An Integrative Approach to the Evolutionary Assembly of Vertebrate Body Plans

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Animal forms - in all their diversity - represent as few as 40+ body plans. How these basic patterns originated remains a core pursuit of evolutionary biology. However, the evolution of a body plan requires non-incremental transitions and does not readily fit models of population-level processes. To fill in this gap, my recent work has documented these transitions in early vertebrates (primitive fishes) and has also yielded a promising model in zebrafish that express a major phenotypic shift as population-level fluctuations. My long-term objective is to uncover mechanisms that both constrained and facilitated phenotypic evolution in early vertebrates. With that goal, I investigate how major discrete variations: a) arise; b) become canalized; and c) increase in disparity. To do this, I focus on key components of the vertebrate body plan: oral apparatus (OA), central nervous system (CNS), and head-trunk boundary (HTB). I hypothesize that major phenotypic variation emerges from: a) canalization of reaction norms; and b) increase in functional linkages. This hypothesis generates the following predictions: 1)Plasticity mediates functional variation caused by a novel allele, shifting reaction norms of linked traits (tested in OA); 2)Reaction norms become canalized (OA); and 3)Rates of trait evolution increase in those functionally linked to the novel trait more than in the trait itself (OA, CNS, HTB). OA: I will reveal previously unknown OA repertoire in vertebrates: a) feeding in the absence of jaw movement, observed in zebrafish mutants lacking jaw joints; and b) newly reconstructed oral discs of stem lampreys that suggest a uniquely assembled suction cup. I aim to test, using the zebrafish mutants, how plastic responses to the jaw disruption (population-level fluctuations) enabled modified suction feeding, and whether this response harbors any potential to become genetically fixed. CNS: A recent discovery revealed vertebrate-like `brain' signaling centers in non-chordate outgroup (hemichordates). However, it remains unclear whether a gene network preceded structure or hidden complexity exists in the seemingly simple hemichordate nervous system. To test this, I will map neural circuitry in hemichordates. HTB: Jawed vertebrates have a complete HTB, but this transition appears saltatory in the absence of intermediate forms. I aim to identify a transitional state of HTB evolution in a sister group of jawed vertebrates. This will constrain when and how HTB structures (neck, heart, pectoral fins) evolved in a vertebrate body. Throughout this project I investigate the mechanisms, both developmental and functional, that yielded the vertebrate body plan and also govern our anatomy. The jawless mutant zebrafish offer a new path to address a long-standing question: How do major variations arise? This facilitates the next phase: our multifaceted analysis to reveal convergent functional evolution or transitional states in early vertebrates.