Myoglobin primary structure reveals multiple convergent transitions to semi-aquatic life in the world's smallest mammalian divers
- Southern Medical University, China
- University of Manitoba, Canada
- University of Liverpool, United Kingdom
- University of Miyazaki, Japan
- National Museum of Nature and Science, Japan
- University of California, Riverside, United States
Abstract
The speciose mammalian order Eulipotyphla (moles, shrews, hedgehogs, solenodons) combines an unusual diversity of semi-aquatic, semi-fossorial, and fossorial forms that arose from terrestrial forbearers. However, our understanding of the ecomorphological pathways leading to these lifestyles has been confounded by a fragmentary fossil record, unresolved phylogenetic relationships, and potential morphological convergence, calling for novel approaches. The net surface charge of the oxygen-storing muscle protein myoglobin (ZMb), which can be readily determined from its primary structure, provides an objective target to address this question due to mechanistic linkages with myoglobin concentration. Here we generate a comprehensive 71 species molecular phylogeny that resolves previously intractable intra-family relationships and then ancestrally reconstruct ZMb evolution to identify ancient lifestyle transitions based on protein sequence alone. Our phylogenetically informed analyses confidently resolve fossorial habits having evolved twice in talpid moles and reveal five independent secondary aquatic transitions in the order housing the world's smallest endothermic divers.
Data availability
The newly obtained myoglobin sequences were deposited to GenBank under accession numbers MW456061 to MW456069 and MW473727- MW473769, and sequence alignments per gene were deposited to Dryad Digital Repository at https://doi.org/10.5061/dryad.brv15dv7q.
Article and author information
Author details
Funding
National Natural Science Foundation of China (31970389)
- Kai He
National Natural Science Foundation of China (31301869)
- Kai He
National Science Foundation (DEB-1457735)
- Mark S Springer
University of Manitoba (41342)
- Kevin L Campbell
Natural Sciences and Engineering Research Council of Canada (RGPIN/238838-2011)
- Kevin L Campbell
Natural Sciences and Engineering Research Council of Canada (RGPIN/6562-2016)
- Kevin L Campbell
Natural Sciences and Engineering Research Council of Canada (RGPIN/412336-2011)
- Kevin L Campbell
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Shigehiro Kuraku, National Institute of Genetics, Japan
Version history
- Received: January 22, 2021
- Accepted: May 4, 2021
- Accepted Manuscript published: May 5, 2021 (version 1)
- Version of Record published: June 15, 2021 (version 2)
- Version of Record updated: June 15, 2021 (version 3)
- Version of Record updated: June 16, 2021 (version 4)
Copyright
© 2021, He et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Myoglobin primary structure reveals multiple convergent transitions to semi-aquatic life in the world's smallest mammalian divers
eLife 10:e66797.
https://doi.org/10.7554/eLife.66797
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