Hidden morphological diversity among early tetrapods

Detailed micro-computed tomography analysis of the skull of Lethiscus stocki places it much earlier in the tetrapod lineage that was previously thought, showing that early tetrapods were more morphologically diverse than has been believed. The aïstopods are a specialized, extinct group of amphibians with elongated bodies and reduced limbs. They are usually placed within the lepospondyl clade, a disparate group of amphibians more or less closely related to amniotes. One of these creatures is Lethiscus stocki, the earliest known tetrapod to post-date the early Carboniferous 'Romer's Gap' that separates the large, archaic early tetrapods from the Devonian from later creatures. Jason Anderson and colleagues digitally dissect a fossil specimen of Lethiscus and show a suite of features that shift it down the evolutionary tree towards the tetrapod base, showing that morphological diversity in the earliest tetrapods was greater than had been thought. The finding also calls for some redefinition of amniotes. Phylogenetic analysis of early tetrapod evolution has resulted in a consensus across diverse data sets1,2,3 in which the tetrapod stem group is a relatively homogenous collection of medium- to large-sized animals showing a progressive loss of ‘fish’ characters as they become increasingly terrestrial4,5, whereas the crown group demonstrates marked morphological diversity and disparity6. The oldest fossil attributed to the tetrapod crown group is the highly specialized aïstopod Lethiscus stocki7,8, which shows a small size, extreme axial elongation, loss of limbs, spool-shaped vertebral centra, and a skull with reduced centres of ossification, in common with an otherwise disparate group of small animals known as lepospondyls. Here we use micro-computed tomography of the only known specimen of Lethiscus to provide new information that strongly challenges this consensus. Digital dissection reveals extremely primitive cranial morphology, including a spiracular notch, a large remnant of the notochord within the braincase, an open ventral cranial fissure, an anteriorly restricted parasphenoid element, and Meckelian ossifications. The braincase is elongate and lies atop a dorsally projecting septum of the parasphenoid bone, similar to stem tetrapods such as embolomeres. This morphology is consistent in a second aïstopod, Coloraderpeton, although the details differ. Phylogenetic analysis, including critical new braincase data, places aïstopods deep on the tetrapod stem, whereas another major lepospondyl lineage is displaced into the amniotes. These results show that stem group tetrapods were much more diverse in their body plans than previously thought. Our study requires a change in commonly used calibration dates for molecular analyses, and emphasizes the importance of character sampling for early tetrapod evolutionary relationships.

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