heads of juveniles of their ancestors, meaning that birds display a phenomenon called paedomorphosis ("child-shape"). This work was published in Nature in 2012 and was covered widely by the press, including the New York Times and the LA Times. After determining overall changes during the evolution of birds, we began to address more specific changes to the molecular mechanisms of development. We found several gene expression patterns in the early embryonic face that were unique to birds and that we posited were involved in the origin of the beak. When we replicated the ancestral gene expression, as displayed for instance by alligators and mammals, in chickens, the chickens developed more ancestral-looking faces, which we confirmed using the same type of shape analysis that we utilized for the first part of the project described above. Finally, we were interested in tooth development in bird ancestors and ultimately tooth loss in birds, another notable event in avian history. To provide a baseline for this work, we examined the molecular patterning of teeth in alligators, which have teeth that in their overall configuration broadly resemble those of fossils along the direct lineage to birds. This work will be published soon in Evolution & Development. Because of the broad interest in our published work, we were able to communicate it to the public in the form of newspaper articles, interviews including a Nature Podcast, and, in the future, textbook sections. Moreover, both PIs have given numerous seminars and lessons for the general public, many of them through the Harvard Museum of Natural History. We have also collaborated with scientists across the world, including South Africa. Finally, a number of students were trained while they assisted with this work. All are now in biology Ph.D. programs. Two were international (from Latin American countries) -- an undergraduate and a master's student -- and one was a female Harvard undergraduate.