Abstract
Through phenotypic plasticity, bones can change in structure and morphology, in response to physiological and biomechanical influences over the course of individual life. Changes in bones also occur in evolution as functional adaptations to the environment. In this study, we report on the evolution of bone mass increase (BMI) that occurred in the postcranium and skull of extinct aquatic sloths. Although non-pathological BMI in postcranial skeleton has been known in aquatic mammals, we here document general BMI in the skull for the first time. We present evidence of thickening of the nasal turbinates, nasal septum and cribriform plate, further thickening of the frontals, and infilling of sinus spaces by compact bone in the late and more aquatic species of the extinct sloth Thalassocnus. Systemic bone mass increase occurred among the successively more aquatic species of Thalassocnus, as an evolutionary adaptation to the lineage's changing environment. The newly documented pachyostotic turbinates appear to have conferred little or no functional advantage and are here hypothesized as a correlation with or consequence of the systemic BMI among Thalassocnus species. This could, in turn, be consistent with a genetic accommodation of a physiological adjustment to a change of environment.
Highlights
It has been known since the nineteenth century that bone structure can change over the course of an individual’s life in response to the pattern and magnitudes of mechanical loads and by other physiological processes [1,2]
The lack of paranasal sinuses was suggested to be an adaptation to diving in extant cetaceans, but this can hardly be argued for sirenians or aquatic sloths, which are/were likely shallow divers, as shown for the latter by their strong osteosclerosis and pachyostosis [9,13]
Formerly known exclusively as a physiological adjustment, was here evidenced to have been retained as an evolutionary adaptation thanks to the outstandingly detailed and early-stage record of a land-to-sea transition in the extinct sloth Thalassocnus. This new result is consistent with a macroevolutionary process of selection on environmentally induced variation of phenotypic plasticity [64,65,66,67,68,69]
Summary
It has been known since the nineteenth century that bone structure can change over the course of an individual’s life in response to the pattern and magnitudes of mechanical loads and by other physiological processes [1,2]. Using the oriented CT-scan stack (see above and electronic supplementary material, files S2, S3, figure S1A – C), we measured with FIJI the thickness of the cranial vault (in mm) at five standard locations, adapting the definitions of Lieberman [6]: supraoccipital anteromedial corner (for further precision, we selected the point of least thickness); maximum thickness of the nuchal region in the midsagittal plane; middle of the parietal (Lieberman [6] used the parietal eminence, but this structure is absent in pilosans [21]); bregma (average of parietal and frontal) and centre of the frontal along the midsagittal axis (the measure was taken internally up to the dorsalmost level of the frontal sinus on the corresponding coronal section). Graphics were produced with strap [26], ggplot2 [27], reshape [28] and cowplot [29] packages
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