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

Patterns of growth throughout the lifetime of an animal reflect critical life history traits such as reproductive timing, physiology, and ecological interactions. The ancestral growth pattern for tetrapods has traditionally been described as slow-to-moderately paced, akin to modern amphibians, with fast growth and high metabolic rates considered a specialized physiological trait of amniotes. Here, we present bone histology from an ontogenetic series of the Early Carboniferous stem tetrapod Whatcheeria deltae, and document evidence of fibrolamellar bone-primary bone tissue associated with fast growth. Our data indicate that Whatcheeria juveniles grew rapidly and reached skeletal maturity quickly, allowing them to occupy a large-bodied predator niche in their paleoenvironment. This life history strategy contrasts with those described for other stem tetrapods and indicates that a diversity of growth patterns existed at the origins of tetrapod diversification. Importantly, Whatcheeria marks an unexpectedly early occurrence of fibrolamellar bone in Tetrapoda, both temporally and phylogenetically. These findings reveal that elevated juvenile growth is not limited to amniotes, but has a deep history in the tetrapod clade and may have played a previously unrecognized role in the tetrapod invasion of land.

Multituberculate Mammals Show Evidence of a Life History Strategy Similar to That of Placentals, Not Marsupials.

AbstractThe remarkable evolutionary success of placental mammals has been partly attributed to their reproductive strategy of prolonged gestation and birthing of relatively precocial, quickly weaned neonates. Although this strategy was conventionally considered derived relative to that of marsupials with highly altricial neonates and long lactation periods, mounting evidence has challenged this view. Until now the fossil record has been relatively silent on this debate, but here we find that proportions of different bone tissue microstructures in the femoral cortices of small extant marsupials and placentals correlate with length of lactation period, allowing us to apply this histological correlate of reproductive strategies to Late Cretaceous and Paleocene members of Multituberculata, an extinct mammalian clade that is phylogenetically stemward of Theria. Multituberculate bone histology closely resembles that of placentals, suggesting that they had similar life history strategies. A stem-therian clade exhibiting evidence of placental-like life histories supports the hypothesis that intense maternal-fetal contact characteristic of placentals is ancestral for therians. Alternatively, multituberculates and placentals may have independently evolved prolonged gestation and abbreviated lactation periods. Our results challenge the hypothesis that the rise of placental mammals was driven by unique life history innovations and shed new light on early mammalian diversification.

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

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.

Evidence of torpor in the tusks of Lystrosaurus from the Early Triassic of Antarctica.

Antarctica has hosted a wide range of ecosystems over the past 500-million years. Early in the Mesozoic, the Antarctic portion of southern Pangaea had a more habitable climate, but its position within the polar circle imposed extreme photoperiod seasonality on its resident flora and fauna. It remains unclear to what degree physiological adaptations underpinned the ability of tetrapods to establish the terrestrial communities captured in the fossil record. Here we use regular and stressful growth marks preserved in the dentine of ever-growing tusks of the Early Triassic mammalian predecessor, Lystrosaurus, to test for adaptations specific to this polar inhabitant. We find evidence of prolonged stress indicative of torpor when compared to tusk samples from non-polar populations of Lystrosaurus. These preliminary findings are to our knowledge the oldest instance of torpor yet reported in the fossil record and demonstrate unexpected physiological flexibility in Lystrosaurus that may have contributed its survivorship through the Permo-Triassic mass extinction.

Histological and developmental insights into the herbivorous dentition of tapinocephalid therapsids.

Tapinocephalids were one of the earliest therapsid clades to evolve herbivory. In acquiring derived tooth-to-tooth occlusion by means of an exaggerated heel and talon crown morphology, members of this family have long been considered herbivorous, yet little work has been done to describe their dentition. Given the early occurrence of this clade and their acquisition of a dentition with several derived features, tapinocephalids serve as an important clade in understanding adaptations to herbivory as well as macroevolutionary patterns of dental trait acquisition. Here we describe the histology of tapinocephalid jaws and incisors to assess adaptations to herbivory. Our results yield new dental characters for tapinocephalids including a peculiar enamel structure and reduced enamel deposition on the occlusal surface. These traits are convergent with other specialized herbivorous dentitions like those found in ornithischian dinosaurs and ungulates. Furthermore, these results demonstrate that while acquiring some specializations, tapinocephalids also retained plesiomorphic traits like alternate, continuous replacement. We interpret these findings as an example of how different combinations of traits can facilitate a derived and specialized dentition and then discuss their implications in the acquisition of a mammal-like dentition.

Dental ontogeny in extinct synapsids reveals a complex evolutionary history of the mammalian tooth attachment system.

The mammalian dentition is uniquely characterized by a combination of precise occlusion, permanent adult teeth and a unique tooth attachment system. Unlike the ankylosed teeth in most reptiles, mammal teeth are supported by a ligamentous tissue that suspends each tooth in its socket, providing flexible and compliant tooth attachment that prolongs the life of each tooth and maintains occlusal relationships. Here we investigate dental ontogeny through histological examination of a wide range of extinct synapsid lineages to assess whether the ligamentous tooth attachment system is unique to mammals and to determine how it evolved. This study shows for the first time that the ligamentous tooth attachment system is not unique to crown mammals within Synapsida, having arisen in several non-mammalian therapsid clades as a result of neoteny and progenesis in dental ontogeny. Mammalian tooth attachment is here re-interpreted as a paedomorphic condition relative to the ancestral synapsid form of tooth attachment.