Body-axis organization in tetrapods: a model-system to disentangle the developmental origins of convergent evolution in deep time

Abstract

Convergent evolution is a central concept in evolutionary theory but the underlying mechanism has been largely debated since On the Origin of Species. Previous hypotheses predict that developmental constraints make some morphologies more likely to arise than others and natural selection discards those of the lowest fitness. However, the quantification of the role and strength of natural selection and developmental constraint in shaping convergent phenotypes on macroevolutionary timescales is challenging because the information regarding performance and development is not directly available. Accordingly, current knowledge of how embryonic development and natural selection drive phenotypic evolution in vertebrates has been extended from studies performed at short temporal scales. We propose here the organization of the tetrapod body-axis as a model system to investigate the developmental origins of convergent evolution over hundreds of millions of years. The quantification of the primary developmental mechanisms driving body-axis organization (i.e. somitogenesis, homeotic effects and differential growth) can be inferred from vertebral counts, and recent techniques of three-dimensional computational biomechanics have the necessary potential to reveal organismal performance even in fossil forms. The combination of both approaches offers a novel and robust methodological framework to test competing hypotheses on the functional and developmental drivers of phenotypic evolution and evolutionary convergence.

Keywords: development; macroevolution; phenotypic evolution; tetrapod axis.

Figure 1.

Body-axis macroevolution in marine tetrapods. (a) phylogenetic relationships of tetrapod lineages that include marine taxa, from [12]. (b) Primary developmental factors governing presacral axial organization [13]. (c) Changes in selective regimes from land-to-sea. Drag is minimized by streamlining the body (and appendages). Thrust and efficiency are increased by swimming strategies that use a lift-based oscillating hydrofoil [14].

Figure 2.

Schematic workflow (divided in three interconnected blocks) for testing competing hypotheses on developmental and functional triggers of evolutionary convergence in the tetrapod body-axis. (a) Derivation of empirical and theoretical (phylo)morphospaces from realized and unrealized combinations of the three developmental variables of body-axis organization to test for morphological convergence and to quantify how accessible design space is to developmental evolution; (b) the quantification of functional parameters derived from the application of biomechanical three-dimensional analyses (CFD) of realized designs, modified from [36]; (c) their integration into the morphospaces to develop performance landscapes to test for functional optimality of explored and unexplored regions of the morphospace, as well as for the existence of potential Pareto fronts. The later represents the set of designs that cannot be improved simultaneously in all tasks and allows for detecting performance trade-offs and it delimits the inaccessible design space from the region occupied by suboptimal designs.