Wednesday, May 9, 2018

[PaleoMammalogy • 2018] Evolutionary Adaptation to Aquatic Lifestyle in Extinct Sloths Thalassocnus Can Lead to Systemic Alteration of Bone Structure

Thalassocnus carolomartini McDonald & Muizon, 2002

 Amson, Billet & de Muizon, 2018

Illustration: Oliver Demuth 

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.

Keywords: bone mass increase, evolutionary adaptation, phenotypic plasticity, physiological adjustment, Thalassocnus, turbinates

Systemic bone structure alteration, formerly known exclusively as a physiological adjustment, was here evidenced to have been retained as an evolutionary adaptation thanks to the outstandingly detailed (both in terms of geological age and anatomy) 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 [Gause, 1942; Sultan, 2017]. In other words, the systemic alteration of the highly plastic bone structure that gradually evolved among the species of Thalassocnus may represent an example of a macroevolutionary transition from a phenotypic accommodation (to an environmental change) to a genetic accommodation. In the context of the so-called extended (evolutionary) synthesis, Pigliucci [2010] points out the difficulty of uncovering such examples, which are required to corroborate the hypothesis that phenotypic plasticity has an important macroevolutionary role.

The precise mechanism causing an adjustment (over the course of an individual's life) of bone structure in response to life in water is not understood. However, one can speculate that the shift of a terrestrial animal to an aquatic environment involves an increase in exercise intensity, which was shown to induce BMI [Lieberman, 1996; Biewener & Bertram, 1994]. There does not seem to be a clear influence of swimming on the bone mass of athletes [Gómez-Bruton, et al., 2013] (but differences in other physical activities probably prevent a direct correlation assessment in humans [Gómez-Bruton, et al., 2016]). However, rats that were swim-trained during growth have a greater overall bone mineral content and bone surface than the sedentary controls [McVeigh, et al., 2010] (but bone mineral density did not differ; and see [Bourrin, et al., 1992] for the opposite effect of endurance swim training on trabecular bone). It is noteworthy, however, that swim-trained animals do not necessarily experience a greater overall exercise intensity, as they were found to voluntarily run less outside the experimental exercise than control and running groups [McVeigh, et al., 2010]. Furthermore, bone structure at locations not directly influenced by locomotion, such as the cranial vault, does not seem to have been investigated in swim-trained animals.

The lack of a similarly detailed fossil record in other ancestrally terrestrial tetrapods adapted to an aquatic lifestyle prevented drawing such a conclusion in their respective cases, but a similar process might have occurred during the evolutionary history of at least some of them. BMI is probably the most widespread lifestyle adaptation among aquatic tetrapods. This suggests that genetic accommodation of a trait subject to physiological adjustment such as bone structure alteration might have played an important role in great evolutionary transitions, of which the secondary adaptations of tetrapods to an aquatic lifestyle is an iconic example.

Eli Amson, Guillaume Billet and Christian de Muizon. 2018. Evolutionary Adaptation to Aquatic Lifestyle in Extinct Sloths Can Lead to Systemic Alteration of Bone Structure.  Proc. R. Soc. B. 285: 20180270. DOI: 10.1098/rspb.2018.0270
The paper about the crazy pachyosteosclerosis in the skull of the marine sloth #Thalassocnus was published this morning in @RSocPublishing Proceedings B: …, to which I contributed my art. It was a pleasure to work with authors. #PaleoArt #SciArt

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