The humerus of Eusthenopteron: a puzzling organization presaging the establishment of tetrapod limb bone marrow
- Proceedings. Biological sciences / The Royal Society
- Published almost 4 years ago
Because of its close relationship to tetrapods, Eusthenopteron is an important taxon for understanding the establishment of the tetrapod body plan. Notably, it is one of the earliest sarcopterygians in which the humerus of the pectoral fin skeleton is preserved. The microanatomical and histological organization of this humerus provides important data for understanding the evolutionary steps that built up the distinctive architecture of tetrapod limb bones. Previous histological studies showed that Eusthenopteron’s long-bone organization was established through typical tetrapod ossification modalities. Based on a three-dimensional reconstruction of the inner microstructure of Eusthenopteron’s humerus, obtained from propagation phase-contrast X-ray synchrotron microtomography, we are now able to show that, despite ossification mechanisms and growth patterns similar to those of tetrapods, it also retains plesiomorphic characters such as a large medullary cavity, partly resulting from the perichondral ossification around a large cartilaginous bud as in actinopterygians. It also exhibits a distinctive tubular organization of bone-marrow processes. The connection between these processes and epiphyseal structures highlights their close functional relationship, suggesting that either bone marrow played a crucial role in the long-bone elongation processes or that trabecular bone resulting from the erosion of hypertrophied cartilage created a microenvironment for haematopoietic stem cell niches.
The transition from fish to tetrapod was arguably the most radical series of adaptive shifts in vertebrate evolutionary history. Data are accumulating rapidly for most aspects of these events, but the life histories of the earliest tetrapods remain completely unknown, leaving a major gap in our understanding of these organisms as living animals. Symptomatic of this problem is the unspoken assumption that the largest known Devonian tetrapod fossils represent adult individuals. Here we present the first, to our knowledge, life history data for a Devonian tetrapod, from the Acanthostega mass-death deposit of Stensiö Bjerg, East Greenland. Using propagation phase-contrast synchrotron microtomography (PPC-SRμCT) to visualize the histology of humeri (upper arm bones) and infer their growth histories, we show that even the largest individuals from this deposit are juveniles. A long early juvenile stage with unossified limb bones, during which individuals grew to almost final size, was followed by a slow-growing late juvenile stage with ossified limbs that lasted for at least six years in some individuals. The late onset of limb ossification suggests that the juveniles were exclusively aquatic, and the predominance of juveniles in the sample suggests segregated distributions of juveniles and adults at least at certain times. The absolute size at which limb ossification began differs greatly between individuals, suggesting the possibility of sexual dimorphism, adaptive strategies or competition-related size variation.
The earliest tetrapods had hands and feet with up to eight digits but this number was subsequently reduced during evolution. It was assumed that lineages with more than five digits no longer exist but investigations of clawed-frogs now indicate that they posses a rudimentary or atavistic sixth digit in their hindlimb. A recent reevaluation of the stem tetrapod Ichthyostega predicts that its seven digits evolved from two different types of ancestral fin radials, pre-axial and post-axial. In this context we now ask the question, should we consider a pre-axial origin of the thumb as reason for its unique genetic signature?
[This corrects the article DOI: 10.1371/journal.pone.0118882.].