What Can We Infer About the Behavior of Extinct Sirenians?

Domning, Daryl P.

doi:10.1007/978-3-030-90742-6_1

Cited by 4 publications

(7 citation statements)

References 37 publications

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“…The larger the nerve spindle, the greater the sensitivity, which implies that anterior teeth likely require substantial vascularization and innervation. This pattern may be analogous to the thick anterior branch of extant sirenians that innervates their keratinized plate through shallow pits [35]. We propose that the anterior distribution of dorsal canaliculi in extant sirenians matches that of vestigial tooth loci, as suggested by our prenatal data (figure 1; electronic supplementary material, figure S4), and that dental innervation is retained after tooth resorption.…”

Section: Discussionsupporting

confidence: 68%

From teeth to pad: tooth loss and development of keratinous structures in sirenians

Hautier,

Gomes Rodrigues,

Ferreira-Cardoso

et al. 2023

Proc. R. Soc. B.

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Sirenians are a well-known example of morphological adaptation to a shallow-water grazing diet characterized by a modified feeding apparatus and orofacial morphology. Such adaptations were accompanied by an anterior tooth reduction associated with the development of keratinized pads, the evolution of which remains elusive. Among sirenians, the recently extinct Steller's sea cow represents a special case for being completely toothless. Here, we used μ-CT scans of sirenian crania to understand how motor-sensor systems associated with tooth innervation responded to innovations such as keratinized pads and continuous dental replacement. In addition, we surveyed nine genes associated with dental reduction for signatures of loss of function. Our results reveal how patterns of innervation changed with modifications of the dental formula, especially continuous replacement in manatees. Both our morphological and genomic data show that dental development was not completely lost in the edentulous Steller's sea cows. By tracing the phylogenetic history of tooth innervation, we illustrate the role of development in promoting the innervation of keratinized pads, similar to the secondary use of dental canals for innervating neomorphic keratinized structures in other tetrapod groups.

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Section: Discussionsupporting

confidence: 68%

From teeth to pad: tooth loss and development of keratinous structures in sirenians

Hautier,

Gomes Rodrigues,

Ferreira-Cardoso

et al. 2023

Proc. R. Soc. B.

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“…Although they became visibly thin during winter when "their spinous processes can be seen", Steller 9 noted that "(t)hese animals are very voracious, and eat incessantly" such that their stupendous stomach ("6 feet [1.8 m] long, 5 feet [1.5 m] wide") and enormous intestines-which measured a remarkable 5,958 inches (~151.5 m) from esophagus to anus, equivalent to "20½ times as long as the whole animal"-are constantly "stuffed with food and seaweed". These observations of a proportionally larger gut 41 are consistent with relatively high energetic requirements relative to extant manatees, which owing to their low metabolic intensity become cold stressed and die if chronically exposed to water temperatures below 15°C 48 . Reductions in insulative blubber thickness during the winter months would have compounded the rate of heat loss of these behemoths to sub-zero degree Celsius air and water, though may have been compensated for by arteriovenous anastomoses that regulated blood flow to the skin, and by countercurrent rete supplying the flippers and tail flukes, the latter of which are well developed in manatees and presumably other sirenians 49,50 .…”

Section: Paleophysiology Of Steller's Sea Cows the Posthumously Publi...supporting

confidence: 64%

“…The latter was presumably supplemented by a substantive heat increment arising from fermentation and other post-prandial processes 50 . Although the attendant increase in the rate of O2 consumption would have mandated a reduction in breath-hold endurance-likely reflecting the relatively short submergence times (4 to 5 minutes) observed by Steller 9 -our results suggests this may be been counteracted by an elevated Hb concentration (blood-O2 carrying capacity) that was potentially coupled to a greater lung volume 41 . Underwater foraging times were presumably further defended by key components of the dive reflex, namely bradycardia and peripheral vasoconstriction.…”

Section: Paleophysiology Of Steller's Sea Cows the Posthumously Publi...mentioning

confidence: 70%

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Evolution of an extreme hemoglobin phenotype contributed to the sub-Arctic specialization of extinct Steller’s sea cows

Signore

Fago

Weber

et al. 2022

Preprint

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The extinct Steller’s sea cow (Hydrodamalis gigas; †1768) was a whale-sized marine mammal that manifested profound morphological adjustments to exploit the harsh coastal climate of the North Pacific. Yet despite first-hand accounts of their biology, little is known regarding underlying physiological specializations to this extreme environment. Here, the adult-expressed hemoglobin (Hb) of this species is shown to harbor a fixed amino acid replacement at an otherwise invariant position (β/δ82Lys→Asn) that is predicted to profoundly alter multiple aspects of Hb function. To unravel the functional and evolutionary consequences of this substitution, we recombinantly synthesized Hb proteins of Steller’s sea cow, a H. gigas β/δ82Asn→Lys Hb mutant, the dugong (Dugong dugon), the last common dugongid ancestor, and the Florida manatee (Trichechus manatus). Our detailed functional analyses demonstrate that the Hb–O2 affinity of Steller’s sea cow evolved to become less affected by temperature compared to other sea cows. This phenotype presumably safeguarded O2 delivery to cool peripheral tissues and largely arises from a reduced intrinsic temperature sensitivity of the H. gigas protein owing to the β/δ82Lys→Asn substitution. We further confirm that this same exchange also underlies the secondary evolution of a reduced blood–O2 affinity phenotype that is moreover unresponsive to the intraerythrocytic allosteric effector 2,3-diphosphoglycerate. This radical modification, which augments O2 offloading by the protein, and presumably impacted maternal/fetal O2 exchange, is the first documented example of this phenotype among mammals. Notably, this replacement also increases protein solubility and is consistent with increased Hb concentrations within both the adult and pre-natal circulations that may have contributed to the elevated metabolic (thermoregulatory) requirements and fetal growth rates associated with their cold adaptation.

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“…However, any solubility-driven increases in red blood cell Hb concentration resulting from the β82Lys→Asn exchange would have allowed Steller’s sea cows to maintain an elevated rate of tissue O 2 delivery to meet their metabolic demands during extended underwater foraging intervals. Although this species was presumably unable to completely submerge ( Domning, 2022 ; Steller, 1751 ), this conjecture is corroborated by Steller’s account that, ‘they keep their heads always under water [foraging] , without regard to life and safety’ ( Steller, 1751 ). A reduced potential for Hb oxidation may also help explain Steller’s vexing observation that ‘what is remarkable, even in the hottest days it [the flesh] can be kept in the open air for a very long time without any bad odor, even though all full of worms [maggots]’ ( Steller, 1751 ).…”

Section: Resultsmentioning

confidence: 89%

Evolution of an extreme hemoglobin phenotype contributed to the sub-Arctic specialization of extinct Steller’s sea cows

Signore

Morrison

Brauner

et al. 2023

eLife

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The extinct Steller's sea cow (Hydrodamalis gigas; †1768) was a whale-sized marine mammal that manifested profound morphological specializations to exploit the harsh coastal climate of the North Pacific. Yet despite first-hand accounts of their biology, little is known regarding the physiological adjustments underlying their evolution to this environment. Here, the adult-expressed hemoglobin (Hb; a2β/δ2) of this sirenian is shown to harbor a fixed amino acid replacement at an otherwise invariant position (β/δ82Lys→Asn) that alters multiple aspects of Hb function. First, our functional characterization of recombinant sirenian Hb proteins demonstrate that the Hb-O2 affinity of this sub-Arctic species was less affected by temperature than those of living (sub)tropical sea cows. This phenotype presumably safeguarded O2 delivery to cool peripheral tissues and largely arises from a reduced intrinsic temperature sensitivity of the H. gigas protein. Additional experiments on H. gigas β/δ82Asn→Lys mutant Hb further reveal this exchange renders Steller's sea cow Hb unresponsive to the potent intraerythrocytic allosteric effector 2,3-diphosphoglycerate, a radical modification that is the first documented example of this phenotype among mammals. Notably, β/δ82Lys→Asn moreover underlies the secondary evolution of a reduced blood-O2 affinity phenotype that would have promoted heightened tissue and maternal/fetal O2 delivery. This conclusion is bolstered by analyses of two Steller's sea cow prenatal Hb proteins (Hb Gower I; z2e2 and HbF; a2g2) that suggest an exclusive embryonic stage expression pattern, and reveal uncommon replacements in H. gigas HbF (g38Thr→Ile and g101Glu→Asp) that increased Hb-O2 affinity relative to dugong HbF. Finally, the β/δ82Lys→Asn replacement of the adult/fetal protein is shown to increase protein solubility, which may have elevated red blood cell Hb content within both the adult and fetal circulations and contributed to meeting the elevated metabolic (thermoregulatory) requirements and fetal growth rates associated with this species cold adaptation.

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What Can We Infer About the Behavior of Extinct Sirenians?

Cited by 4 publications

References 37 publications

From teeth to pad: tooth loss and development of keratinous structures in sirenians

From teeth to pad: tooth loss and development of keratinous structures in sirenians

Evolution of an extreme hemoglobin phenotype contributed to the sub-Arctic specialization of extinct Steller’s sea cows

Evolution of an extreme hemoglobin phenotype contributed to the sub-Arctic specialization of extinct Steller’s sea cows

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