Osteohistology of Greererpeton provides insight into the life history of an early Carboniferous tetrapod

Abstract

The vertebrate transition to land is one of the most consequential, yet poorly understood periods in tetrapod evolution. Despite the importance of the water–land transition in establishing modern ecosystems, we still know very little about the life histories of the earliest tetrapods. Bone histology provides an exceptional opportunity to study the biology of early tetrapods and has the potential to reveal new insights into their life histories. Here, we examine the femoral bone histology from an ontogenetic series of Greererpeton, an early tetrapod from the Middle‐Late Mississippian (early Carboniferous) of North America. Thin‐sections and micro‐CT data show a moderately paced rate of bone deposition with significant cortical thickening through development. An interruption to regular bone deposition, as indicated by a zone of avascular tissue and growth marks, is notable at the same late juvenile stage of development throughout our sample. This suggests that an inherent aspect to the life history of juvenile Greererpeton resulted in a temporary reduction in bone deposition. We review several possible life history correlates for this bony signature including metamorphosis, an extended juvenile phase, environmental stress, and movement (migration/dispersal) between habitats. We argue that given the anatomy of Greererpeton, it is unlikely that events related to polymorphism (metamorphosis, extended juvenile phase) can explain the bony signature observed in our sample. Furthermore, the ubiquity of this signal in our sample indicates a taxon‐level rather than a population‐level trait, which is expected for an environmental stress. We conclude that movement via dispersal represents a likely correlate, as such events are a common life history strategy of aquatically bound vertebrates.

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

“…The pattern of growth described here for Whatcheeria strongly juxtaposes that recently described for a slightly younger Carboniferous stem tetrapod, Greererpeton 37 , whose elongated and gracile gross anatomy suggest a particularly aquatic, perhaps benthic lifestyle 63 (Fig. 5 ).…”

“… Whatcheeria ( a – d ) is a large-bodied predator whose juvenile growth is characterized by fibrolamellar bone ( a ) that is eventually remodeled and completely replaced with parallel-fibered tissue ( b , c ) and subsequent slow deposition of lamellar bone ( c , d ). By contrast, Greererpeton 37 ( e – g ) is characterized by moderately paced bone deposition, even early in ontogeny ( e ), with a distinct lamellar band of bone deposited at the late juvenile stage ( e – g ). Sub-adult growth in Greererpeton is subsequently characterized by slowly deposited tissues ( f ) as well as endosteal deposition that results in a particularly thick adult cortex ( g ).…”

“…Finally, another possibility is that young juveniles occupied distinct habitats or nurseries 24 , 58 and therefore small individuals were not captured alongside the sub-adult and adult population. In any scenario, the absence of young juveniles is curious and important to note in the record of Whatcheeria and other early tetrapod ontogenetic series 37 .…”

“…5 ). An ontogenetic dataset showed that Greererpeton growth was characterized by a moderately paced rate of bone deposition, cortical thickening through development, and some evidence of growth marks 37 (Fig. 5e–g ).…”

Ossification patterns of the carpus and tarsus in salamanders and impacts of preaxial dominance on the fin-to-limb transition

“…(distal tarsals 1 and 2) ( 62 ), and two early tetrapods from the Carboniferous, Greererpeton burkemorani (dt 1) ( 64 ) and Proterogyrinus scheelei (distal carpals 1 and 2) ( 65 ). The phylogenetic positions of these two Carboniferous tetrapods are unstable; Greererpeton was recovered as closely related to either the basal crown or stem tetrapods, and Proterogyrinus is widely accepted as affiliated to Embolomeri, which, in turn, was argued as an order of crown or stem tetrapods or Reptiliomorpha [e.g., ( 66 , 67 )]. An even more primitive stem tetrapod, Whatcheeria deltae , was recently shown to have ossified distal tarsals 1, 4, and 5, with distal tarsal 4 being the largest in the digital arch ( 68 ).…”