Article

Interordinal gene capture, the phylogenetic position of Steller’s sea cow based on molecular and morphological data, and the macroevolutionary history of Sirenia

Authors:
To read the full-text of this research, you can request a copy directly from the authors.

No full-text available

Request Full-text Paper PDF

To read the full-text of this research,
you can request a copy directly from the authors.

... Concerning their systematic position, sirenians unequivocally belong to the endemic Afro-Arabian clades Afrotheria and Paenungulata (Murphy et al., 2001;Springer et al., 2003;Meredith et al., 2011), and based on recent large-scale genetic datasets, Sirenia is probably the extant sister taxon of the order Proboscidea (elephants) to the exclusion of Hyracoidea (hyraxes or dassies) (e.g., Heritage, Seiffert & Borths, 2021;Poulakakis & Stamatakis, 2010;Schull et al., 2022;Springer et al., 2015). Given that the oldest paenungulate fossils are from the Paleocene of Afro-Arabia (e.g., Gheerbrant, Bouya & Amaghzaz, 2012), it seems likely that the sirenian stem lineage arose on the same landmass during the very early Cenozoic. ...
... Conversely, the middle Eocene to Recent fossil record of sea cows is quite good, and provides evidence of times with much higher taxonomic and morphological diversity compared to the extant group-and notably so during the Oligo-Miocene interval (Domning, 2009). Sirenian fossils of Eocene age have evidenced several transitions in their highly derived anatomy including the loss of hindlimbs, modification of the forelimbs into "flippers", alterations of the vertebral column and dental formula, and the development of pachyosteosclerotic ribs (Domning, 2001a;Springer et al., 2015;Vélez-Juarbe & Wood, 2018). ...
... Most well-documented extinct sea cow species have already been scored for morphological characters, and these data have been employed several times to estimate relationships among living and fossil taxa using parsimony methods (e.g., Springer et al., 2015;Vélez-Juarbe & Wood, 2018). Abundant DNA evidence is also now available for all extant sirenian species (plus Steller's sea cow), but molecular and morphological data have never been assessed simultaneously using statistical phylogenetic methods. ...
Article
Full-text available
Molecular phylogenetic studies that have included sirenians from the genera Trichechus, Dugong, and Hydrodamalis have resolved their interrelationships but have yielded divergence age estimates that are problematically discordant. The ages of these lineage splits have profound implications for how to interpret the sirenian fossil record — including clade membership, biogeographic patterns, and correlations with Earth history events. In an effort to address these issues, here we present a total evidence phylogenetic analysis of Sirenia that includes living and fossil species and applies Bayesian tip-dating methods to estimate their interrelationships and divergence times. In addition to extant sirenians, our dataset includes 56 fossil species from 106 dated localities and numerous afrotherian outgroup taxa. Genetic, morphological, temporal, and biogeographic data are assessed simultaneously to bring all available evidence to bear on sirenian phylogeny. The resulting time-tree is then used for Bayesian geocoordinates reconstruction analysis, which models ancestral geographic areas at splits throughout the phylogeny, thereby allowing us to infer the direction and timing of dispersals. Our results suggest that Pan-Sirenia arose in North Africa during the latest Paleocene and that the Eocene evolution of stem sirenians was primarily situated in the Tethyan realm. In the late Eocene, some lineages moved into more northern European latitudes, an area that became the source region for a key trans-Atlantic dispersal towards the Caribbean and northern-adjacent west Atlantic. This event led to the phylogenetic and biogeographic founding of crown Sirenia with the Dugongidae-Trichechidae split occurring at the Eocene-Oligocene boundary (~33.9 Ma), temporally coincident with the onset of dropping global sea levels and temperatures. This region became the nexus of sirenian diversification and supported taxonomically-rich dugongid communities until the earliest Pliocene. The Dugonginae-Hydrodamalinae split occurred near Florida during the early Miocene (~21.2 Ma) and was followed by a west-bound dispersal that gave rise to the Pacific hydrodamalines. The late middle Miocene (~12.2 Ma) split of Dugong from all other dugongines also occurred near Florida and our analyses suggest that the Indo-Pacific distribution of modern dugongs is the result of a trans-Pacific dispersal. From at least the early Miocene, trichechid evolution was based entirely in South America, presumably within the Pebas Wetlands System. We infer that the eventual establishment of Amazon drainage into the South Atlantic allowed the dispersal of Trichechus out of South America no earlier than the mid-Pliocene. Our analyses provide a new temporal and biogeographic framework for understanding major events in sirenian evolution and their possible relationships to oceanographic and climatic changes. These hypotheses can be further tested with the recovery and integration of new fossil evidence. PeerJ 10:e13886 http://dx.doi.org/10.7717/peerj.13886
... Sirenia is a monophyletic order of mammals included in the superorder Afrotheria Stanhope et al., 1998, a clade well supported by molecular and genomic data (Amrine-Madsen et al., 2003;Murphy et al., 2004;Springer et al., 2015), which encompasses the extant placental mammals that originated in Africa: Tenrecoidea, Macroscelidea, Tubulidentata, Proboscidea, Hyracoidea and Sirenia (Tabuce et al., 2008). Within this superorder, the sirenians, proboscideans and hyracoideans form the clade Paenungulata Simpson, 1945, which is also broadly accepted on the basis of chromosomal studies (e.g. ...
... The character matrix created by Domning (1994) is the basis for almost all subsequent sirenian cladistic analyses, albeit with the addition of new characters or redefinitions of some of them (i.e. Bajpai & Domning, 1997;Domning & Aguilera, 2008;Vélez-Juarbe & Domning, 2014;Springer et al., 2015;Domning et al., 2017). The exception is the phylogenetic analysis by Sagne (2001a), in whose matrix more than half the characters are new. ...
... Protosirenids have been recovered both as a paraphyletic group (e.g. Domning, 1994;Springer et al., 2015;Balaguer & Alba, 2016) and as a monophyletic group (e.g. Velez-Juarbe et al., 2012;Vélez-Juarbe & Domning, 2014;Díaz-Berenguer et al., 2018), containing Trichechidae in some cases (e.g. ...
Article
The pan-sirenian Bauplan is conservative, probably owing to the constraints of adaptation to an aquatic lifestyle. Gathering morphological data from extinct forms is complex, resulting in poorly resolved phylogenies for stem pansirenians. Extant sirenians ossify the falx cerebri and the tentorium cerebelli, membranes of the dura mater of the brain attached to the parietal bone. Nevertheless, these ossifications are not present in some pan-sirenians. The basioccipital bone has received little attention in the literature except for establishing the relative age of individuals. Here, we present new cranial elements and a detailed description of the skull of Sobrarbesiren cardieli, a stem pan-sirenian from the Lutetian of Spain represented by eight individuals; we study its intraspecific variation and palaeoecological implications and explore the evolution of the endocranial structures and the basioccipital bone in pan-sirenians. Six new phylogenetic characters are added to the latest pan-sirenian dataset, resulting in a wellresolved topology where Sobrarbesiren is recovered close to the root, in a clade with Prototherium and Eotheroides aegyptiacum. The basioccipital bone and the ossified endocranial membranes have a phylogenetic signal, and the absence of such endocranial structures represents the plesiomorphic condition for pan-sirenians and is not diagnostic for the family Protosirenidae as previously believed.
... Our analysis of mitochondrial genomes from the 12 Steller's sea cows confirms that they are different individuals (section SM1). We mapped the recovered data to a new de novo-assembled draft genome of the dugong (Dugong dugon, originating from the Australian Museum; section SM2), which is the closest living relative of Steller's sea cow (7,8). To explore how genomic changes along the lineage to Steller's sea cow might explain their unique phenotypes, we generated a comparative dataset consisting of 4877 orthologous genes. ...
... To this end, we annotated our new dugong genome and a previously published Florida manatee genome [Trichechus manatus latirostris (9); University of California, Santa Cruz (UCSC) GCA_000243295.1] using the MAKER pipeline (10) and annotations from human, mouse, and elephant genomes (11). Because pseudogenization can shape phenotypes (7,12), we focused first on identification of inactivated genes and found two arachidonate lipoxygenases (ALOXE3 and ALOX12B) that have been inactivated via premature stop codons along the lineage to Steller's sea cow (section SM3). ...
... A shift in the energetic balance toward fat accumulation renders an increased capacity for fasting, which may have been key to both survival and long-distance movements of Steller's sea cows. Steller's sea cows lacked dentition (4,7), and their diet depended almost exclusively on kelp (28). Dragon kelp (Eularia fistulosa), the predominant surface canopy kelp species in the western North Pacific, is present only from about May through September (1), such that animals would have entered a fasting state for many months each year. ...
Article
Full-text available
Steller’s sea cow, an extinct sirenian and one of the largest Quaternary mammals, was described by Georg Steller in 1741 and eradicated by humans within 27 years. Here, we complement Steller’s descriptions with paleogenomic data from 12 individuals. We identified convergent evolution between Steller’s sea cow and cetaceans but not extant sirenians, suggesting a role of several genes in adaptation to cold aquatic (or marine) environments. Among these are inactivations of lipoxygenase genes, which in humans and mouse models cause ichthyosis, a skin disease characterized by a thick, hyperkeratotic epidermis that recapitulates Steller’s sea cows’ reportedly bark-like skin. We also found that Steller’s sea cows’ abundance was continuously declining for tens of thousands of years before their description, implying that environmental changes also contributed to their extinction.
... Sirenia is the sister-group of Proboscidea (Seiffert 2007;Springer et al. 2015;Sharko et al. 2019;de Souza et al. 2021), and both are grouped with the extinct clade Embrithopoda in Tethytheria (Paenungulata: Afrotheria), a group that originated from mammals that lived close to the Tethys Sea (Gheerbrant et al. 2018(Gheerbrant et al. , 2020. Stem sirenians differentiated from other tethytherians during the Paleocene, according to molecular dating analyses (Springer et al. 2015), but the first fossils appear in the early Eocene (Domning 2001b). ...
... Sirenia is the sister-group of Proboscidea (Seiffert 2007;Springer et al. 2015;Sharko et al. 2019;de Souza et al. 2021), and both are grouped with the extinct clade Embrithopoda in Tethytheria (Paenungulata: Afrotheria), a group that originated from mammals that lived close to the Tethys Sea (Gheerbrant et al. 2018(Gheerbrant et al. , 2020. Stem sirenians differentiated from other tethytherians during the Paleocene, according to molecular dating analyses (Springer et al. 2015), but the first fossils appear in the early Eocene (Domning 2001b). These Paleogene fossils illustrate the transition from amphibious to fully aquatic mammals (Domning 2001b;Zalmout and Gingerich 2012;Benoit et al. 2013). ...
... However, this taxonomic identification was only made "provisionally", as it was based on poor diagnostic traits (Toledo and Domning 1991). Recent comprehensive phylogenetic analyses of Sirenia have not recovered species of Dioplotherium as a monophyletic clade (Springer et al. 2015;Vélez-Juarbe and Wood 2019). Vélez-Juarbe and Wood (2019) mentioned that MPEG 63-V seems to be a new taxon, closely related to D. allisoni (Kilmer, 1965). ...
Article
Full-text available
Sirenians are placental mammals that comprise the extant manatees (Trichechus manatus, T. inunguis, and T. senegalensis) and dugongs (Dugong dugon). Since the late 19th century, cranial endocasts of extinct sirenians have been employed to study the neurological evolution of these mammals during the Cenozoic. Here, we analyzed the endocranial morphology of Dioplotherium cf. allisoni (MPEG 63–V) from the middle Miocene of South America to gain insights on brain morphology and encephalization. This sirenian was ca. three meters long, weighed approximately 800 kg, and inhabited coastal marine environments of northern Brazil 14.2 to 12.7 million years ago. The cranial endocast of this animal is lissencephalic, with two smooth hemispheres divided by a deep median sulcus and presenting a weakly marked Sylvian fissure separating frontal and temporal lobes. The olfactory bulbs are small (compared to Paleogene stem sirenians as well as terrestrial mammals), and the optic nerves were thin but long. The sphenorbital fissure and mandibular canal are bulky, indicating the presence of large sensory trigeminal components that innervate the facial region, which was presumably covered by perioral bristles and facial hairs used to feed and explore the environment. The encephalization quotient is 0.36 (Jerison’s EQ) and 0.34 (Manger’s EQ). Ancestral character state reconstruction suggests that, despite an overall slight increase in the degree of encephalization of sirenians, except for the extant Dugong dugon, other analyzed taxa present values below 0.5. This is in accordance with previous studies that have maintained that sirenians have a relatively small brain size compared to other tethytherians, perhaps associated with their lifestyle. Graphical Abstract
... senegalensis), that inhabit the warm waters of the Atlantic, Pacific, and Indian oceans. The dugong is the closest species to H. gigas as has been shown in previous studies 8,9 . ...
... Surprisingly, the leptin (LEP) gene was under the positive selection in H. gigas as well as in other Pinnipedia and Cetacea species 13 . The toothrelated enamelin (ENAM) has been found as a gene that evolved under positive selection as also described previously 9 . GO analysis for genes with stricter dN/dS ratio (above three) categories were also found to be related to the defense response (GO:0006952) or GO:0048018-receptor ligand activity (Supplementary Table 6). ...
... Phylogenetic analysis based on mitochondrial and nuclear genomes. Phylogenetic reconstruction based on coding sequences (CDS) of mtDNA showed the "classical" topology for modern and extinct species from Tethytheria 8,9 . Proboscidea and Sirenia specimens have proper clustering according to their phylogenetic position and our H. gigas specimen as well as previously published 8 , located in one cluster. ...
Article
Full-text available
Anthropogenic activity is the top factor directly related to the extinction of several animal species. The last Steller's sea cow (Hydrodamalis gigas) population on the Commander Islands (Russia) was wiped out in the second half of the 18 th century due to sailors and fur traders hunting it for the meat and fat. However, new data suggests that the extinction process of this species began much earlier. Here, we present a nuclear de novo assembled genome of H. gigas with a 25.4× depth coverage. Our results demonstrate that the heterozygosity of the last population of this animal is low and comparable to the last woolly mammoth population that inhabited Wrangel Island 4000 years ago. Besides, as a matter of consideration, our findings also demonstrate that the extinction of this marine mammal starts along the North Pacific coastal line much earlier than the first Paleolithic humans arrived in the Bering sea region.
... First, and most substantially, our crown age for Sirenia (manatees, dugongs, and sea cows; approximately 13 Ma: 7.0, 22.6) is reconstructed as younger than the minimum age constraint of 41.3 Ma given in Foley and colleagues [63] and, thus, "undead" for at least 20 Ma. We reconstruct the sirenian stem divergence at approximately 54 Ma (41.5, 67.3), which implies a long stem to the crown divergence of Dugong, Trichechus, and Hydrodamalis-rather than the perspective in which those three modern genera are deeply divergent from each other [60,63,135]. This issue hinges on the acceptance of the fossils Halitherium and Eotheroides as crown sirenians because they form the minimum age constraint in previous studies. ...
... This issue hinges on the acceptance of the fossils Halitherium and Eotheroides as crown sirenians because they form the minimum age constraint in previous studies. The most recent cladistic analysis of Springer and colleagues [135] found 40% BS for the placement of Halitherium and Eotheroides inside of crown Sirenia (stem taxa of the Dugong-Hydrodamalis clade, to the exclusion of Trichechus [135]). Based on our criteria for fossil inclusion [57], these fossils were placed too tenuously for use as Sirenia crown constraints. ...
... This issue hinges on the acceptance of the fossils Halitherium and Eotheroides as crown sirenians because they form the minimum age constraint in previous studies. The most recent cladistic analysis of Springer and colleagues [135] found 40% BS for the placement of Halitherium and Eotheroides inside of crown Sirenia (stem taxa of the Dugong-Hydrodamalis clade, to the exclusion of Trichechus [135]). Based on our criteria for fossil inclusion [57], these fossils were placed too tenuously for use as Sirenia crown constraints. ...
Article
Full-text available
Big, time-scaled phylogenies are fundamental to connecting evolutionary processes to modern biodiversity patterns. Yet inferring reliable phylogenetic trees for thousands of species involves numerous trade-offs that have limited their utility to comparative biologists. To establish a robust evolutionary timescale for all approximately 6,000 living species of mammals, we developed credible sets of trees that capture root-to-tip uncertainty in topology and divergence times. Our “backbone-and-patch” approach to tree building applies a newly assembled 31-gene supermatrix to two levels of Bayesian inference: (1) backbone relationships and ages among major lineages, using fossil node or tip dating, and (2) species-level “patch” phylogenies with nonoverlapping in-groups that each correspond to one representative lineage in the backbone. Species unsampled for DNA are either excluded (“DNA-only” trees) or imputed within taxonomic constraints using branch lengths drawn from local birth–death models (“completed” trees). Joining time-scaled patches to backbones results in species-level trees of extant Mammalia with all branches estimated under the same modeling framework, thereby facilitating rate comparisons among lineages as disparate as marsupials and placentals. We compare our phylogenetic trees to previous estimates of mammal-wide phylogeny and divergence times, finding that (1) node ages are broadly concordant among studies, and (2) recent (tip-level) rates of speciation are estimated more accurately in our study than in previous “supertree” approaches, in which unresolved nodes led to branch-length artifacts. Credible sets of mammalian phylogenetic history are now available for download at http://vertlife.org/phylosubsets, enabling investigations of long-standing questions in comparative biology.
... The earliest known fossil sirenians (prorastomids, e.g., Prorastomus and Pezosiren) are from the middle Eocene ($47 Ma) and were fully capable of terrestrial locomotion (Domning 2001). However, they exhibited a number of aquatic specializations that suggest they spent appreciable time foraging underwater, such as retracted nares to aid respiration while breaching water, a jaw modified for bottom feeding, and a slender body with prominent tail that allowed locomotion via dorsoventral spinal undulation combined with hindlimb thrusts (Domning 2001;Springer et al. 2015). These features are more pronounced in the next phase of sirenian evolution (protosirenids, e.g., Protosiren), which show further streamlining of the body, reduced limbs, and an enlarged tail that implies a mostly aquatic lifestyle, but likely capable of dragging itself short distances on land (Domning and Gingerich 1994). ...
... We obtained complete coding sequences of Mb, Ngb, Cygb, and the full complement of aand b-globin genes from two dugongs and three $1,000 year old Steller's sea cow specimens using microarray hybridization enrichment coupled with Illumina sequencing. Details outlining the construction of DNA libraries, target enrichment, Illumina sequencing, and sequence assembly are described elsewhere (Springer et al. 2015). Briefly, barcoded DNA libraries suitable for Illumina sequencing were prepared from dugong and Steller's sea cow extracts, and subsequently enriched for globin sequences using Agilent SureSelect Capture arrays primarily designed based on African elephant sequence information. ...
... The coding sequences of the various globin genes were deduced from these assemblies and used in subsequent analyses. DNA damage artifacts (C!T and G!A) in the Steller's sea cow assemblies were identified and corrected following Springer et al. (2015). ...
Article
Full-text available
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 non-synonymous/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 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. By 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.
... For the phylogenetic analysis, we used the character-state matrix of Springer et al. (2015), with the addition of the following taxa: Callistosiren boriquensis, Dioplotherium cf. D. allisoni (MPEG-63 V), Dusisiren dewana Takahashi, Domning, and Saito, 1986, Dusisiren reinharti Domning, 1978, Eosiren imenti Domning, Gingerich, Simons, and Ankel-Simons, 1994, E. libyca Andrews, 1902, Eotheroides clavigerum Zalmout and Gingerich, 2012, Eo. lambondrano Samonds, Zalmout, Irwin, Krause, Rogers, and Raharivony, 2009, Eo. sandersi Zalmout and Gingerich, 2012, Kaupitherium bronni (Krauss, 1858, K. gruelli, Lentiarenium cristolii (Fitzinger, 1842), Libysiren sickenbergi Domning, Heal, andSorbi, 2017, Metaxytherium subapenninum (Bruno, 1839), Potamosiren magdalenensis Reinhart, 1951, Prototherium ausetanum Balaguer and Alba, 2016, P. intermedium Bizzotto, 1983, P. veronense (Zigno, 1875, Ribodon limbatus Ameghino, 1883, and Sobrarbesiren cardieli Díaz-Berenguer, Badiola, Moreno-Azanza, and Canudo, 2018. ...
... Scoring for L. cristolii was modified from earlier analyses (e.g., Velez-Juarbe and Domning, 2014a) based on the redescription by Voss et al. (2016). The matrix was analyzed using PAUP* (version 4.0a [build 161]) (Swofford, 2017), via a heuristic search using the tree bisection-reconnection algorithm, and using a backbone constraint based on the molecular tree from Springer et al. (2015). Statistical support was obtained by doing 1000 bootstrap replicates. ...
... Furthermore, our analysis recovered, for the first time, a monophyletic relationship between Bharatisiren kachchhensis and B. indica. Previous analyses showed Bharatisiren to be either para-or polyphyletic ( Velez-Juarbe et al., 2012a;Springer et al., 2015;Velez-Juarbe and Domning, 2015). Bharatisiren spp. ...
Article
Herein, we describe a new early Miocene dugongine from marine deposits of the Culebra Cut (Gaillard Cut) of the Panama Canal. The new taxon, Culebratherium alemani, gen. et sp. nov., represents one of the few records of late Aquitanian–early Burdigalian sirenians and the oldest sirenian from Central America. A phylogenetic analysis places Culebratherium in a clade with Dioplotherium cf. D. allisoni (Miocene of Brazil), Dioplotherium allisoni (Miocene of Baja California Sur, Mexico, and California, U.S.A.), and Dioplotherium sp. (Pliocene of Yucatan, Mexico). Similar to these taxa, Culebratherium is characterized by the presence of large incisor tusks, a premaxillary symphysis without a boss, a premaxilla-frontal suture forming a butt joint, and a moderately downturned rostrum. In addition, Culebratherium exhibits prominent occipital-cervical attachment sites for enlarged neck musculature. These features taken together are interpreted as adaptations for uprooting large, deeply buried seagrass rhizomes. Other dugongines with similar, yet convergent, dental and facial adaptations are known from earlier or coeval deposits in Puerto Rico, Florida, South Carolina, California, Baja California Sur, Brazil, and India and were constituents of sympatric paleocommunities of sirenians. Only fragmentary evidence of a second smaller and unidentifiable sirenian species is known from the Culebra Formation, but future discoveries may reveal a similar sympatric paleocommunity during the early Miocene of Panama. Finally, we used the results of the phylogenetic analysis to propose the new clade Pan-Sirenia as the most inclusive group consisting of stem and crown groups and redefine the Sirenia, Dugongidae, and Dugonginae clades.
... Numerous morphological studies have demonstrated the similarity between the Pacific sirenian species H. gigas and D. dugon [5,6], whereas the molecular genetic data for Steller's sea cow are limited and demonstrate the phylogenetic relationships within the Sirenia order and its closest relatives based on immunological data [7], cytB mitochondrial gene fragments [8] and 30 kb of exon sequences from 26 nuclear genes [9]. Phylogenetic analysis based on molecular data provides support for the inclusion of H. gigas with D. dugon in the Family Dugongidae and allow construction of the phylogeny for the Sirenia and Tethytheria [9,10]. ...
... Numerous morphological studies have demonstrated the similarity between the Pacific sirenian species H. gigas and D. dugon [5,6], whereas the molecular genetic data for Steller's sea cow are limited and demonstrate the phylogenetic relationships within the Sirenia order and its closest relatives based on immunological data [7], cytB mitochondrial gene fragments [8] and 30 kb of exon sequences from 26 nuclear genes [9]. Phylogenetic analysis based on molecular data provides support for the inclusion of H. gigas with D. dugon in the Family Dugongidae and allow construction of the phylogeny for the Sirenia and Tethytheria [9,10]. In this paper, we present the first complete sequence of the Steller's sea cow mitogenome, its characteristics, and a phylogenetic analysis based on complete mitochondrial genomes of Tethytheria. ...
... Phylogenetic analysis based on the whole mitochondrial DNA of modern Tethytheria and rooted by the rock hyrax or rock badger (P. capensis) presents "traditional" topology which has been previously described [9,10]. ...
Article
The Steller's sea cow – Hydrodamalis gigas (Dugongidae: Sirenia) – is an extinct herbivorous marine mammal which inhabited the North Pacific Ocean during the Pleistocene and Holocene. H. gigas was the largest member of the Sirenia order and disappeared in the middle of the 18th century. Here, we present the complete sequence of the mitochondrial genome of this extinct animal. The Steller's sea cow mitochondrial DNA (mtDNA) is 16,872 base pairs (bp) in length and contains a set of mitochondrial genes typical for mammals. Phylogenetic analysis based on complete mitochondrial genomes of the sirenian species allows accurate assessment of the degree of their mitogenomic diversification during millions of years of evolution.
... (Ch. Character state following the descriptions and numbering sequence of Domning 23 as updated by Vélez-Juarbe et al. 24 and Springer et al. 1 (e.g., Ch. 102 (0) refers to state 0 of character 102)): sirenian, based on the following synapomorphies: retracted and enlarged external nares (Ch. 8 (1)); premaxilla contacts the frontals (Ch. 9 (1)); and a P1-5, M1-3 postcanine dental formula (Ch. ...
... It is distinguished from "Halitherium" taulannense in having I3 present, a zygomatic-orbital bridge of the maxilla elevated more than 1 cm above the alveolar margin (Ch. 11 (1)) and an external auditory meatus that is narrow and slit-like (Ch. 82 (0)). ...
... The resulting dataset includes a total of 50 taxa, including 48 sirenians with the proboscidean Phosphatherium escuilliei Gheerbrant et al. 34 , plus the multitaxic Elephantidae as the outgroup (Supplementary Information Data matrix 1). Following Springer et al. 1 , of the total of 74 parsimony-informative characters scored, characters 1,6,7,16,31,36,38,44,49,50,51,60,65,67,68,70 and 71 were treated as additive (ordered) characters, whereas relative steps between states of characters 10, 27, and 47 are defined by step matrices. The name Halitherium schinzii was replaced by Kaupitherium gruelli, following Voss et al. 35 . ...
Article
Full-text available
Sirenians are the only extant herbivorous mammals fully adapted to an aquatic lifestyle. They originated in Africa during the Paleocene from an undetermined clade of afrotherian mammals, and by the end of the Eocene they were widely distributed across the tropical latitudes. Here we introduce Sobrarbesiren cardieli gen. et sp. nov. It is the first adequately-known quadrupedal sirenian from Eurasia and the oldest record of this clade from western Europe. Fossils have been recovered from the middle Lutetian (SBZ15) site of Castejón de Sobrarbe-41 (Huesca, Spain), and comprise many cranial and postcranial remains, including pelvic girdle and hind limb bones, from at least six sirenian individuals of different ontogenetic stages. Sobrarbesiren shows a suite of characters previously considered synapomorphies of different clades of derived sirenians, such as the presence of the processus retroversus of the squamosal and the pterygoid fossa, combined with ancestral characters such as the presence of an alisphenoid canal, a permanent P5, at least two sacral vertebrae, a primitive pelvis and functional femora and fibulae. Sobrarbesiren is recovered as the sister taxon of Dugongidae and represents a transitional stage of adaptation to aquatic life between the amphibious quadrupedal prorastomids and the aquatic quadrupedal protosirenids.
... 4.0a; Swofford, 2020); all characters were treated as unordered and of equal weight. A heuristic search of 1000 replicates was performed using the tree bisection-reconnection (TBR) algorithm and using a backbone constraint tree based on the molecular phylogeny from Springer et al. (2015). Bootstrap values were obtained by performing 1000 replicates (Supplementary material S2). ...
... This dietary shift in hydrodamalines, from the more fibrous seagrasses to the softer kelps higher up in the water column is reflected in the reduction of rostral deflection and complete loss of adult dentition in Hydrodamalis spp. (Domning, 1978;Domning and Furusawa, 1994;Springer et al., 2015). ...
Article
Potamosiren magdalenensis Reinhart, is an extinct species of manatee (Sirenia, Trichechidae, Trichechinae), which has only been recorded for the middle Miocene Honda Group, in the La Venta area (Huila Department, Colombia). A new specimen referable to Potamosiren cf. P. magdalenensis is reported herein, collected from the early Miocene Barzalosa Formation. This unit crops out in the Pubenza locality, at the Tocaima municipality of the Cundinamarca Department, Colombia. The material described here represents the first evidence of a mammal from the Barzalosa Formation, the earliest record of Potamosiren so far reported and one of the only two trichechid records for the early Miocene of South America. The new specimen adds to a small but growing record of extinct trichechids, increasing the fossil record of this group in South America and allowing us to further explore their evolutionary history. The early Miocene appearance of trichechines coincides geographically and temporally with the onset of the Pebas Mega-Wetland System, which likely provided favourable conditions for the invasion of freshwater ecosystems of this group of fully aquatic mammals. Finally, the depositional environments represented by the Barzalosa Fm and a review of the fossil record of trichechines further support the notion that manatees have had a close association with freshwater systems since early in their evolutionary history, and that reinvasion of marine ecosystems did not occur until much later.
... The dugong mtDNA control region sequences were aligned with GENBANK reference sequences from all closely related species in order to estimate approximate times of divergence between lineages, based on known calibrated fossil divergence dates [54]. Bayesian analyses resulted in estimates of divergence times for each lineage (Fig 3 and S1 Table). ...
... In the absence of reliable rate estimates, we require a divergence dating analysis that incorporates reliable estimates of divergences among closely related species. This information now exists thanks to the comprehensive analysis of fossil, morphological and molecular data of the Sirenian lineage provided by Springer et al [54], although it is necessary to go back more than 20 MY to the nearest species divergence (from Steller's sea cow, H. gigas). Our new mtDNA control region sequence from the extinct Steller's sea cow enabled a robust dated phylogenetic analysis of the Sirenian lineage. ...
Article
Full-text available
We investigated the phylogeography of the dugong (Dugong dugon) across its original range using museum material from 14 natural history museum and university collections. The mitochondrial DNA control region was successfully amplified from samples of bone or tooth powder from 162 individuals. These samples range from 1827 to 1996 and span the historical distribution range of the dugong. We were able to successfully amplify overlapping fragments of the D-loop region of the mitochondrial DNA (mtDNA) resulting in sequences of a 355 bp fragment for 162 individuals for the final analyses. This included a new sequence (189 bp) from a previously unidentified piece of skin of the extinct Steller's sea cow (Hydrodamalis gigas), as an outgroup. The resulting dugong sequences match those from previous studies of dugongs from Australia and Indonesia, but revealed several new and divergent mtDNA lineages in the Indian Ocean. One mtDNA lineage includes most specimens from the Western Indian Ocean, with another distinct lineage isolated to nearby Madagascar and Comores. There is little geographic structuring detectable among other populations in the Western Indian Ocean and all populations from that region appear to have historically contained comparatively low levels of genetic diversity. The genetic diversity of several Indian Ocean samples collected after 1950 was lower than that of the samples collected earlier from similar locations, a result coincident with the anecdotal reductions in population size. The new lineages and potential loss of diversity highlight the particular conservation importance and vulnerability of dugong populations in the Western Indian Ocean.
... All analyzed afrotherian share the presumptive translocation of DR loci (Figure 2); this translocation was not found in other boreoeutherian or xenarthran genomes analyzed here (data not shown). Other presumptive chromosomal rearrangements were (39) and presumptive evolutionary events leading to current afrotherian MHC structure. On the left the human class II MHC region is depicted as an outgroup and model of the mammalian genome organization. ...
... A better resolution of orthology among translocated loci would probably be achieved using less divergent taxa, since the clades analyzed here diverged early in afrotherian evolution. For instance, one of the closest pair of species studied here is the African elephant and the Florida manatee, with estimates of 70∼65 million years of divergence (39,59). The non-translocated DRA from manatee indeed clustered with the non-translocated elephant homolog, but the lack of other sequences (i.e., translocated Trma-DRA and non-translocated Trma-DRB) presently hinders a more comprehensive analysis. ...
Article
Full-text available
Sirenians share with cetaceans and pinnipeds several convergent traits selected for the aquatic lifestyle. Living in water poses new challenges not only for locomotion and feeding but also for combating new pathogens, which may render the immune system one of the best tools aquatic mammals have for dealing with aquatic microbial threats. So far, only cetaceans have had their class II Major Histocompatibility Complex (MHC) organization characterized, despite the importance of MHC genes for adaptive immune responses. This study aims to characterize the organization of the marine mammal class II MHC using publicly available genomes. We located class II sequences in the genomes of one sirenian, four pinnipeds and eight cetaceans using NCBI-BLAST and reannotated the sequences using local BLAST search with exon and intron libraries. Scaffolds containing class II sequences were compared using dotplot analysis and introns were used for phylogenetic analysis. The manatee class II region shares overall synteny with other mammals, however most DR loci were translocated from the canonical location, past the extended class II region. Detailed analysis of the genomes of closely related taxa revealed that this presumed translocation is shared with all other living afrotherians. Other presumptive chromosome rearrangements in Afrotheria are the deletion of DQ loci in Afrosoricida and deletion of DP in E. telfairi. Pinnipeds share the main features of dog MHC: lack of a functional pair of DPA/DPB genes and inverted DRB locus between DQ and DO subregions. All cetaceans share the Cetartiodactyla inversion separating class II genes into two subregions: class IIa, with DR and DQ genes, and class IIb, with non-classic genes and a DRB pseudogene. These results point to three distinct and unheralded class II MHC structures in marine mammals: one canonical organization but lacking DP genes in pinnipeds; one bearing an inversion separating IIa and IIb subregions lacking DP genes found in cetaceans; and one with a translocation separating the most diverse class II gene from the MHC found in afrotherians and presumptive functional DR, DQ, and DP genes. Future functional research will reveal how these aquatic mammals cope with pathogen pressures with these divergent MHC organizations.
... Regulatory elements of seven additional eutherians were also retrieved by hybridization capture and next-generation sequencing techniques. Briefly, UCP1 enhancers, PRRs, and basal promoters of four rhinoceroses (black rhinoceros: Diceros bicornis, Indian rhinoceros: Rhinoceros unicornis, Sumatran rhinoceros; Dicerorhinus sumatrensis, and woolly rhinoceros; Coelodonta antiquitatis), one tapir (Malayan tapir; Tapirus indicus), and two sirenians (dugong; Dugong dugon, and Steller's sea cow; Hydrodamalis gigas), were targeted using hybridization capture and next-generation sequencing techniques (Springer et al., 2015;Gaudry et al., 2017). Barcoded rhinoceros DNA libraries were constructed using NEBNext Fast DNA Library Prep Set for Ion Torrent and NEBNext DNA Library Prep Master Mix Set for 454 kits (New England Biolabs; Ipswich, Massachusetts, USA) and target-enriched using MyBaits (Mycroarray; Ann Arbor, Michigan, USA) 120mer RNA probes designed to capture UCP1 exons and regulatory elements based on the orthologous sequences of the white rhinoceros (Ceratotherium simum) genome. ...
... Indeed, other pseudogenized genes (e.g., AMBN, AMEL, ENAM, and MMP20) in baleen whales and the Steller's sea cow (H. gigas) show exceptionally low rates of molecular decay (Meredith et al., 2011;Springer et al., 2015). Consequently the high (>80%) enhancer sequence identity shared between UCP1-pseudogenized species (horse, minke whale, pig, baiji, bowhead whale, African elephant, and manatee) and humans is not surprising. ...
Article
Full-text available
Uncoupling protein 1 (UCP1) permits non-shivering thermogenesis (NST) when highly expressed in brown adipose tissue (BAT) mitochondria. Exclusive to placental mammals, BAT has commonly been regarded to be advantageous for thermoregulation in hibernators, small-bodied species, and the neonates of larger species. While numerous regulatory control motifs associated with UCP1 transcription have been proposed for murid rodents, it remains unclear whether these are conserved across the eutherian mammal phylogeny and hence essential for UCP1 expression. To address this shortcoming, we conducted a broad comparative survey of putative UCP1 transcriptional regulatory elements in 139 mammals (135 eutherians). We find no evidence for presence of a UCP1 enhancer in monotremes and marsupials, supporting the hypothesis that this control region evolved in a stem eutherian ancestor. We additionally reveal that several putative promoter elements (e.g., CRE-4, CCAAT) identified in murid rodents are not conserved among BAT-expressing eutherians, and together with the putative regulatory region (PRR) and CpG island do not appear to be crucial for UCP1 expression. The specificity and importance of the upTRE, dnTRE, URE1, CRE-2, RARE-2, NBRE, BRE-1, and BRE-2 enhancer elements first described from rats and mice are moreover uncertain as these motifs differ substantially—but generally remain highly conserved—in other BAT-expressing eutherians. Other UCP1 enhancer motifs (CRE-3, PPRE, and RARE-3) as well as the TATA box are also highly conserved in nearly all eutherian lineages with an intact UCP1. While these transcriptional regulatory motifs are generally also maintained in species where this gene is pseudogenized, the loss or degeneration of key basal promoter (e.g., TATA box) and enhancer elements in other UCP1-lacking lineages make it unlikely that the enhancer region is pleiotropic (i.e., co-regulates additional genes). Importantly, differential losses of (or mutations within) putative regulatory elements among the eutherian lineages with an intact UCP1 suggests that the transcriptional control of gene expression is not highly conserved in this mammalian clade.
... Shotgun sequencing of such DNA libraries then becomes inefficient in terms of associated costs necessary to attain coverage levels allowing for reconstructing specific barcode loci. Target gene capture as alternative can be an additional costly and time-intensive step, especially when a second round of capture is performed which has been shown to increase sequencing success (e.g., Li et al., 2013Li et al., , 2015Templeton et al., 2013;Springer et al., 2015;Paijmans et al., 2016). In an effort to increase efficiency and decrease overall costs for target capture of sample specific barcode markers in museum specimens, we report here on the design and successful application of an RNA bait set targeting taxonomically useful barcode markers in a variety of natural history collection samples of different phyla. ...
Article
Full-text available
A growing number of publications presenting results from sequencing natural history collection specimens reflect the importance of DNA sequence information from such samples. Ancient DNA extraction and library preparation methods in combination with target gene capture are a way of unlocking archival DNA, including from formalin-fixed wet-collection material. Here we report on an experiment, in which we used an RNA bait set containing baits from a wide taxonomic range of species for DNA hybridisation capture of nuclear and mitochondrial targets for analysing natural history collection specimens. The bait set used consists of 2,492 mitochondrial and 530 nuclear RNA baits and comprises specific barcode loci of diverse animal groups including both invertebrates and vertebrates. The baits allowed to capture DNA sequence information of target barcode loci from 84% of the 37 samples tested, with nuclear markers being captured more frequently and consensus sequences of these being more complete compared to mitochondrial markers. Samples from dry material had a higher rate of success than wet-collection specimens, although target sequence information could be captured from 50% of formalin-fixed samples. Our study illustrates how efforts to obtain barcode sequence information from natural history collection specimens may be combined and are a way of implementing barcoding inventories of scientific collection material.
... Cooper et al. 2014). More recently, Tethytheria and additional placental groups were recovered within the clade Afrotheria (Springer et al. 1997(Springer et al. , 2015Murphy et al. 2001aMurphy et al. , b, 2021, a group that includes Afrosoricida (e.g. tenrecs, golden moles), Macroscelidea (elephant shrews), Tubulidentata (aardvarks), Proboscidea (elephants), Sirenia, and Hyracoidea (hyraxes). ...
Chapter
Sirenians represent a striking group of quadruped mammals that are adapted to marine life. There are four extant species of sirenians (three sea cows and the dugong) but the fossil record, which extends from the early Eocene, shows a much richer diversity, and global distribution. Sirenians belong to the crown-group Sirenia and their closest extinct relatives belong to Pan-Sirenia. Sirenia is nested within Tethytheria, along with elephants and desmostylids, and Tethytheria belongs to the larger mammalian clade Afrotheria. The paleoneurology of Pan-Sirenia and Sirenia is based on anatomical descriptions of approximately two dozen natural and digital cranial endocasts and a couple of bony labyrinth endocasts. Sirenian brains are characterized by lissencephalic cerebral hemispheres, reduced olfactory system, reduction in the optic nerves, presence of a large trigeminal nerve and associated components, and thick meninges of the central nervous system. In contrast to other modern paenungulates, which include the gyrencephalic and large-brained elephants, sirenians have lissencephalic brains whose components are linearly arranged, and small relative brain sizes (EQs). Future work is needed to further incorporate the anatomical diversity of sirenian cranial endocasts into phylogenetic character matrices and to increase our knowledge about the inner ear evolution of the group.
... Tooth development is a complex process that involves hundreds of genes, most of which are pleiotropic and also perform essential functions outside of odontogenesis (Thesleff 2006). However, ten genes have been shown to be toothspecific with respect to their crucial functions that are maintained by natural selection (Deméré et al. 2008;McKnight and Fisher 2009;Meredith et al. 2009Meredith et al. , 2011Meredith et al. , 2013Meredith et al. , 2014Kawasaki et al. 2014Kawasaki et al. , 2020Gasse et al. 2015;Springer et al. 2015Springer et al. , 2016Springer et al. , 2019Mu et al. 2021) ( Table 2). All of these genes have become pseudogenized in one or more clades of mammals that have lost their postnatal teeth (baleen whales, anteaters, pangolins, Steller's sea cow) or have lost the enamel on their teeth (armadillos, sloths, aardvarks, pygmy and dwarf sperm whales). ...
Article
Full-text available
The transition in Mysticeti (Cetacea) from capture of individual prey using teeth to bulk filtering batches of small prey using baleen ranks among the most dramatic evolutionary transformations in mammalian history. We review phylogenetic work on the homology of mysticete feeding structures from anatomical, ontogenetic, and genomic perspectives. Six characters with key functional significance for filter-feeding behavior are mapped to cladograms based on 11 morphological datasets to reconstruct evolutionary change across the teeth-to-baleen transition. This comparative summary within a common parsimony framework reveals extensive conflicts among independent systematic efforts but also broad support for the newly named clade Kinetomenta (Aetiocetidae + Chaeomysticeti). Complementary anatomical studies using CT scans and ontogenetic series hint at commonalities between the developmental programs for teeth and baleen, lending further support for a 'transitional chimaeric feeder' scenario that best explains current evidence on the transition to filter feeding. For some extant mysticetes, the ontogenetic sequence in fetal specimens recapitulates the inferred evolutionary transformation: from teeth, to teeth and baleen, to just baleen. Phylogenetic mapping of inactivating mutations reveals mutational decay of ‘dental genes’ related to enamel formation before the emergence of crown Mysticeti, while ‘baleen genes’ that were repurposed or newly derived during the evolutionary elaboration of baleen currently are poorly characterized. Review and meta-analysis of available data suggest that the teeth-to-baleen transition in Mysticeti is one of the best characterized macroevolutionary shifts due to the diversity of data from the genome, the fossil record, comparative anatomy, and ontogeny that directly bears on this remarkable evolutionary transformation.
... Shotgun sequencing of such DNA libraries then becomes inefficient in terms of associated costs necessary to attain coverage levels allowing for reconstructing specific barcode loci. Target gene capture as alternative can be an additional costly and time-intensive step, especially when a second round of capture is performed which has been shown to increase sequencing success (e.g., Li et al., 2013Li et al., , 2015Templeton et al., 2013;Springer et al., 2015;Paijmans et al., 2016). In an effort to increase efficiency and decrease overall costs for target capture of sample specific barcode markers in museum specimens, we report here on the design and successful application of an RNA bait set targeting taxonomically useful barcode markers in a variety of natural history collection samples of different phyla. ...
Article
Full-text available
A growing number of publications presenting results from sequencing natural history collection specimens reflect the importance of DNA sequence information from such samples. Ancient DNA extraction and library preparation methods in combination with target gene capture are a way of unlocking archival DNA, including from formalin-fixed wet-collection material. Here we report on an experiment, in which we used an RNA bait set containing baits from a wide taxonomic range of species for DNA hybridisation capture of nuclear and mitochondrial targets for analysing natural history collection specimens. The bait set used consists of 2,492 mitochondrial and 530 nuclear RNA baits and comprises specific barcode loci of diverse animal groups including both invertebrates and vertebrates. The baits allowed to capture DNA sequence information of target barcode loci from 84% of the 37 samples tested, with nuclear markers being captured more frequently and consensus sequences of these being more complete compared to mitochondrial markers. Samples from dry material had a higher rate of success than wet-collection specimens, although target sequence information could be captured from 50% of formalin-fixed samples. Our study illustrates how efforts to obtain barcode sequence information from natural history collection specimens may be combined and are a way of implementing barcoding inventories of scientific collection material.
... Nine genes were chosen for study based on prior evidence that these loci are enamel-specific or dentin/tooth-specific based on inactivation of these genes in one or more clades of toothless or enamelless vertebrate species (Deméré et al., 2008;McKnight and Fisher, 2009;Meredith et al., 2009Meredith et al., , 2011aMeredith et al., , 2013Meredith et al., , 2014Gasse et al., 2012;Kawasaki et al., 2014;Springer et al., 2015Springer et al., , 2016aSpringer et al., , 2019Mu et al., 2021;Gatesy et al., 2022). Additional evidence for the enamel or tooth specificity of these genes derives from mutagenesis studies in mice and natural genetic variation in humans that causes nonsyndromic cases of amelogenesis imperfecta, dentinogenesis imperfecta, or dentin dysplasia (Table 1). ...
Article
Full-text available
The loss of teeth and evolution of baleen racks in Mysticeti was a profound transformation that permitted baleen whales to radiate and diversify into a previously underutilized ecological niche of bulk filter-feeding on zooplankton and other small prey. Ancestral state reconstructions suggest that postnatal teeth were lost in the common ancestor of crown Mysticeti. Genomic studies provide some support for this hypothesis and suggest that the genetic toolkit for enamel production was inactivated in the common ancestor of living baleen whales. However, molecular studies to date have not provided direct evidence for the complete loss of teeth, including their dentin component, on the stem mysticete branch. Given these results, several questions remain unanswered: (1) Were teeth lost in a single step or did enamel loss precede dentin loss? (2) Was enamel lost early or late on the stem mysticete branch? (3) If enamel and dentin/tooth loss were decoupled in the ancestry of baleen whales, did dentin loss occur on the stem mysticete branch or independently in different crown mysticete lineages? To address these outstanding questions, we compiled and analyzed complete protein-coding sequences for nine tooth-related genes from cetaceans with available genome data. Seven of these genes are associated with enamel formation (ACP4, AMBN, AMELX, AMTN, ENAM, KLK4, MMP20) whereas two other genes are either dentin-specific (DSPP) or tooth-specific (ODAPH) but not enamel-specific. Molecular evolutionary analyses indicate that all seven enamel-specific genes have inactivating mutations that are scattered across branches of the mysticete tree. Three of the enamel genes (ACP4, KLK4, MMP20) have inactivating mutations that are shared by all mysticetes. The two genes that are dentin-specific (DSPP) or tooth-specific (ODAPH) do not have any inactivating mutations that are shared by all mysticetes, but there are shared mutations in Balaenidae as well as in Plicogulae (Neobalaenidae + Balaenopteroidea). These shared mutations suggest that teeth were lost at most two times. Shared inactivating mutations and dN/dS analyses, in combination with cetacean divergence times, were used to estimate inactivation times of genes and by proxy enamel and tooth phenotypes at ancestral nodes. The results of these analyses are most compatible with a two-step model for the loss of teeth in the ancestry of living baleen whales: enamel was lost very early on the stem Mysticeti branch followed by the independent loss of dentin (and teeth) in the common ancestors of Balaenidae and Plicogulae, respectively. These results imply that some stem mysticetes, and even early crown mysticetes, may have had vestigial teeth comprised of dentin with no enamel. Our results also demonstrate that all odontocete species (in our study) with absent or degenerative enamel have inactivating mutations in one or more of their enamel genes.
... Tooth development is a complex process that involves hundreds of genes, most of which are pleiotropic and also perform essential functions outside of odontogenesis (Thesleff 2006). However, ten genes have been shown to be tooth-specific with respect to their crucial functions that are maintained by natural selection McKnight and Fisher 2009;Meredith et al. 2009Meredith et al. , 2011Meredith et al. , 2013Meredith et al. , 2014Gasse et al. 2012;Kawasaki et al. 2014Kawasaki et al. , 2020Springer et al. 2015Springer et al. , 2016Springer et al. , 2019Mu et al. 2021) ( Table 2). All of these genes have become pseudogenized in one or more clades of mammals that have lost their postnatal teeth (baleen whales, anteaters, pangolins, Stellar's sea cow) or lost the enamel on their teeth (armadillos, sloths, aardvarks, pygmy and dwarf sperm whales). ...
Preprint
Full-text available
The transition in Mysticeti (Cetacea) from capture of individual prey using teeth to bulk filtering batches of small prey using baleen ranks among the most dramatic evolutionary transformations in mammalian history. We review phylogenetic work on the homology of mysticete feeding structures from anatomical, ontogenetic, and genomic perspectives. Six characters with key functional significance for filter-feeding behavior are mapped to cladograms based on 11 morphological datasets to reconstruct evolutionary change across the teeth-to-baleen transition. This comparative summary within a common parsimony framework reveals extensive conflicts among independent systematic efforts but also broad support for the newly named clade Kinetomenta (Aetiocetidae + Chaeomysticeti). Complementary anatomical studies using CTscans and ontogenetic series hint at commonalities between the developmental programs for teeth and baleen, lending further support for a transitional chimaeric feeder scenario that best explains current knowledge on the transition to filter feeding. For some extant mysticetes, the ontogenetic sequence in fetal specimens recapitulates the inferred evolutionary transformation: from teeth, to teeth and baleen, to just baleen. Phylogenetic mapping of inactivating mutations reveals mutational decay of dental genes related to enamel formation before the emergence of crown Mysticeti, while baleen genes that were repurposed or newly derived during the evolutionary elaboration of baleen currently are poorly characterized. Review and meta-analysis of available data suggest that the teeth-to-baleen transition in Mysticeti ranks among the best characterized macroevolutionary shifts due to the diversity of data from the genome, the fossil record, comparative anatomy, and ontogeny that directly bears on this remarkable evolutionary transformation.
... The present-day sirenians comprise the manatees (Trichechidae) and the dugongs (Dugongidae). Sirenians originated from an undetermined clade of terrestrial afrotherian mammals in the Paleocene (Springer et al. 2015). Throughout the Eocene, they diversified and colonized the tropical seas of the planet (Domning et al. 2010). ...
Article
Full-text available
The Sobrarbe-Pirineos UNESCO Global Geopark, located in the Central Pyrenees, is a region of remarkable geodiversity that includes extensive Eocene fossil-bearing sites and constitutes an important archive of paleobiodiversity. The Sobrarbe-Piri-neos Geopark hosts outcrops of Eocene formations bearing an unusual abundance and diversity of fossils from marine and continental sedimentary environments, making the Sobrarbe-Pirineos Geopark a perfect window for learning about tropical ecosystems of the Eocene of southern Europe. These environments were in part tectonically controlled and offer a unique opportunity to understand how faunas changed in an active area. Here, we outline the main groups of fossils from the Sobrarbe-Pirineos Geopark, including popular examples such as the "Crocodile of Ordesa-Vio" and the sirenian Sobrarbesiren. The Geopark has been a major tool in the geoconservation of Eocene fossils.
... Det kan tilläggas att man också har lyckats utvinna DNA ur rester av Stellers sjöko. Analyser av detta DNA har bekräftat att arten var närmare släkt med dugongen än med manaterna, vilket man redan tidigare hade antagit på anatomiska grunder (Rainey et al. 1984, Ozawa et al. 1997, Springer et al. 2015, Sharko et al. 2019. ...
... Captured libraries were subsequently purified using the MinElute® PCR clean-up kit (QIAGEN®) and DNA quantified using a Qubit Fluorometer (high sensitivity DNA kit). The whole procedure was repeated to further increase target content (Li, Hofreiter, Straube, Corrigan, & Naylor, 2013, Li et al., 2015Paijmans et al., 2016;Springer et al., 2015;Templeton et al., 2013). Libraries were then sequenced on either an Illumina® Nextseq (single end, 75 bp read length) or Miniseq instrument (paired end, 250 bp read length). ...
Article
Full-text available
Millions of scientific specimens are housed in museum collections, a large part of which are fluid preserved. The use of formaldehyde as fixative and subsequent storage in ethanol is especially common in ichthyology and herpetology. This type of preservation damages DNA and reduces the chance of successful retrieval of genetic data. We applied ancient DNA extraction and single stranded library construction protocols to a variety of vertebrate samples obtained from wet collections and of different ages. Our results show that almost all samples tested yielded endogenous DNA. Archival DNA extraction was successful across different tissue types as well as using small amounts of tissue. Conversion of archival DNA fragments into single‐stranded libraries resulted in usable data even for samples with initially undetectable DNA amounts. Subsequent target capture approaches for mitochondrial DNA using home‐made baits on a subset of 30 samples resulted in almost complete mitochondrial genome sequences in several instances. Thus, application of ancient DNA methodology makes wet collection specimens, including type material as well as rare, old or extinct species, accessible for genetic and genomic analyses. Our results, accompanied by detailed step‐by‐step protocols, are a large step forward to open the DNA archive of museum wet collections for scientific studies.
... Fabre, pers. comm.; Oryzorictes tetradactylus, divergence from most closely related sampled species O. hova at 5.13 Ma [80]; Hydrodamalis gigas, divergence from most closely related sampled species Dugong dugon at 28.59 Ma [81]). ...
Article
Full-text available
Background Mammals are a highly diverse group, with body mass ranging from 2 g to 170 t, and encompassing species with terrestrial, aquatic, aerial, and subterranean lifestyles. The skeleton is involved in most aspects of vertebrate life history, but while previous macroevolutionary analyses have shown that structural, phylogenetic, and functional factors influence the gross morphology of skeletal elements, their inner structure has received comparatively little attention. Here we analysed bone structure of the humerus and mid-lumbar vertebrae across mammals and their correlations with different lifestyles and body size. Results We acquired bone structure parameters in appendicular and axial elements (humerus and mid-lumbar vertebra) from 190 species across therian mammals (placentals + marsupials). Our sample captures all transitions to aerial, fully aquatic, and subterranean lifestyles in extant therian clades. We found that mammalian bone structure is highly disparate and we show that the investigated vertebral structure parameters mostly correlate with body size, but not lifestyle, while the opposite is true for humeral parameters. The latter also show a high degree of convergence among the clades that have acquired specialised (non-terrestrial) lifestyles. Conclusions In light of phylogenetic, size, and functional factors, the distribution of each investigated structural parameter reveals patterns explaining the construction of appendicular and axial skeletal elements in mammalian species spanning most of the extant diversity of the clade in terms of body size and lifestyle. These patterns should be further investigated with analyses focused on specific lifestyle transitions that would ideally include key fossils.
... With the increasing availability of genomic resources for nonmodel species, this kind of approach will become more broadly applicable-even though capture already shows potential to work across substantial divergence times (e.g., Bragg et al., 2016;Hedtke et al., 2013;Li et al., 2013;Portik et al., 2016). Springer et al., 2015) can be used to screen samples from related species for intraspecific variation. ...
Preprint
Full-text available
Hybridization capture coupled with high-throughput sequencing can be used to gain information about nuclear sequence variation at hundreds to thousands of loci. A cross-species approach makes use of molecular data of one species to enrich target loci in other (related) species. This is particularly valuable for non-model organisms, for which often no a priori knowledge exists regarding these loci. Here, we have adopted cross-species capture to obtain data for 809 nuclear coding DNA sequences (CDS) in a non-model organism, the Eurasian lynx Lynx lynx , using baits designed with the help of the published genome of a related model organism (the domestic cat Felis catus ). In this manner, we were able to survey intraspecific variation at hundreds of nuclear loci across the European range of L. lynx . A large set of bi-allelic candidate SNPs was then tested in a high throughput SNP-genotyping platform (Fluidigm), which we reduced to a final 96 SNP-panel based on assay performance and reliability; validation was carried out with additional samples not included in the SNP discovery phase. The 96 SNP-panel developed from CDS performed very successfully in the identification of individuals and in population genetic structure inference (incl. the assignment of individuals to their source population). In keeping with recent studies, our results show that genic SNPs can be valuable for genetic monitoring of wildlife species.
... Final elution was in 30 μL of 10 mM Tris-Cl, 0.05% TWEEN-20 solution (pH 8.0). To increase target capture success, the procedure was performed twice, i.e. the amplified captured library was used as a template for repeating the process as in Li et al. (2013Li et al. ( , 2015, Paijmans et al. (2016Paijmans et al. ( , 2017, Springer et al. (2015) and Templeton et al. (2013). Enriched libraries were pooled in equimolar amounts (10 nM) and sequenced on an Illumina NextSeq500/550 platform using a 75 cycle SE high-output kit aiming at 3 million reads per sample. ...
Article
Full-text available
The subgenus Mantidactylus is a group of frogs endemic to Madagascar, including the largest anuran species on the island. Although these frogs are common and widely distributed, their taxonomy remains unclear. Two species are currently recognised, M. grandidieri and M. guttulatus, with another available name, Rana pigra, considered to be a synonym of M. grandidieri. However, molecular studies have suggested the presence of several cryptic species within the group. Additionally, due to the lack of prominent morphological features, allocating the available names to evolutionary lineages has proven challenging. In the present study, we take a first step towards solving these problems by using fragments of the 16S mitochondrial gene and RAG1 nuclear gene from all over the range of the subgenus to describe its genetic diversity. We also use a newly designed target enrichment laboratory protocol to sequence three mitochondrial fragments from five name-holding museum specimens (as old as 120 years) in order to determine to which lineages the existing names should be applied. The study of the 16S mitochondrial gene revealed 7 geographically separated lineages, distinct enough to be considered candidate species. Out of the five museum specimens analysed, four successfully yielded DNA sequences and could be attributed to one of the aforementioned lineages. Therefore, the name Mantidactylus grandidieri should be applied to the populations from North-Eastern Madagascar, while M. guttulatus refers to populations from inland localities along the Eastern coast of the island. On the other hand, the holotype of Rana pigra did not yield enough genetic material to allow definitive identification. While our data were not sufficient to assess the status of the four lineages distributed along the Eastern coast, the populations from North-Western Madagascar were highly distinct on both the mitochondrial and nuclear markers. We thus describe them as a new species, M. radaka sp. nov.
... Traditionally, species were distinguished by comparing morphological and anatomical traits, a method established in 1735 (Linneaus, 1735) and globally adopted and standardized (http://iczn.org/). The advent of low-cost molecular techniques triggered a bloom of the mitochondrial and nuclear genomic data (Springer et al., 2015) to characterize distinct evolutionary lineages. Today, biologists generally rely on molecular rather than morphological data to discriminate biodiversity and characterize evolutionary (phylogenetic) relationships amongst species, largely due to the size and extent of the genomic data, the spectrum of genetic markers with varying evolutionary rates, and applicability across various groups of organisms (Hillis, 1987). ...
... Previous studies have shown that one or more of nine tooth-related genes (ACP4, AMBN, AMEL, AMTN, C4orf26 (= ODAPH), DSPP, ENAM, KLK4, MMP20) are inactivated in a variety of toothless vertebrates that have been investigated including birds [16][17][18][19], turtles [20], and several mammalian lineages comprising baleen whales, pangolins, anteaters, and Steller's sea cow [19,[21][22][23][24][25][26][27][28]. Many of these genes are also inactivated in mammals with enamelless teeth such as pygmy and dwarf sperm whales, aardvarks, sloths, and armadillos [19,23,24,[28][29][30]. ...
Article
Full-text available
Background The gene for odontogenic ameloblast-associated (ODAM) is a member of the secretory calcium-binding phosphoprotein gene family. ODAM is primarily expressed in dental tissues including the enamel organ and the junctional epithelium, and may also have pleiotropic functions that are unrelated to teeth. Here, we leverage the power of natural selection to test competing hypotheses that ODAM is tooth-specific versus pleiotropic. Specifically, we compiled and screened complete protein-coding sequences, plus sequences for flanking intronic regions, for ODAM in 165 placental mammals to determine if this gene contains inactivating mutations in lineages that either lack teeth (baleen whales, pangolins, anteaters) or lack enamel on their teeth (aardvarks, sloths, armadillos), as would be expected if the only essential functions of ODAM are related to tooth development and the adhesion of the gingival junctional epithelium to the enamel tooth surface. Results We discovered inactivating mutations in all species of placental mammals that either lack teeth or lack enamel on their teeth. A surprising result is that ODAM is also inactivated in a few additional lineages including all toothed whales that were examined. We hypothesize that ODAM inactivation is related to the simplified outer enamel surface of toothed whales. An alternate hypothesis is that ODAM inactivation in toothed whales may be related to altered antimicrobial functions of the junctional epithelium in aquatic habitats. Selection analyses on ODAM sequences revealed that the composite dN/dS value for pseudogenic branches is close to 1.0 as expected for a neutrally evolving pseudogene. DN/dS values on transitional branches were used to estimate ODAM inactivation times. In the case of pangolins, ODAM was inactivated ~ 65 million years ago, which is older than the oldest pangolin fossil (Eomanis, 47 Ma) and suggests an even more ancient loss or simplification of teeth in this lineage. Conclusion Our results validate the hypothesis that the only essential functions of ODAM that are maintained by natural selection are related to tooth development and/or the maintenance of a healthy junctional epithelium that attaches to the enamel surface of teeth. Electronic supplementary material The online version of this article (10.1186/s12862-019-1359-6) contains supplementary material, which is available to authorized users.
... We applied a touch down hybridisation with decreasing hybridisation temperature from 65°to 50°C in steps of 11 h totaling 36 h of hybridisation. The captured library is again amplified, size selected [69] and used as a starting point for a second round of capture, which is shown to increase the number of genes captured [68,70]. ...
Article
Full-text available
Background Previous molecular studies on the phylogeny and classification of clupeocephalan fishes revealed numerous new taxonomic entities. For re-analysing these taxa, we perform target gene capturing and subsequent next generation sequencing of putative ortholog exons of major clupeocephalan lineages. Sequence information for the RNA bait design was derived from publicly available genomes of bony fishes. Newly acquired sequence data comprising > 800 exon sequences was subsequently used for phylogenetic reconstructions. Results Our results support monophyletic Otomorpha comprising Alepocephaliformes. Within Ostariophysi, Gonorynchiformes are sister to a clade comprising Cypriniformes, Characiformes, Siluriformes and Gymnotiformes, where the interrelationships of Characiformes, Siluriformes and Gymnotiformes remain enigmatic. Euteleosts comprise four major clades: Lepidogalaxiiformes, Protacanthopterygii, Stomiatii, and Galaxiiformes plus Neoteleostei. The monotypic Lepidogalaxiiformes form the sister-group to all remaining euteleosts. Protacanthopterygii, comprising Argentini-, Esoci- and Salmoniformes, is sister to Stomiatii (Osmeriformes and Stomiatiformes) and Galaxiiformes plus Neoteleostei. Conclusions Several proposed monophyla defined by morphological apomorphies within the Clupeocephalan phylogeny are confirmed by the phylogenetic estimates presented herein. However, other morphologically described groups cannot be reconciled with molecular phylogenies. Thus, numerous morphological apomoprhies of supposed monophyla are called into question. The interpretation of suggested morphological synapomorphies of otomorph fishes is strongly affected by the inclusion of deep-sea inhabiting, and to that effect morphologically adapted Alepocephaliformes. Our revision of these potential synapomorphies, in the context that Alepocephaliformes are otomorph fishes, reveals that only a single character of the total nine characters proposed as synapomorphic for the group is clearly valid for all otomorphs. Three further characters remain possible apomorphies since their status remains unclear in the deep-sea adapted Alepocephaliformes showing developmental lag and lacking a swim bladder. Further, our analysis places Galaxiiformes as sister group to neoteleosts, which contradicts some previous molecular phylogenetic studies. This needs further investigation from a morphological perspective, as suggested synapomophies for several euteleostean lineages are challenged or still lacking. For the verification of results presented herein, a denser phylogenomic-level taxon sampling should be applied. Electronic supplementary material The online version of this article (10.1186/s12862-018-1267-1) contains supplementary material, which is available to authorized users.
... Domning and coworkers have made many observations in the Caribbean and West Atlantic region describing fossil sirenians and their palaeoecology (e.g. Velez-Juarbe 2014; Springer et al. 2015). Velez-Juarve (2014) has also discussed possible reasons for the late arrival of sirenians and seagrasses in Australia and South America. ...
Chapter
Seagrasses are an organismal biological group united by their ability to grow in marine environments. As marine flowering plants they have evolved a combined suite of adaptations multiple times enabling the four known lineages containing species of seagrass to survive, and thrive, in the sea. Unlike many other biological groups of plants however, seagrasses are all derived from a single order of flowering plants, the Alismatales. This order, being derived early in the evolution of the monocotyledons, is comprised predominantly of aquatic plants, of all forms–emergent, submerged, freshwater, estuarine and marine. A review of seagrass fossils suggests that new discoveries of seagrass fossils along with confirmation of some earlier finds lead to a clear signal that some seagrass species had a wider distribution in the past compared with today. The discovery of new fossil sites should be encouraged as this will likely produce important valuable information on the evolution of this group. In general the biogeography of seagrasses suggests that these organisms evolved successfully in the Tethys Sea of the Late Cretaceous. However, the modern division into two groups, temperate and tropical tends to suggest that at some point an ecological separation occurred in both the Northern and Southern Hemispheres. There are a disproportionately large number of temperate seagrass species in southern Australia and there is significant endemism shown in Posidonia, Amphibolis and a unique species of Halophila (H. australis). The use of genetic and genomic techniques has begun to explain these distributions but we can expect a much bigger picture to emerge in the near future.
... The placement of Eotheroides is insufficiently well-supported for use as a strong prior. The phylogenetic analysis of Voss [59] placed Eotheroides as a stem sirenian, and although Springer et al. [60] favoured crown placement, majority-rule of their bootstrap analysis does not resolve stem or crown placement. More generally, the placement of early sirenians relative to the modern Dugongidae (dugongs) and Trichechidae (manatees) is potentially complicated by the plesiomorphic feeding and habitat ecology of early fully aquatic sirenians being more closely retained by dugongs than manatees [61]. ...
... Thus, baits designed for other purposes (e.g. resolving taxonomic uncertainties, Yuan et al., 2016; identifying regulatory sequences, Yoshihara et al., 2016; identifying adaptive genes, Roffler et al., 2016; investigating loci linked to traits, Springer et al., 2015) can be used to screen samples from related species for intraspecific variation. Colours are used to differentiate between genotyping success at standard template DNA concentration (red circles, 50 ng/µL) and low template DNA concentration (blue circles, 0.5 ng/µL). ...
Article
Targeted capture coupled with high throughput sequencing can be used to gain information about nuclear sequence variation at hundreds to thousands of loci. Divergent reference capture makes use of molecular data of one species to enrich target loci in other (related) species. This is particularly valuable for non‐model organisms, for which often no a priori knowledge exists regarding these loci. Here, we have used targeted capture to obtain data for 809 nuclear coding DNA sequences (CDS) in a non‐model organism, the Eurasian lynx Lynx lynx, using baits designed with the help of the published genome of a related model organism (the domestic cat Felis catus). Using this approach, we were able to survey intraspecific variation at hundreds of nuclear loci in L. lynx across the species’ European range. A large set of bi‐allelic candidate SNPs was then evaluated using a high throughput SNP‐genotyping platform (Fluidigm), which we then reduced to a final 96 SNP‐panel based on assay performance and reliability; validation was carried out with 100 additional Eurasian lynx samples not included in the SNP discovery phase. The 96 SNP‐panel developed from CDS performed very successfully in the identification of individuals and in population genetic structure inference (including the assignment of individuals to their source population). In keeping with recent studies, our results show that genic SNPs can be valuable for genetic monitoring of wildlife species. This article is protected by copyright. All rights reserved.
... The latter are quite robust and thick (no quantitative assessment was made). In the earliest-diverging sirenian Prorastomus (Early Eocene [37]), the skull walls are thick and compact, and the ethmoturbinates are described as more extensive and thinner than in the later members of the clade [38]. In Protosiren (Middle Eocene; see [39], fig. ...
... The latter are quite robust and thick (no quantitative assessment was made). In the earliest-diverging sirenian Prorastomus (Early Eocene [37]), the skull walls are thick and compact, and the ethmoturbinates are described as more extensive and thinner than in the later members of the clade [38]. In Protosiren (Middle Eocene; see [39], fig. ...
Article
Full-text available
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.
Article
The Cenozoic diversification of placental mammals is the archetypal adaptive radiation. Yet, discrepancies between molecular divergence estimates and the fossil record fuel ongoing debate around the timing, tempo, and drivers of this radiation. Analysis of a three-dimensional skull dataset for living and extinct placental mammals demonstrates that evolutionary rates peak early and attenuate quickly. This long-term decline in tempo is punctuated by bursts of innovation that decreased in amplitude over the past 66 million years. Social, precocial, aquatic, and herbivorous species evolve fastest, especially whales, elephants, sirenians, and extinct ungulates. Slow rates in rodents and bats indicate dissociation of taxonomic and morphological diversification. Frustratingly, highly similar ancestral shape estimates for placental mammal superorders suggest that their earliest representatives may continue to elude unequivocal identification.
Preprint
Full-text available
The extinct Steller's sea cow ( Hydrodamalis gigas ) 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-O 2 affinity of Steller's sea cow evolved to become less affected by temperature compared to other sea cows. This phenotype presumably safeguarded O 2 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-O 2 affinity phenotype that is moreover unresponsive to the intraerythrocytic allosteric effector 2,3-diphosphoglycerate. This radical modification, which augments O 2 offloading by the protein, and presumably impacted maternal/fetal O 2 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.
Preprint
The precise pattern and timing of speciation events that gave rise to all living placental mammals remain controversial. We provide a comprehensive phylogenetic analysis of genetic variation across an alignment of 241 placental mammal genome assemblies, addressing prior concerns regarding limited genomic sampling across species. We compared neutral genome-wide phylogenomic signal using concatenation and coalescent-based approaches, interrogated phylogenetic variation across chromosomes and analyzed extensive catalogs of structural variants. Interordinal relationships exhibit relatively low rates of phylogenomic conflict across diverse datasets and analytical methods. Conversely, X-chromosome versus autosome conflicts characterize multiple independent clades that radiated during the Cenozoic. Genomic timetrees reveal an accumulation of cladogenic events before and immediately following the KPg boundary implying important roles for Cretaceous continental vicariance and the KPg extinction in the placental radiation.
Article
Full-text available
Vocal production learning is the ability to modify a vocal output in response to auditory experience. It is essential for human speech production and language acquisition. Vocal learning evolved independently several times in vertebrates, indicating evolutionary pressure in favor of this trait. This enables cross-species comparative analysis to be used to test evolutionary hypotheses. Humans share this ability with a versatile but limited group of species: songbirds, parrots and hummingbirds, bats, cetaceans, seals, and elephants. Although case studies demonstrate that African savanna and Asian elephants are capable of heterospecific imitation, including imitation of human words, our understanding of both the underlying mechanisms and the adaptive relevance within the elephant’s natural communication system is limited. Even though comparing phylogenetically distant species is intriguing, it is also worthwhile to investigate whether and to what extent learned vocal behavior is apparent in species phylogenetically close to an established vocal learner. For elephants, this entails determining whether their living relatives share their special ability for (complex) vocal learning. In this review, we address vocal learning in Elephantidea and Sirenia, sister groups within the Paenungulata. So far, no research has been done on vocal learning in Sirenians. Because of their aquatic lifestyle, vocalization structure, and evolutionary relationship to elephants, we believe Sirenians are a particularly interesting group to study. This review covers the most important acoustic aspects related to vocal learning in elephants, manatees, and dugongs, as well as knowledge gaps that must be filled for one to fully comprehend why vocal learning evolved (or did not) in these distinctive but phylogenetically related taxa.
Article
Two sirenian species are present in the late Eocene Samlat Formation near Ad-Dakhla in southwestern Morocco. A well preserved mandible with left and right dentaries belongs to a new protosirenid genus and species Dakhlasiren marocensis closely related to the genus Protosiren. An early dugongid of uncertain identification (cf. Eotheroides sp.) is also present, represented by vertebrae and ribs. Protosirenids differ from dugongids in the form of the brain, size and separation of nasal bones, and conformation of the anterior mandible. Protosirenids also differ in having vertebrae with larger neural canals, in having ligamentous rib articulations, and in lacking the pachyostotic ribs characteristic of dugongids. We tentatively interpret the latter differences to be related to feeding on softer vegetation farther offshore, with a thoracic rete mirabile for counter-current heat exchange and a collapsible rib cage to enable deeper dives. Dakhlasiren seemingly carried the divergent specializations of Protosiren a step farther by reduction of tongue musculature and loss of a masticatory surface at the front of the mandible. https://authors.elsevier.com/c/1elPL,XIvblkif
Article
Full-text available
Background : The study of regressive evolution has yielded a wealth of examples where the underlying genes bear molecular signatures of trait degradation, such as pseudogenization or deletion. Typically, it appears that such disrupted genes are limited to the function of the regressed trait, whereas pleiotropic genes tend to be maintained by natural selection to support their myriad purposes. One such set of pleiotropic genes is involved in the synthesis ( AANAT , ASMT ) and signaling ( MTNR1A , MTNR1B ) of melatonin, a hormone secreted by the vertebrate pineal gland. Melatonin provides a signal of environmental darkness, thereby influencing the circadian and circannual rhythmicity of numerous physiological traits. Therefore, the complete loss of a pineal gland and the underlying melatonin pathway genes seems likely to be maladaptive, unless compensated by extrapineal sources of melatonin. Methods : We examined AANAT , ASMT , MTNR1A and MTNR1B in 123 vertebrate species, including pineal-less placental mammals and crocodylians. We searched for inactivating mutations and modelled selective pressures (dN/dS) to test whether the genes remain functionally intact. Results : We report that crocodylians retain intact melatonin genes and express AANAT and ASMT in their eyes, whereas all four genes have been repeatedly inactivated in the pineal-less xenarthrans, pangolins, sirenians, and whales. Furthermore, colugos have lost these genes, and several lineages of subterranean mammals have partial melatonin pathway dysfunction. These results are supported by the presence of shared inactivating mutations across clades and analyses of selection pressure based on the ratio of non-synonymous to synonymous substitutions (dN/dS), suggesting extended periods of relaxed selection on these genes. Conclusions: The losses of melatonin synthesis and signaling date to tens of millions of years ago in several lineages of placental mammals, raising questions about the evolutionary resilience of pleiotropic genes, and the causes and consequences of losing melatonin pathways in these species.
Preprint
Full-text available
The loss of teeth and evolution of baleen racks in Mysticeti was a profound transformation that permitted baleen whales to radiate and diversify into a previously underutilized ecological niche of bulk filter-feeding on zooplankton and other small prey. Ancestral state reconstructions suggest that teeth were lost in the common ancestor of crown Mysticeti. Genomic studies provide some support for this hypothesis and suggest that the genetic toolkit for enamel production was inactivated in the common ancestor of living baleen whales. However, molecular studies to date have not provided direct evidence for the complete loss of teeth, including their dentin component, on the stem mysticete branch. Given these results, several questions remain unanswered: (1) Were teeth lost in a single step or did enamel loss precede dentin loss? (2) Was enamel lost early or late on the stem mysticete branch? (3) If enamel and dentin/tooth loss were decoupled in the ancestry of baleen whales, did dentin loss occur on the stem mysticete branch or independently in different crown mysticete lineages? To address these outstanding questions, we compiled and analyzed complete protein-coding sequences for nine tooth-related genes from cetaceans with available genome data. Seven of these genes are associated with enamel formation (ACP4, AMBN, AMELX, AMTN, ENAM, KLK4, MMP20) whereas two other genes are either dentin-specific (DSPP) or tooth-specific (ODAPH) but not enamel-specific. Molecular evolutionary analyses indicate that all seven enamel-specific genes have inactivating mutations that are scattered across branches of the mysticete tree. Three of the enamel genes (ACP4, KLK4, MMP20) have inactivating mutations that are shared by all mysticetes. The two genes that are dentin-specific (DSPP) or tooth-specific (ODAPH) do not have any inactivating mutations that are shared by all mysticetes, but there are shared mutations in Balaenidae as well as in Plicogulae (Neobalaenidae + Balaenopteroidea). These shared mutations suggest that teeth were lost at most two times. Shared inactivating mutations and dN/dS analyses, in combination with cetacean divergence times, were used to estimate inactivation times of genes and by proxy enamel and tooth phenotypes. The results of these analyses are most compatible with a two-step model for the loss of teeth in the ancestry of living baleen whales: enamel was lost very early on the stem Mysticeti branch followed by the independent loss of dentin (and teeth) in the common ancestors of Balaenidae and Plicogulae, respectively. These results imply that some stem mysticetes, and even early crown mysticetes, may have had vestigial teeth comprised of dentin with no enamel. Our results also demonstrate that all odontocete species (in our study) with absent or degenerative enamel have inactivating mutations in one or more of their enamel genes.
Article
Background : The study of regressive evolution has yielded a wealth of examples where the underlying genes bear molecular signatures of trait degradation, such as pseudogenization or deletion. Typically, it appears that such disrupted genes are limited to the function of the regressed trait, whereas pleiotropic genes tend to be maintained by natural selection to support their myriad purposes. One such set of genes is involved in the synthesis ( AANAT , ASMT ) and signaling ( MTNR1A , MTNR1B ) of melatonin, a hormone secreted by the vertebrate pineal gland. Melatonin provides a signal of environmental darkness, thereby influencing the circadian and circannual rhythmicity of numerous physiological traits. Therefore, the complete loss of a pineal gland and the underlying melatonin pathway genes seems likely to be maladaptive, unless compensated by extrapineal sources of melatonin. Methods : We examined AANAT , ASMT , MTNR1A and MTNR1B in 123 vertebrate species, including pineal-less placental mammals and crocodylians. We searched for inactivating mutations and modelled selective pressures (dN/dS) to test whether the genes remain functionally intact. Results : We report that crocodylians retain intact melatonin genes and express AANAT and ASMT in their eyes, whereas all four genes have been repeatedly inactivated in the pineal-less xenarthrans, pangolins, sirenians, and whales. Furthermore, colugos have lost these genes, and several lineages of subterranean mammals have partial melatonin pathway dysfunction. These results are supported by the presence of shared inactivating mutations across clades and analyses of selection pressure based on the ratio of non-synonymous to synonymous substitutions (dN/dS), suggesting extended periods of relaxed selection on these genes. Conclusions: The losses of melatonin synthesis and signaling dates to tens of millions of years ago in several lineages of placental mammals, raising questions about the evolutionary resilience of pleiotropic genes, and the causes and consequences of losing melatonin pathways in these species.
Article
The macroevolutionary transition from terra firma to obligatory inhabitance of the marine hydrosphere has occurred twice in the history of Mammalia: Cetacea and Sirenia. In the case of Cetacea (whales, dolphins, and porpoises), molecular phylogenies provide unambiguous evidence that fully aquatic cetaceans and semiaquatic hippopotamids (hippos) are each other’s closest living relatives. Ancestral reconstructions suggest that some adaptations to the aquatic realm evolved in the common ancestor of Cetancodonta (Cetacea + Hippopotamidae). An alternative hypothesis is that these adaptations evolved independently in cetaceans and hippos. Here, we focus on the integumentary system and evaluate these hypotheses by integrating new histological data for cetaceans and hippos, the first genome-scale data for pygmy hippopotamus, and comprehensive genomic screens and molecular evolutionary analyses for protein-coding genes that have been inactivated in hippos and cetaceans. We identified eight skin-related genes that are inactivated in both cetaceans and hippos, including genes that are related to sebaceous glands, hair follicles, and epidermal differentiation. However, none of these genes exhibit inactivating mutations that are shared by cetaceans and hippos. Mean dates for the inactivation of skin genes in these two clades serve as proxies for phenotypic changes and suggest that hair reduction/loss, the loss of sebaceous glands, and changes to the keratinization program occurred ∼16 Ma earlier in cetaceans (∼46.5 Ma) than in hippos (∼30.5 Ma). These results, together with histological differences in the integument and prior analyses of oxygen isotopes from stem hippopotamids (“anthracotheres”), support the hypothesis that aquatic skin adaptations evolved independently in hippos and cetaceans.
Book
This fully updated second edition explores protocols that address the most challenging aspects of experimental work in ancient DNA, such as preparing ancient samples for DNA extraction, the DNA extraction itself, and transforming extracted ancient DNA molecules for sequencing library preparation. The volume also examines the analysis of high-throughput sequencing data recovered from ancient specimens, which, because of the degraded nature of ancient DNA and common co-extraction of contaminant DNA, has challenges that are unique compared to data recovered from modern specimens.Written in the highly successful Methods in Molecular Biology series format, chapters include introductions to their respective topics, lists of the necessary materials and reagents, step-by-step, readily reproducible laboratory protocols, and tips on troubleshooting and avoiding known pitfalls. Authoritative and cutting-edge, Ancient DNA: Methods and Protocols, Second Edition aims to serve both experts and beginners by presenting protocols in a manner that makes them easily accessible for everyday use in the lab.
Article
Chelonioidea (sea turtles) are a group where available morphological evidence for crown-group relationships are incongruent with those established using molecular data. However, morphological surveys of crown-group taxa tend to focus on a recurring subset of the extant species. The Australian flatback sea turtle, Natator depressus, is often excluded from comparisons and it is the most poorly known of the seven extant species of Chelonioidea. Previous descriptions of its skull morphology are limited and conflict. Here we describe three skulls of adult N. depressus and re-examine the phylogenetic relationships according to morphological character data. Using X-ray micro Computed Tomography we describe internal structures of the braincase and identify new phylogenetically informative characters not previously reported. Phylogenetic analysis using a Bayesian approach strongly supports a sister-group relationship between Chelonia mydas and N. depressus, a topology that was not supported by previous analyses of morphological data but one that matches the topology supported by analysis of molecular data. Our results highlight the general need to sample the morphological anatomy of crown-group taxa more thoroughly before concluding that morphological and molecular evidence are incongruous.
Article
Stegosiren macei, a new genus and species of halitheriine dugongid from the mid-Oligocene of South Carolina, U.S.A. (Ashley and Chandler Bridge formations, late Rupelian–late Chattian), represents a stage of halitheriine evolution more derived than that of the Old World early Oligocene Eosiren imenti and Halitherium schinzii, but slightly less derived than the West Atlantic late Oligocene Metaxytherium albifontanum. It is more comparable in stage of evolution to its early Oligocene contemporaries Caribosiren turneri and Priscosiren atlantica and may be a sister taxon of these two. It is distinguished autapomorphically from all other sirenians by a notably broadened frontal roof and a thickened anterior tip of the frontal, which formed a butt joint with the premaxilla. Analogous (independently evolved) joints in several other sirenians (principally dugongines) are correlated with enlarged upper tusks thought to be used for excavating seagrass rhizomes. This suggests that large tusks also may have been present (although not preserved) in Stegosiren, which is only the second halitheriine in which such a feature has been observed. Stegosiren macei brings to at least seven the number of potentially sympatric sirenian species lineages known from the West Atlantic-Caribbean Oligocene (six or more from South Carolina alone). This extraordinary sirenian diversity, unmatched elsewhere in the world, poses problems for ecomorphology and feeding-niche partitioning.
Article
Full-text available
The near lack of vertebrate fossils from the Cenozoic of Madagascar has left many of the details regarding the origin and evolution of the island’s extant faunas unknown. However, recent fossil discoveries from Madagascar’s nearshore marine deposits have begun to elucidate this mystery. These finds include sharks, bony fish, turtles, crocodylians, a middle Eocene sirenian (Eotheroides lambondrano), and the island’s first fossil dolphin. We report here at least three (possibly four) different early (or possibly later) Miocene dugongid sirenians recovered from the island of Nosy Makamby, Mahajanga Basin, northwestern Madagascar. These include (1) a fragmentary braincase originally attributed to the genus Halitherium but here reidentified as a previously named species known only from Libya (Rytiodus heali; Dugonginae); (2) a newly named genus and species (Norosiren zazavavindrano) interpreted as a primitive relative of Xenosiren (Dugonginae); (3) a probable dugongine not yet identified with any known species; and (4) a taxon reported here as Metaxytherium cf. krahuletzi (Halitheriinae), the first Neogene halitheriine credibly reported from the Indian Ocean basin. This pattern of shallow marine environments harboring multispecies sirenian paleofaunas is seen elsewhere in the world, and these three or four contemporaneous sirenians represent the first glimpse into Madagascar’s sea cow diversity during the Miocene. This specific time period is a poorly known and critical interval for interpreting Madagascar’s past, and these specimens are potentially highly significant for reconstructing sirenian evolutionary and biogeographic history. Surprisingly, this sirenian fauna, so far, shares no genera with the roughly contemporaneous and relatively nearby one from Kutch, western India.
Chapter
Genetic studies that include ancient samples are often hampered by the low amount of endogenous DNA that ancient samples often contain, relative to co-extracted “contaminant” DNA from other organisms. One approach to mitigate this challenge is to perform hybridization-based capture of target genomic regions using DNA or RNA baits. Such baits are designed to have high sequence similarity to the target genomic regions and can reduce the off-target fraction in DNA sequencing libraries. Here, we present a protocol to use Agilent SureSelect microarrays to enrich ancient DNA libraries for small-to-medium-sized target loci, such as mitochondrial genomes, from ancient DNA extracts. The protocol that we present builds on previously published work by introducing improvements that improve recovery of short DNA fragments while minimizing the cost and duration of the experiment.
Chapter
Environmental DNA preserved in sediments is rapidly gaining importance as a tool in paleoecology. Sampling procedures for sedimentary ancient DNA (sedaDNA) have to be well planned to ensure clean subsampling of the inside of sediment cores and avoid introducing contamination. Additionally, ancient DNA extraction protocols may need to be optimized for the recovery of DNA from sediments, which may contain inhibitors. Here we describe procedures for subsampling both nonfrozen and frozen sediment cores, and we describe an efficient method for ancient DNA extraction from such samples.
Article
Full-text available
Sirenians have been extensively recorded from the Mediterranean and west European localities but there are only few finds to the east of it, from the area covered by the Paratethys. For the early Oligocene, to our knowledge, there are no published records of sirenians from inner seas of the Old World. Here we report a specimen of Dugongidae indet., consisting of two partial vertebrae and 12 fragments of ribs, collected in a manganese ore mine in Ukraine and dated as the earliest Oligocene (33–32 Ma). The specimens, as preserved, did not differ in morphology and size from ‘Halitherium schinzii’ and therefore can belong to Kaupitherium, at present the single early Oligocene genus recorded from Europe. However, its vertebral and rib anatomy is not specific for Kaupitherium, so we identify it only by family level. The marks of scavenging on a rib possibly are due to gastropod or bivalve mollusks. The sea, as suggested from biotic data, had a temperate or subtropical climate, relatively cold waters and high diversity of pelagic and deepwater habitats. Thus, the onset of the Oligocene was a period when sirenians could enter temperate inner Eurasian waters, a marginal area in their worldwide dispersal.
Article
Full-text available
Steller’s classic work, published in Latin in 1751 and in German in 1753, contains the only scientific description from life of the Steller’s sea cow (Hydrodamalis gigas), as well as the first scientific descriptions of the fur seal or “sea bear” (Callorhinus ursinus), Steller’s sea lion (Eumetopias jubatus), and the sea otter (Enhydra lutris). Steller’s sea cow was a sirenian, or manatee, inhabiting the North Pacific Ocean and Bering Sea. It was first discovered by Europeans in 1741 and rendered extinct by 1768. It was a 30-foot long, plant-eating aquatic mammal, weighing up to 12 tons, that lived in large herds on the coasts of Alaska and Kamchatka. Steller made his observations as part of Vitus Bering’s second voyage, during which the crew was shipwrecked for 9 months on Bering Island, from November 1741 to August 1742. This voyage was undertaken as part of the Great Northern Expedition, commissioned by the Imperial Academy of Sciences in St. Petersburg, to prosecute the exploration of the North Pacific and western North America. This English translation originally appeared in 1899, in an appendix to The Fur Seals and Fur-Seal Islands of the North Pacific Ocean, edited by David Starr Jordan, Part 3 (Washington, 1899), pp. 179–218. A brief bibliography, links to online works and sites, and illustrations have been added by the present editor.
Article
Full-text available
Ancient mitochondrial DNA has been used in a wide variety of palaeontological and archaeological studies, ranging from population dynamics of extinct species to patterns of domestication. Most of these studies have traditionally been based on the analysis of short fragments from the mitochondrial control region, analysed using PCR coupled with Sanger sequencing. With the introduction of high-throughput sequencing, as well as new enrichment technologies, the recovery of full mitochondrial genomes (mitogenomes) from ancient specimens has become significantly less complicated. Here we present a protocol to build ancient extracts into Illumina high-throughput sequencing libraries, and subsequent Agilent array-based capture to enrich for the desired mitogenome. Both are based on previously published protocols, with the introduction of several improvements aimed to increase the recovery of short DNA fragments, while keeping the cost and effort requirements low. This protocol was designed for enrichment of mitochondrial DNA in ancient or degraded samples. However, the protocols can be easily adapted for using for building libraries for shotgun-sequencing of whole genomes, or enrichment of other genomic regions.
Article
Full-text available
Edentulism, the absence of teeth, has evolved convergently among vertebrates, including birds, turtles, and several lineages of mammals. Instead of teeth, modern birds (Neornithes) use a horny beak (rhamphotheca) and a muscular gizzard to acquire and process food. We performed comparative genomic analyses representing lineages of nearly all extant bird orders and recovered shared, inactivating mutations within genes expressed in both the enamel and dentin of teeth of other vertebrate species, indicating that the common ancestor of modern birds lacked mineralized teeth. We estimate that tooth loss, or at least the loss of enamel caps that provide the outer layer of mineralized teeth, occurred about 116 million years ago. Copyright © 2014, American Association for the Advancement of Science.
Article
Full-text available
Newly discovered remains of the early Middle Eocene (Lutetian) sirenian Protosiren (Protosi-renidae) in shark tooth rich conglomerates from a coastal delta environment northwest of the European Rhenish Massif at Fürstenau (northwestern Germany), represent the most northerly occurrence of this genus whose global distribution was generally restricted to warm waters. Its presence of the remains so far north can be explained by seasonal inflow of warm Tethys surface water into the cool, upwelling-influenced, basin. The existence of two discrete centers of sirenian evolution can be explained by the opening of the Atlantic and the upwelling that separated the North American warm water fau-nal province from those of Africa and Eurasia. A slightly modified evolutionary model is presented in which the oldest Early Eocene mana-tee sirenians evolved in the Caribbean of Central America. Protosiren, however, appears to have developed polyphyletically along the African coastline of the Tethys, and represents the oldest known dugong ancestor. Younger (Oligo-cene) European sirenian skeletons of Halith-erium and Anomotherium are included in the phylostratigraphic model in which sirenians had generally reduced their teeth by 28 Ma as an adaptation for feeding on sea-plants (macroal-gae/seagrass). Teeth from early megatooth sharks, which preyed on sirenians, have been recorded from shallow marine Eocene and Oli-gocene coastlines of the southern proto-North Sea Basin, and shark bite marks have been found on sirenian skeletons.
Article
Full-text available
Small-bodied, insectivorous Nyctitheriidae are known in the Palaeogene fossil record almost exclusively from teeth and fragmentary jaws and have been referred to Eulipotyphla (shrews, moles and hedgehogs) based on dental similarities. By contrast, isolated postcrania attributed to the group suggest arboreality and a relationship to Euarchonta (primates, treeshrews and colugos). Cretaceous–Palaeocene adapisoriculid insectivores have also been proposed as early euarchontans based on postcranial similarities. We describe the first known dentally associated nyctitheriid auditory regions and postcrania, and use them to test the proposed relationship to Euarchonta with cladistic analyses of 415 dental, cranial and postcranial characteristics scored for 92 fossil and extant mammalian taxa. Although nyctitheriid postcrania share similarities with euarchontans likely related to arboreality, results of cladistic analyses suggest that nyctitheriids are closely related to Eulipotyphla. Adapisoriculidae is found to be outside of crown Placentalia. These results suggest that similarities in postcranial morphology among nyctitheriids, adapisoriculids and euarchontans represent separate instances of convergence or primitive retention of climbing capabilities.
Article
Full-text available
Anthracobunidae is an Eocene family of large mammals from south Asia that is commonly considered to be part of the radiation that gave rise to elephants (proboscideans) and sea cows (sirenians). We describe a new collection of anthracobunid fossils from Middle Eocene rocks of Indo-Pakistan that more than doubles the number of known anthracobunid fossils and challenges their putative relationships, instead implying that they are stem perissodactyls. Cranial, dental, and postcranial elements allow a revision of species and the recognition of a new anthracobunid genus. Analyses of stable isotopes and long bone geometry together suggest that most anthracobunids fed on land, but spent a considerable amount of time near water. This new evidence expands our understanding of stem perissodactyl diversity and sheds new light on perissodactyl origins.
Article
Full-text available
Cetacea (whales, dolphins, and porpoises) is a model group for investigating the molecular signature of macroevolutionary transitions. Recent research has begun to reveal the molecular underpinnings of the remarkable anatomical and behavioral transformation in this clade. This shift from terrestrial to aquatic environments is arguably the best-understood major morphological transition in vertebrate evolution. The ancestral body plan and physiology were extensively modified and, in many cases, these crucial changes are recorded in cetacean genomes. Recent studies have highlighted cetaceans as central to understanding adaptive molecular convergence and pseudogene formation. Here, we review current research in cetacean molecular evolution and the potential of Cetacea as a model for the study of other macroevolutionary transitions from a genomic perspective.
Article
Full-text available
The International Commission on Stratigraphy (ICS) has a long tradition of producing international charts that communicate higher-order divisions of geological time and actual knowledge on the absolute numerical ages of their boundaries. The primary objective of ICS is to define precisely a global standard set of timecorrelative units (Systems, Series, and Stages) for stratigraphic successions worldwide. These units are, in turn, the basis for the Periods, Epochs and Ages of the Geological Time Scale. Setting an international global standard is fundamental for expressing geological knowledge. It is also of considerable pragmatic importance as it provides the framework through which regional-scale higher-resolution divisions can be linked, equated and collated. This is a status update on the International Chronostratigraphic Chart and the ICS website www.stratigraphy.org.
Article
Full-text available
Mitochondrial DNA (mtDNA) typing can be a useful aid for identifying people from compromised samples when nuclear DNA is too damaged, degraded or below detection thresholds for routine short tandem repeat (STR)-based analysis. Standard mtDNA typing, focused on PCR amplicon sequencing of the control region (HVS I and HVS II), is limited by the resolving power of this short sequence, which misses up to 70% of the variation present in the mtDNA genome. We used in-solution hybridisation-based DNA capture (using DNA capture probes prepared from modern human mtDNA) to recover mtDNA from post-mortem human remains in which the majority of DNA is both highly fragmented (<100 base pairs in length) and chemically damaged. The method 'immortalises' the finite quantities of DNA in valuable extracts as DNA libraries, which is followed by the targeted enrichment of endogenous mtDNA sequences and characterisation by next-generation sequencing (NGS). We sequenced whole mitochondrial genomes for human identification from samples where standard nuclear STR typing produced only partial profiles or demonstrably failed and/or where standard mtDNA hypervariable region sequences lacked resolving power. Multiple rounds of enrichment can substantially improve coverage and sequencing depth of mtDNA genomes from highly degraded samples. The application of this method has led to the reliable mitochondrial sequencing of human skeletal remains from unidentified World War Two (WWII) casualties approximately 70 years old and from archaeological remains (up to 2,500 years old). This approach has potential applications in forensic science, historical human identification cases, archived medical samples, kinship analysis and population studies. In particular the methodology can be applied to any case, involving human or non-human species, where whole mitochondrial genome sequences are required to provide the highest level of maternal lineage discrimination. Multiple rounds of in-solution hybridisation-based DNA capture can retrieve whole mitochondrial genome sequences from even the most challenging samples.
Article
Full-text available
Tree-building with diverse data maximizes explanatory power. Application of molecular clock models to ancient speciation events risks a bias against detection of fast radiations subsequent to the Cretaceous-Paleogene (K-Pg) event. Contrary to Springer et al., post–K-Pg placental diversification does not require “virus-like” substitution rates. Even constraining clade ages to their model, the explosive model best explains placental evolution.
Article
Full-text available
O'Leary et al. (Research Article, 8 February 2013, p. 662) examined mammalian relationships and divergence times and concluded that a single placental ancestor crossed the Cretaceous-Paleogene (K-Pg) boundary. This conclusion relies on phylogenetic analyses that fail to discriminate between homology and homoplasy and further implies virus-like rates of nucleotide substitution in early Paleocene placentals.
Article
Full-text available
The supraordinal mammalian clade Afrotheria was first recognized in its entirety based on DNA analysis dating to the mid-1990s. Since then, this "African clade", which includes proboscideans, sirenians, hyracoids, tubulidentates, elephant-shrews, tenrecs and chrysochlorids, has been supported by numerous molecular and genomic studies. According to these molecular inferences, the origin of crown Afrotheria goes back into the Cretaceous, with estimates from over 100 to under 80 Mya. Morphological phylogenies have not completely recovered Afrotheria, although its paenungulate core (proboscideans, sirenians and hyracoids) was named in 1945 by the paleontologist George Simpson. Recent paleontological studies concur with molecular ones in evoking some affinities between paenungulates, aardvarks and elephant-shrews. Moreover, the position of tenrecs and golden moles within afrotherians is supported by some recent concatenations of morphological and molecular phylogenetic datasets. The phylogenetic position of Afrotheria relative to the other supraordinal placental clades has been debated, the most recent analyses of genomic and concatenated data support a basal position within Placentalia. Molecular data suggest an African origin for Afrotheria and a long period of endemism on that continent. When adding the paleontological data to this scenario, the paleobiogeographic history of Afrotheria becomes more complex. For instance, these data argue for the broad distribution of afrotherians during the Tertiary and do not exclude their Laurasian origin. In fact, some Laurasian taxa could be closely related to the earliest afrotherians (hyracoids, proboscideans and elephant-shrews) found in the early Eocene of North Africa. Other Afrotherian groups are known with certitude from East Africa since the beginning of the Miocene.
Article
Full-text available
Molecular estimates for the divergence of Chrysochloridae (golden moles) and Tenrecoidea (tenrecs) date back to near the K-T boundary, but at present the oldest undoubted fossil members of these clades are early Miocene in age (~20 Ma). The only Paleogene African genus that has been proposed as a possible stem tenrecoid is late Eocene (~34 Ma) Widanelfarasia from Egypt, heretofore known only from the lower dentition. Here we employ high-resolution computed tomography to reveal the morphology of the maxillary post-canine dentition of Widanelfarasia, and describe fragmentary dental and mandibular remains of early Oligocene Jawharia (gen. nov.) and Eochrysochloris (gen. nov.). The upper molar dentition of Widanelfarasia provides evidence for an intermediate morphological stage between moderate dilambdodonty and incipient zalambdodonty. Phylogenetic analysis employing the morphological character matrix of Asher and Hofreiter (2006) places Widanelfarasia within crown Tenrecoidea, but an alternative placement of that genus as a stem tenrecoid could not be statistically rejected. Additional support for the latter hypothesis, and for the hypothesis of convergent evolution of zalambdodonty within Afrosoricida, is provided by Eochrysochloris gen. nov., which shares apomorphic premolar features with Miocene Prochrysochloris and extant chrysochlorids, but retains a well-developed talonid basin on its lower molars. Jawharia gen. nov. is interpreted as an advanced stem tenrecoid that provides additional support for the hypothesis that tenrecoid zalambdodonty evolved from moderate dilambdodonty. Some of the apomor-phic morphological features shared by Widanelfarasia and early Miocene Protenrec are also seen in Todralestes, from the oldest (late Paleocene) placental mammal-bearing locality in Africa. As such Todralestes may be a stem or crown afrosoricid, and, if so, the oldest known Afro-Arabian member of Afrotheria.
Article
Full-text available
Estimated phylogenies of evolutionarily diverse taxa will be well supported and more likely to be historically accurate when the analysis contains large amounts of data-many genes sequenced across many taxa. Inferring such phylogenies for non-model organisms is challenging given limited resources for whole-genome sequencing. We take advantage of genomic data from a single species to test the limits of hybridization-based enrichment of hundreds of exons across frog species that diverged up to 250 million years ago. Enrichment success for a given species depends greatly on the divergence time between it and the reference species, and the resulting alignment contains a significant proportion of missing data. However, our alignment generates a well-supported phylogeny of frogs, suggesting that this technique is a practical solution towards resolving relationships across deep evolutionary time.
Article
Full-text available
The Lemudong'o Formation is defined here as part of a late Miocene to Late Pleistocene sequence of stratified lavas, air-fall and waterlain tuffs, lacustrine, alluvial, and fluvial sediments, and paleosols, that crop out over an approximately 25 3 50 km area on the western margin of the southern Kenyan Rift Valley, approximately 100 km west of Nairobi. The study area is deeply incised by three major permanent river systems that expose sediments of three late Neogene lake basins. The Lemudong'o Formation comprises deposits of the second paleolake basin, which formed during the late Miocene. Stratigraphic sections in several localities are described and correlated in this report, the Lemudong'o Formation is defined, and a basin sedimentary history and environmental reconstruction is proposed. The Lemudong'o Formation has three main phases of sedimentation with a total thickness of 135 m. Phase 1 is represented by predominantly lacustrine and lake-margin siltstones, mudstones, and sandstones. Phase 2 comprises paleosols in the basin center, and fluvial and alluvial sediments on the eastern basin margin. Phase 3 comprises mainly waterlain tuffs and silts, capped by a welded tuff. Phase 2 may reflect a more arid climate, or a lower basin-overflow elevation. Four tuffs in upper phase-1 mudstones in Lemudong'o Gorge are dated to 6.12-6.08 Ma. The main fossil-bearing horizons at Lemudong'o Gorge Locality 1 lie between, and immediately above, the dated tuffs. Fossils are associated with beach and/or deltaic sands and fine gravels, and silty and sandy claystones representative of an intermittently flooded lake margin.
Article
Full-text available
A small sample of hyracoid fossils from the late Miocene (,6.1 Ma) deposits at Lemudong'o, Narok, Kenya, belong to Dendrohyrax. This genus was unknown in the fossil record until recently, when almost simultaneously it was discovered at Lukeino (6 Ma) and Lemudong'o, both in Kenya. The fossils from Lemudong'o belong to a small species of the genus, not very different from Dendrohyrax validus. The Lukeino specimens are larger, and have been attributed to a new species Dendrohyrax samueli. The presence of tree hyraxes at these sites is indicative of forest at the time of deposition of the strata.
Article
Full-text available
DNA hybridization capture combined with next generation sequencing can be used to determine the sequences of hundreds of target genes across hundreds of individuals in a single experiment. However, the approach has thus far only been successfully applied to capture targets that are highly similar in sequence to the bait molecules. Here we introduce modifications that extend the reach of the method to allow efficient capture of highly divergent homologous target sequences using a single set of baits. These modifications have important implications for comparative biology.
Article
Full-text available
Background Secondary edentulism (toothlessness) has evolved on multiple occasions in amniotes including several mammalian lineages (pangolins, anteaters, baleen whales), birds, and turtles. All edentulous amniote clades have evolved from ancestors with enamel-capped teeth. Previous studies have documented the molecular decay of tooth-specific genes in edentulous mammals, all of which lost their teeth in the Cenozoic, and birds, which lost their teeth in the Cretaceous. By contrast with mammals and birds, tooth loss in turtles occurred in the Jurassic (201.6-145.5 Ma), providing an extended time window for tooth gene degradation in this clade. The release of the painted turtle and Chinese softshell turtle genomes provides an opportunity to recover the decayed remains of tooth-specific genes in Testudines. Results We queried available genomes of Testudines (Chrysemys picta [painted turtle], Pelodiscus sinensis [Chinese softshell turtle]), Aves (Anas platyrhynchos [duck], Gallus gallus [chicken], Meleagris gallopavo [turkey], Melopsittacus undulatus [budgerigar], Taeniopygia guttata [zebra finch]), and enamelless mammals (Orycteropus afer [aardvark], Choloepus hoffmanni [Hoffmann’s two-toed sloth], Dasypus novemcinctus [nine-banded armadillo]) for remnants of three enamel matrix protein (EMP) genes with putative enamel-specific functions. Remnants of the AMBN and ENAM genes were recovered in Chrysemys and retain their original synteny. Remnants of AMEL were recovered in both testudines, although there are no shared frameshifts. We also show that there are inactivated copies of AMBN, AMEL and ENAM in representatives of divergent avian lineages including Galloanserae, Passeriformes, and Psittaciformes, and that there are shared frameshift mutations in all three genes that predate the basal split in Neognathae. Among enamelless mammals, all three EMP genes exhibit inactivating mutations in Orycteropus and Choloepus. Conclusions Our results highlight the power of combining fossil and genomic evidence to decipher macroevolutionary transitions and characterize the functional range of different loci involved in tooth development. The fossil record and phylogenetics combine to predict the occurrence of molecular fossils of tooth-specific genes in the genomes of edentulous amniotes, and in every case these molecular fossils have been discovered. The widespread occurrence of EMP pseudogenes in turtles, birds, and edentulous/enamelless mammals also provides compelling evidence that in amniotes, the only unique, non-redundant function of these genes is in enamel formation.
Article
Full-text available
Sea cows (manatees, dugongs) are the only living marine mammals to feed solely on aquatic plants. Unlike whales or dolphins (Cetacea), the earliest evolutionary history of sirenians is poorly documented, and limited to a few fossils including skulls and skeletons of two genera composing the stem family of Prorastomidae (Prorastomus and Pezosiren). Surprisingly, these fossils come from the Eocene of Jamaica, while stem Hyracoidea and Proboscidea - the putative sister-groups to Sirenia - are recorded in Africa as early as the Late Paleocene. So far, the historical biogeography of early Sirenia has remained obscure given this paradox between phylogeny and fossil record. Here we use X-ray microtomography to investigate a newly discovered sirenian petrosal from the Eocene of Tunisia. This fossil represents the oldest occurrence of sirenians in Africa. The morphology of this petrosal is more primitive than the Jamaican prorastomids' one, which emphasizes the basal position of this new African taxon within the Sirenia clade. This discovery testifies to the great antiquity of Sirenia in Africa, and therefore supports their African origin. While isotopic analyses previously suggested sirenians had adapted directly to the marine environment, new paleoenvironmental evidence suggests that basal-most sea cows were likely restricted to fresh waters.
Article
Full-text available
Phylogenetic relationships, divergence times, and patterns of biogeographic descent among primate species are both complex and contentious. Here, we generate a robust molecular phylogeny for 70 primate genera and 367 primate species based on a concatenation of 69 nuclear gene segments and ten mitochondrial gene sequences, most of which were extracted from GenBank. Relaxed clock analyses of divergence times with 14 fossil-calibrated nodes suggest that living Primates last shared a common ancestor 71-63 Ma, and that divergences within both Strepsirrhini and Haplorhini are entirely post-Cretaceous. These results are consistent with the hypothesis that the Cretaceous-Paleogene mass extinction of non-avian dinosaurs played an important role in the diversification of placental mammals. Previous queries into primate historical biogeography have suggested Africa, Asia, Europe, or North America as the ancestral area of crown primates, but were based on methods that were coopted from phylogeny reconstruction. By contrast, we analyzed our molecular phylogeny with two methods that were developed explicitly for ancestral area reconstruction, and find support for the hypothesis that the most recent common ancestor of living Primates resided in Asia. Analyses of primate macroevolutionary dynamics provide support for a diversification rate increase in the late Miocene, possibly in response to elevated global mean temperatures, and are consistent with the fossil record. By contrast, diversification analyses failed to detect evidence for rate-shift changes near the Eocene-Oligocene boundary even though the fossil record provides clear evidence for a major turnover event ("Grande Coupure") at this time. Our results highlight the power and limitations of inferring diversification dynamics from molecular phylogenies, as well as the sensitivity of diversification analyses to different species concepts.
Article
Full-text available
Nementchatherium senarhense, gen. et sp. nov. from the Middle–Late Eocene of Bir El Ater (Algeria) is described and assigned to the subfamily Herodotiinae (Macroscelidea). This genus and the other primitive elephant-shrews are compared with the Louisininae (Hyopsodontidae, Condylarthra) from the Early Paleogene of Europe. These groups have been included in a phylogenetic analysis based on dental characters, in order to clarify the origin of Macroscelidea. Phylogenetic reconstruction suggests that Louisininae are belonging in the polyphyletic Hyopsodontidae except for Microhyus which is considered here as the sister-group the Macroscelidea. These results suggest a terrestrial interchange between Africa and Eurasia during the Early Eocene. The phylogenetic analysis suggests also that the Macroscelidea-Microhyus clade is closely related to the Proboscidea. Like molecular phylogenies, especially those concerning the African molecular clade (=Afrotheria), our results, provide evidence for a macroscelid-tethytherian relationship. However, if the Macroscelidea emerged from European “condylarth” at the Early Eocene as our data suggest, the Proboscidea are already differentiated in Africa during this period. Then, it seems that Macroscelidea and Proboscidea are paraphyletic. The assumption of a unique group of condylarthran type at the origin of Afrotheria (macroscelids, tethytherians, tubulidentates, tenrecid and chrysochlorid insectivores) cannot be excluded, but the current paleontological data do not fit with that hypothesis.