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.

Dollo meets Bergmann: morphological evolution in secondary aquatic mammals

“…For instance, hindlimb reduction in tetrapods is related to multiple gene expression loss, including Sonic hedgehog (Shh), which gradually became unexpressed in the Cetacean lineage [69,70]. Adaptive changes in the Homeobox (Hox) gene expression and in its regulation underwent convergent evolution in fully aquatic mammals (whales, pinnipeds and sirenians) along with several morphological and physiological adaptations to aquatic lifestyle [13,[71][72][73][74][75]. The strong genomic implications linked to adaptations to a fully aquatic life are likely instrumental to making this transition irreversible.…”

“…Adapting to the constraints and opportunities presented by new realms requires several unique evolutionary innovations [5,11,12]. For instance, when transitioning from a terrestrial to a buoyant environment, different lineages independently evolved similar adaptations to be able to survive in the new habitat, such as streamlined body plans, dorsal nares and similar locomotory systems [5,[12][13][14][15]. These secondary aquatic adaptations in tetrapods are often interpreted as examples of Dollo's Law, which predicts the irreversibility of the loss of complex characters [16].…”

Divergent vertebral formulae shape the evolution of axial complexity in mammals

“…Here, we use a similar methodological and conceptual approach to examine complexity in another exemplary model system, the vertebral column of mammals [28][29][30] , although other serial structures (for example, body segments, paired appendages and teeth) would be suitable in other groups (for example, annelids, arthropods and vertebrates) [24][25][26][27] . The plasticity of the mammalian column results from developmental [46][47][48][49][50][51] , ecological 47,[52][53][54] , functional 51,[55][56][57] and evolutionary 48,49,53,54,58,59 factors, which also explain differences in vertebral numbers.…”

“…The hierarchical organization of biological systems offers additional proxies for complexity, such as the length and interconnectedness of biochemical pathways and gene regulatory networks or the degree of integration and modularity in the form and function of organismal parts 23 . One key aspect of anatomical complexity is the proliferation of, and the differentiation between, serial homologues [23][24][25][26][27][28][29][30] . The complexity of serial structures can be quantified as the number of elements forming a series (for example, 24 presacral vertebrae), the number of element types (for example, three types of presacral vertebrae: cervical, thoracic and lumbar) and/or the number of elements of each type (for example, 7 cervicals, 12 thoracics and 5 lumbars).…”

The influence of the land-to-sea macroevolutionary transition on vertebral column disparification in Pinnipedia

“…[4,8,15]). Therefore, the marine environment releases (in part) the axial skeleton from its role in body support under gravity [4,[16][17][18][19], and it allows oscillatory or undulatory movements [20]. On the other hand, this new physical environment imposed selective regimes leading to a major reorganization of their body plans, including the acquisition of streamlined, torpedo-shaped bodies, the transformation of limbs into flippers, and sometimes the appearance of caudal flukes [21][22][23].…”