Preface to the special issue on evolution and morphological diversity

A century ago developmental biology was primarily comparative embryology, the beginnings of “evo devo”. Today, anyone interested in an unusual organism can find anatomical studies and developmental staging series dating to the 19 and early 20 century, but often not more recent than the 1940s. The advent of molecular developmental genetics led to a funneling of focus down to a few model organisms based on ease of acquisition and husbandry, simple genetics, and a standard toolkit to study and manipulate developmental processes. Thus there was one plant, one worm, one fly, one fish, one bird, and one mammal. Despite once thriving as important embryological models at Woods Hole and elsewhere, marine invertebrates were woefully underrepresented in mainstream developmental genetics, and nonavian reptiles were left right out. Similarly, developmental biology once played a prominent role in evolutionary biology. For example, 19 century embryologists recognized the importance of conserved developmental traits as clues to shared ancestry among species. Indeed in The Origin of Species, Charles Darwin pondered the fact of “embryos of different species within the same class, generally, but not universally, resembling each other” (Darwin, 1859, Chapter 13, p.442). However, with the rise of statistical population genetics in the mid20 century and a focus on the proximate and ultimate causes of natural selection, there was no longer a clear place for developmental mechanisms in the new Modern Synthesis. Nevertheless, many researchers continued to pursue an understanding of the developmental mechanisms that distinguish species from one another, but on the edges of the fold of evolution. Bold ideas about simple developmental mechanisms of major evolutionary change, including the supposition of unfortunately named “hopeful monsters” (Goldschmidt, 1940), percolated through the literature but were largely dismissed by the Synthesis. Decades later, Davidson and others proposed that regulation of gene expression was a principal mechanism of developmental evolution (Britten and Davidson, 1969). The theoretical importance of gene regulatory control was augmented by the discovery of extensively conserved developmental “toolkit” genes, such as the Hox genes in diverse animals (McGinnis et al., 1984). Together, these ideas issued a major challenge to both evolutionary and developmental biologists studying a wide variety of organisms: if disparate species share such similar genes that control key developmental processes, how do gene regulatory networks shape an organism and generate species diversity? We started graduate school at a time when the zebrafish was considered an “emerging model system”, and there was some trepidation at the time in the greater field of developmental genetics. What could one learn from the zebrafish that couldn’t be studied in a mouse? Would findings in the zebrafish be fishspecific and therefore “uninteresting”? Over the past two decades, we witnessed a rapid emergence of molecular studies of evolution and development and a remarkable expansion of the number of study species. In retrospect, the focus on model systems in developmental genetics was essential to pioneer powerful experimental approaches that ultimately benefit studies of evolutionary diversity. Complex molecular methods once limited functional experiments such as gene targeting to this small number of model species. More recently, the explosion of new genome editing technologies has begun to allow specific engineering – deletion, insertion, or replacement – in the genomes of a multitude of species (Gaj et al., 2013). In parallel, technical advances driven by sequencing the genomes of human and model species have dramatically driven down costs and improved ease of assembly and annotation. As a result, there are currently over 3,000 sequenced eukaryotic genomes with an anticipated acceleration as more species are added to cover phylogenetic diversity and to address problems of economic and health importance (diArk, http://www. diark.org/diark). Hence, we have now entered an exciting period in evolutionary and developmental genetics. Instead of relying exclusively on a small group of traditional model organisms, we can now select appropriate animal models to understand specific traits and processes based upon their biology rather than historical precedence. These opportunities raise a set of big picture “existential” questions for the field of evo devo. Within the broader field of evolutionary biology, can we relate principles of population genetics and selection to the molecular regulation of development? How does phenotypic variation in a population offset developmental canalization to provide the material for natural selection? Can we define a set of developmental “rules” for evolution on par with the statistical and theoretical framework of the Modern Synthesis, D E V E L O P M E N T A L D Y N A M IC S