Shifting the Black Box: Approaches to the Development and Evolution of the Vertebrate Mesoderm

Abstract

The genotype was an abstraction at the time of the Modern Synthesis, though its direct causation of the phenotype was comfortably assumed. The cellular and developmental processes that actually build the phenotype were relegated to a black box and largely considered irrelevant to evolutionary biology. Techniques for manipulating DNA and sequencing of whole genomes have now given the genotype physical presence, and dramatic correlations of genetic and phenotypic perturbation reinforce the earlier assumptions. The last four decades have brought development back into the mainstream of evolutionary biology with the formalization of evo-devo. However, the genocentric perspective persists. A majority of evo-devo studies focus on evolution of developmental genes, and we still lack adequate knowledge of the rich phenomena between genotype and phenotype. Here I present data and perspectives from the vertebrate mesoderm and its musculoskeletal derivatives. The conserved embryonic cell populations of somitic and lateral plate mesoderm interact to generate the enormous range of diversity within the phylum, and understanding changes in these interactions can explain and predict both innovation and constraint. A wealth of work has mapped the expression and interactions of genes at play in the mesoderm, but while the musculoskeletal system varies widely, the genetic picture is highly conserved. Here I focus on the embryological, cellular context in which the genes take their actions, and argue that this context is the source of morphological variation leading to evolution. Correlations between genetic perturbations and morphological outcomes are valuable data but rarely address what actually goes on during morphogenesis. Cell behaviors like shape change, proliferation, growth, migration, and adhesion are activities that build structure in the embryo. These essential phenomena are often still stuck under the black box, which must be lifted to understand the dynamics that are the source of variation for evolutionary change.