TY - JOUR A1 - Signore, Anthony V. A1 - Paijmans, Johanna L. A. A1 - Hofreiter, Michael A1 - Fago, Angela A1 - Weber, Roy E. A1 - Springer, Mark S. A1 - Campbell, Kevin L. T1 - Emergence of a chimeric globin pseudogene and increased Hemoglobin Oxygen Affinity Underlie the evolution of aquatic specializations in Sirenia JF - Molecular biology and evolution N2 - As limits on O2 availability during submergence impose severe constraints on aerobic respiration, the oxygen binding globin proteins of marine mammals are expected to have evolved under strong evolutionary pressures during their land-to-sea transition. Here, we address this question for the order Sirenia by retrieving, annotating, and performing detailed selection analyses on the globin repertoire of the extinct Steller’s sea cow (Hydrodamalis gigas), dugong (Dugong dugon), and Florida manatee (Trichechus manatus latirostris) in relation to their closest living terrestrial relatives (elephants and hyraxes). These analyses indicate most loci experienced elevated nucleotide substitution rates during their transition to a fully aquatic lifestyle. While most of these genes evolved under neutrality or strong purifying selection, the rate of nonsynonymous/synonymous replacements increased in two genes (Hbz-T1 and Hba-T1) that encode the α-type chains of hemoglobin (Hb) during each stage of life. Notably, the relaxed evolution of Hba-T1 is temporally coupled with the emergence of a chimeric pseudogene (Hba-T2/Hbq-ps) that contributed to the tandemly linked Hba-T1 of stem sirenians via interparalog gene conversion. Functional tests on recombinant Hb proteins from extant and ancestral sirenians further revealed that the molecular remodeling of Hba-T1 coincided with increased Hb–O2 affinity in early sirenians. Available evidence suggests that this trait evolved to maximize O2 extraction from finite lung stores and suppress tissue O2 offloading, thereby facilitating the low metabolic intensities of extant sirenians. In contrast, the derived reduction in Hb–O2 affinity in (sub)Arctic Steller’s sea cows is consistent with fueling increased thermogenesis by these once colossal marine herbivores. KW - ancient DNA KW - aquatic adaptation KW - gene conversion KW - hemoglobin KW - oxygen affinity KW - molecular evolution KW - myoglobin KW - neuroglobin KW - cytoglobin KW - pseudogene Y1 - 2019 U6 - https://doi.org/10.1093/molbev/msz044 SN - 0737-4038 SN - 1537-1719 VL - 36 IS - 6 SP - 1134 EP - 1147 PB - Oxford Univ. Press CY - Oxford ER - TY - JOUR A1 - Gaudry, Michael J. A1 - Jastroch, Martin A1 - Treberg, Jason R. A1 - Hofreiter, Michael A1 - Paijmans, Johanna L. A. A1 - Starrett, James A1 - Wales, Nathan A1 - Signore, Anthony V. A1 - Springer, Mark S. A1 - Campbell, Kevin L. T1 - Inactivation of thermogenic UCP1 as a historical contingency in multiple placental mammal clades JF - Science Advances Y1 - 2017 U6 - https://doi.org/10.1126/sciadv.1602878 SN - 2375-2548 VL - 3 SP - S337 EP - S337 PB - American Assoc. for the Advancement of Science CY - Washington ER - TY - JOUR A1 - Campbell, Kevin L. A1 - Hofreiter, Michael T1 - Resurrecting phenotypes from ancient DNA sequences: promises and perspectives JF - Canadian journal of zoology = Revue canadienne de zoologie N2 - Anatomical changes in extinct mammalian lineages over evolutionary time, such as the loss of fingers and teeth and the rapid increase in body size that accompanied the late Miocene dispersal of the progenitors of Steller's sea cows (Hydrodamalis gigas (Zimmermann, 1780)) into North Pacific waters and the convergent development of a thick pelage and accompanying reductions in ear and tail surface area of woolly mammoths (Mammuthus primigenius (Blumenbach, 1799)) and woolly rhinoceros (Coelodonta antiquitatis (Blumenbach, 1799)), are prime examples of adaptive evolution underlying the exploitation of new habitats. It is likely, however, that biochemical specializations adopted during these evolutionary transitions were of similar or even greater biological importance. As these "living" processes do not fossilize, direct information regarding the physiological attributes of extinct species has largely remained beyond the range of scientific inquiry. However, the ability to retrieve genomic sequences from ancient DNA samples, combined with ectopic expression systems, now permit the evolutionary origins and structural and functional properties of authentic prehistoric proteins to be examined in great detail. Exponential technical advances in ancient DNA retrieval, enrichment, and sequencing will soon permit targeted generation of complete genomes from hundreds of extinct species across the last one million years that, in combination with emerging in vitro expression, genome engineering, and cell differentiation techniques, promises to herald an exciting new trajectory of evolutionary research at the interface of biochemistry, genomics, palaeontology, and cell biology. KW - paleophysiology KW - ancient DNA KW - extinct species KW - adaptation KW - protein structure Y1 - 2015 U6 - https://doi.org/10.1139/cjz-2014-0337 SN - 0008-4301 SN - 1480-3283 VL - 93 IS - 9 SP - 701 EP - 710 PB - NRC Research Press CY - Ottawa ER - TY - JOUR A1 - Springer, Mark S. A1 - Signore, Anthony V. A1 - Paijmans, Johanna L. A. A1 - Velez-Juarbe, Jorge A1 - Domning, Daryl P. A1 - Bauer, Cameron E. A1 - He, Kai A1 - Crerar, Lorelei A1 - Campos, Paula F. A1 - Murphy, William J. A1 - Meredith, Robert W. A1 - Gatesy, John A1 - Willerslev, Eske A1 - MacPhee, Ross D. E. A1 - Hofreiter, Michael A1 - Campbell, Kevin L. T1 - Interordinal gene capture, the phylogenetic position of Steller's sea cow based on molecular and morphological data, and the macroevolutionary history of Sirenia JF - Molecular phylogenetics and evolution N2 - The recently extinct (ca. 1768) Steller's sea cow (Hydrodamalis gigas) was a large, edentulous North Pacific sirenian. The phylogenetic affinities of this taxon to other members of this clade, living and extinct, are uncertain based on previous morphological and molecular studies. We employed hybridization capture methods and second generation sequencing technology to obtain >30 kb of exon sequences from 26 nuclear genes for both H. gigas and Dugong dugon. We also obtained complete coding sequences for the tooth-related enamelin (ENAM) gene. Hybridization probes designed using dugong and manatee sequences were both highly effective in retrieving sequences from H. gigas (mean = 98.8% coverage), as were more divergent probes for regions of ENAM (99.0% coverage) that were designed exclusively from a proboscidean (African elephant) and a hyracoid (Cape hyrax). New sequences were combined with available sequences for representatives of all other afrotherian orders. We also expanded a previously published morphological matrix for living and fossil Sirenia by adding both new taxa and nine new postcranial characters. Maximum likelihood and parsimony analyses of the molecular data provide robust support for an association of H. gigas and D. dugon to the exclusion of living trichechids (manatees). Parsimony analyses of the morphological data also support the inclusion of H. gigas in Dugongidae with D. dugon and fossil dugongids. Timetree analyses based on calibration density approaches with hard- and soft-bounded constraints suggest that H. gigas and D. dugon diverged in the Oligocene and that crown sirenians last shared a common ancestor in the Eocene. The coding sequence for the ENAM gene in H. gigas does not contain frameshift mutations or stop codons, but there is a transversion mutation (AG to CG) in the acceptor splice site of intron 2. This disruption in the edentulous Steller's sea cow is consistent with previous studies that have documented inactivating mutations in tooth-specific loci of a variety of edentulous and enamelless vertebrates including birds, turtles, aardvarks, pangolins, xenarthrans, and baleen whales. Further, branch-site dN/dS analyses provide evidence for positive selection in ENAM on the stem dugongid branch where extensive tooth reduction occurred, followed by neutral evolution on the Hydrodamalis branch. Finally, we present a synthetic evolutionary tree for living and fossil sirenians showing several key innovations in the history of this clade including character state changes that parallel those that occurred in the evolutionary history of cetaceans. (C) 2015 Elsevier Inc. All rights reserved. Y1 - 2015 U6 - https://doi.org/10.1016/j.ympev.2015.05.022 SN - 1055-7903 SN - 1095-9513 VL - 91 SP - 178 EP - 193 PB - Elsevier CY - San Diego ER -