Fossil bone histology reveals ancient origins for rapid juvenile growth in tetrapods

The study investigates when rapid juvenile growth associated with fibrolamellar bone first evolved within Tetrapoda. Elevated growth rates and high metabolic activity are characteristic of modern birds and mammals and were historically considered derived amniote traits, whereas ancestral tetrapods were assumed to have slower, amphibian-like growth. Bone histology provides a proxy for somatic growth rates because tissue organization reflects rates of bone deposition. Prior interpretations of early tetrapods have been limited by incomplete ontogenetic sampling and remodeling that can obscure early growth records. This work examines an ontogenetic series of femora from the Early Carboniferous stem tetrapod Whatcheeria deltae to test whether juveniles show fibrolamellar bone indicative of rapid growth, to document ontogenetic changes in bone tissues and cortical thickness, and to evaluate implications for life history, physiology, and early tetrapod ecological diversification.

The paper contextualizes fibrolamellar bone as a tissue strongly linked to rapid growth and elevated metabolic rates in extant endotherms (birds, mammals) and documents its occurrence across various fossil clades (e.g., dinosaurs, pterosaurs, sauropodomorphs, early reptiles, and non-amniote synapsids). In contrast, lissamphibians and many stem tetrapods typically exhibit slower growth and more organized, avascular bone tissues, though exceptions exist. Previous work on Devonian tetrapods (e.g., Acanthostega) suggested extended juvenile phases with slow deposition of lamellar bone, unossified elements until late juvenility, and expansive trabecular medullary cavities. The authors highlight how ontogenetic remodeling can erase juvenile growth signals, potentially biasing interpretations. They note that comprehensive ontogenetic histological datasets are rare, complicating comparisons across phylogeny and ecology, and emphasize the need for series-based sampling to resolve growth dynamics near the base of Tetrapoda.

• Specimens: Nine femora of Whatcheeria spanning four size classes (I–IV) defined by prior morphological/ossification criteria.
• Imaging: All specimens scanned via high-resolution micro-computed tomography (µCT) using a Bruker Skyscan 1173 at the MCZ Digital Imaging Facility (settings: 130 kV, 6 µA, 0.25 mm brass filter). Scan data archived at FMNH.
• Histology: Destructive thin-sectioning of four femora representing size classes I–IV (FMNH PR 5022, PR 5021, PR 1962, PR 5023). Transverse thin sections taken at the mid-diaphysis (primary center of ossification and longest growth record). Sections examined under polarized light with a lambda filter.
• Quantification: Total cross-sectional and cortical bone areas measured in ImageJ to assess cortical contribution to cross-sectional area. Tissue types (fibrolamellar, parallel-fibered, lamellar), vascular patterns, secondary remodeling, and trabecular architecture were recorded.
• Data availability: Histological images deposited in Morphobank (Project 1722).
• Analytical aim: Track ontogenetic shifts in cortical thickness and tissue organization; correlate size classes to ontogenetic stages; evaluate presence/absence of growth marks; interpret growth rates and life history implications from tissue types and remodeling patterns.

• Discovery of fibrolamellar bone in juvenile Whatcheeria (size class I; FMNH PR 5022), indicating rapid somatic growth and elevated metabolic rates early in ontogeny.
• Ontogenetic transformation of bone tissues: juveniles dominated by fibrolamellar bone (with reticular primary canals) shift to parallel-fibered and then predominantly lamellar bone in adults, accompanied by extensive secondary remodeling that largely obliterates primary juvenile tissues.
• Cortical thinning through growth with medullary trabecular expansion. Quantified cortical contribution to cross-sectional area (CSA):
  • Size class I (FMNH PR 5022): 57% cortical
  • Size class II (FMNH PR 5021): 25% cortical
  • Size class III (FMNH PR 1962): 34% cortical
  • Size class IV (FMNH PR 5023): 35% cortical
• Development of trabecular struts from scaffolding of the primary cortex; well-developed, interconnected trabecular networks in larger individuals.
• No lines of arrested growth or indicators of complete/partial growth cessation detected, even in highly organized lamellar cortices of larger specimens, implying continuous, albeit slowing, growth through to maturity.
• Ontogenetic stage correlation of size classes: size class I = late-stage juvenile; size class II = sub-adult; size classes III–IV = skeletally mature adults.
• Temporal and phylogenetic significance: Whatcheeria provides an unexpectedly early occurrence of fibrolamellar bone within Tetrapoda, extending the deep history of rapid juvenile growth beyond crown amniotes.
• Ecological implication: Rapid juvenile growth likely facilitated earlier attainment of large body size and sexual maturity, supporting occupation of a large-bodied predatory niche.

The presence of fibrolamellar bone in juvenile Whatcheeria demonstrates that rapid juvenile growth was present near the origin of tetrapods and was not exclusive to amniotes. The ontogenetic transition from fibrolamellar to parallel-fibered and then lamellar bone, alongside cortical thinning and medullary trabecular development, reflects a life history strategy of rapid early growth followed by slowed deposition toward skeletal maturity. Extensive remodeling in sub-adults and adults obliterates much of the primary juvenile record, explaining why adult microstructure can resemble that of Devonian taxa with slower growth and highlighting the risk of inferring life history from adult tissues alone. The absence of early juveniles in the fossil record of the Hiemstra Quarry could reflect a short juvenile phase (reducing preservation likelihood), taphonomic size-sorting, or juvenile habitat partitioning (nursery areas). Comparisons with Devonian stem tetrapods (e.g., Acanthostega) and contemporaneous taxa (e.g., Greererpeton) suggest diverse growth strategies early in tetrapod evolution, with Whatcheeria’s elevated juvenile growth potentially linked to ecological differentiation as a large-bodied predator. Collectively, these results argue for a deeper origin of elevated growth rates and metabolic capacities in tetrapods and suggest such physiology may have aided early terrestrialization dynamics.

This study documents a remarkably early instance of fibrolamellar bone in a stem tetrapod, demonstrating rapid juvenile growth in Whatcheeria deltae. Histological evidence across an ontogenetic series shows juveniles grew quickly and reached skeletal maturity relatively fast, enabling occupation of a large-bodied predatory niche. These findings expand the temporal and phylogenetic scope of elevated growth beyond crown tetrapods and reveal that diverse growth patterns existed early in tetrapod evolution. Future work should target earlier juvenile stages, additional skeletal elements, broader taxonomic sampling, and environmental context to refine growth models and test the prevalence and ecological drivers of elevated juvenile growth in early tetrapods.

• Sampling is restricted to femoral histology; results may not generalize to other skeletal elements.
• Only four femora were destructively thin-sectioned, limiting quantitative breadth; other specimens were assessed via µCT.
• The earliest juvenile stages are absent from the sampled assemblage, potentially biasing ontogenetic interpretation.
• Taphonomic and ecological biases at the Hiemstra Quarry may under-represent small/young individuals.
• Extensive remodeling in sub-adults/adults erases juvenile primary tissues, complicating reconstruction of early growth dynamics.