Unique bone microanatomy reveals ancestry of subterranean specializations in mammals

Abstract Acquiring a subterranean lifestyle entails a substantial shift for many aspects of terrestrial vertebrates’ biology. Although this lifestyle is associated with multiple instances of convergent evolution, the relative success of some subterranean lineages largely remains unexplained. Here, w...

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Main Authors: Eli Amson, Torsten M. Scheyer, Quentin Martinez, Achim H. Schwermann, Daisuke Koyabu, Kai He, Reinhard Ziegler
Format: Article
Language:English
Published: Oxford University Press 2022-12-01
Series:Evolution Letters
Subjects:
Online Access:https://doi.org/10.1002/evl3.303
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author Eli Amson
Torsten M. Scheyer
Quentin Martinez
Achim H. Schwermann
Daisuke Koyabu
Kai He
Reinhard Ziegler
author_facet Eli Amson
Torsten M. Scheyer
Quentin Martinez
Achim H. Schwermann
Daisuke Koyabu
Kai He
Reinhard Ziegler
author_sort Eli Amson
collection DOAJ
description Abstract Acquiring a subterranean lifestyle entails a substantial shift for many aspects of terrestrial vertebrates’ biology. Although this lifestyle is associated with multiple instances of convergent evolution, the relative success of some subterranean lineages largely remains unexplained. Here, we focus on the mammalian transitions to life underground, quantifying bone microanatomy through high‐resolution X‐ray tomography. The true moles stand out in this dataset. Examination of this family's bone histology reveals that the highly fossorial moles acquired a unique phenotype involving large amounts of compacted coarse cancellous bone. This phenotype exceeds the adaptive optimum seemingly shared by several other subterranean mammals and can be traced back to some of the first known members of the family. This remarkable microanatomy was acquired early in the history of the group and evolved faster than the gross morphology innovations of true moles’ forelimb. This echoes the pattern described for other lifestyle transitions, such as the acquisition of bone mass specializations in secondarily aquatic tetrapods. Highly plastic traits—such as those pertaining to bone structure—are hence involved in the early stages of different types of lifestyle transitions.
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spelling doaj.art-24148fa6c4a94ce4bda35820c7ab668b2023-09-03T08:02:49ZengOxford University PressEvolution Letters2056-37442022-12-016655256110.1002/evl3.303Unique bone microanatomy reveals ancestry of subterranean specializations in mammalsEli Amson0Torsten M. Scheyer1Quentin Martinez2Achim H. Schwermann3Daisuke Koyabu4Kai He5Reinhard Ziegler6Staatliches Museum für Naturkunde Stuttgart DE‐70191 Stuttgart GermanyPalaeontological Institute and Museum University of Zurich Zurich CH‐8006 SwitzerlandStaatliches Museum für Naturkunde Stuttgart DE‐70191 Stuttgart GermanyLWL‐Museum für Naturkunde Westfälisches Landesmuseum mit Planetarium DE‐48161 Münster GermanyResearch and Development Center for Precision Medicine University of Tsukuba Tsukuba 305‐8550 JapanKey Laboratory of Conservation and Application in Biodiversity of South China, School of Life Sciences Guangzhou University Guangzhou 510006 ChinaStaatliches Museum für Naturkunde Stuttgart DE‐70191 Stuttgart GermanyAbstract Acquiring a subterranean lifestyle entails a substantial shift for many aspects of terrestrial vertebrates’ biology. Although this lifestyle is associated with multiple instances of convergent evolution, the relative success of some subterranean lineages largely remains unexplained. Here, we focus on the mammalian transitions to life underground, quantifying bone microanatomy through high‐resolution X‐ray tomography. The true moles stand out in this dataset. Examination of this family's bone histology reveals that the highly fossorial moles acquired a unique phenotype involving large amounts of compacted coarse cancellous bone. This phenotype exceeds the adaptive optimum seemingly shared by several other subterranean mammals and can be traced back to some of the first known members of the family. This remarkable microanatomy was acquired early in the history of the group and evolved faster than the gross morphology innovations of true moles’ forelimb. This echoes the pattern described for other lifestyle transitions, such as the acquisition of bone mass specializations in secondarily aquatic tetrapods. Highly plastic traits—such as those pertaining to bone structure—are hence involved in the early stages of different types of lifestyle transitions.https://doi.org/10.1002/evl3.303Bone histologycompacted coarse cancellous boneosteogenesisphenotypic plasticitysubterranean mammalsTalpidae
spellingShingle Eli Amson
Torsten M. Scheyer
Quentin Martinez
Achim H. Schwermann
Daisuke Koyabu
Kai He
Reinhard Ziegler
Unique bone microanatomy reveals ancestry of subterranean specializations in mammals
Evolution Letters
Bone histology
compacted coarse cancellous bone
osteogenesis
phenotypic plasticity
subterranean mammals
Talpidae
title Unique bone microanatomy reveals ancestry of subterranean specializations in mammals
title_full Unique bone microanatomy reveals ancestry of subterranean specializations in mammals
title_fullStr Unique bone microanatomy reveals ancestry of subterranean specializations in mammals
title_full_unstemmed Unique bone microanatomy reveals ancestry of subterranean specializations in mammals
title_short Unique bone microanatomy reveals ancestry of subterranean specializations in mammals
title_sort unique bone microanatomy reveals ancestry of subterranean specializations in mammals
topic Bone histology
compacted coarse cancellous bone
osteogenesis
phenotypic plasticity
subterranean mammals
Talpidae
url https://doi.org/10.1002/evl3.303
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