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The Extreme Life Of A Sloth

The pleiotropic GNB3 [ 46 , 47 ] is the only gene that has remained functional in all rod monochromats examined figure 2. Horizontal bars indicate geological ranges of the oldest xenarthran Riostegotherium , glyptodont Glyptatelus and pilosan fossils Pseudoglyptodon. Patterns of protein loss in the phototransduction cascades of various mammals.

Accession numbers for all sequences can be found in the electronic supplementary material, table S6. Robertson et al. The presence of rod monochromacy has major implications for understanding xenarthran behavioural ecology and evolution.

Daggers indicate extinct taxa. Rod monochromacy represents an extreme retinal adaptation to dim-light conditions because rods, not cones, are activated when very few photons are kohl 39; s sloth. Results were assembled into kohl 39; s sloth with the de novo assembly tool in G eneious. Inactivation times of pseudogenes were estimated using previously described methods [ 730 ].

This web page for crown Xenarthra, Pilosa anteaters and slothsVermilingua anteaters and Folivora sloths are kohl 39; s sloth from [ 31 ]; date for crown armadillos is from [ 48 ]. DNA alignments uploaded as electronic supplementary material, dataset S1.

We estimate that this was inactivated in a stem xenarthran approximately 95 Ma figure 3 ; electronic supplementary material, table S4. Mylodon darwinii 's low coverage genome was examined only for genes that are pseudogenic in C. For C. The absence of an arrow indicates the predicted disruption of that portion of the cascade.

We performed PCR and Sanger sequencing on cone phototransduction genes of 10 additional xenarthrans to test for shared inactivating mutations and estimated the timing of inactivation for photoreceptor pseudogenes. We confirmed that this mutation is present in two additional sloths Bradypus tridactylus pale-throated three-toed slothCholoepus didactylus Linnaeus' two-toed sloth and five armadillos Euphractus sexcinctus six-banded armadilloChaetophractus villosus big hairy armadilloTolypeutes matacus southern three-banded armadilloPriodontes maximus giant armadilloZaedyus pichiy pichi figure 1.

Molecular timetrees suggest that xenarthrans last shared a common ancestor near the K-Pg boundary [ 3148 ]. Therefore a long history of extreme dim-light conditions is predicted to eliminate the function of cones via directional selection for a higher density of rods or relaxed selection on the maintenance of cones.

The presence of rod monochromacy in galway poker festival 2020 should be taken into account in future behavioural, ecological and conservation studies involving this enigmatic lineage of mammals. Most xenarthran species do not occupy dim-light niches [ 12 ], but all three groups of xenarthrans are reported in behavioural [ 13 — 18 ] and anatomical studies [ 19 — 22 ] to have vision consistent with rod monochromacy wherein the retina link cones entirely.

Paintings by Carl Buell copyright John Gatesy. Kohl 39; s sloth a molecular phylogenetic method to date gene inactivations [ 27 ], we estimated that SWS1 was pseudogenized approximately 80 Ma in a stem xenarthran figure 3 ; electronic supplementary material, table S4rendering the earliest crown xenarthrans at most LWS-cone monochromats.

Proc Biol Sci. Electrophysiological, molecular and genetic techniques have greatly increased our knowledge of the retinal basis for vision in mammals [ 1 — 4 ]. Christopher A.

We assumed phylogenetic relationships and divergence time global means from [ 31 ] for these calculations. These findings indicate that xenarthrans inhabited an extreme dim-light niche early in their evolution, which we suggest was a subterranean habit given fossorial adaptations in fossil and many living xenarthrans. Though extant anteaters and sloths are terrestrial to arboreal, xenarthran synapomorphies include features that reflect a fossorial ancestry: strongly curved claws; a secondary scapular spine, allowing for a stronger retraction of the humerus [ 75 ]; plus a synsacrum and lateral accessory articulations of the lumbar vertebrae, which help stabilize the body while digging [ 76 , 77 ]. Additionally, as xenarthrans are frequently the victims of vehicular collisions [ 17 ], awareness of their degenerate vision should aid in their conservation. For comparison, we searched for cone phototransduction genes in the genomes of two known rod monochromats Physeter macrocephalus giant sperm whale and Balaenoptera acutorostrata minke whale , a xenarthran analogue Manis pentadactyla Chinese pangolin and an LWS-cone monochromat Tursiops truncatus bottlenose dolphin electronic supplementary material, dataset S1. We propose that the loss of SWS1 and GRK7 in stem xenarthrans, and the subseqent, independent loss of cones in pilosans and armadillos, respectively, is a consequence of early xenarthrans passing through a subterranean bottleneck. The loss of additional cone classes is relatively common and has evolved independently in assorted nocturnal, aquatic and subterranean mammals [ 3 , 6 , 7 ]. The alignments used for the analyses can be found in the electronic supplementary material, dataset S2. This estimate predates the earliest unambiguous pilosan fossils No inactivating mutations in exons 4 and 5 of PDE6C were shared by all armadillos electronic supplementary material, table S3 , but our estimates for the inactivation of SWS1 Rod monochromacy is characterized by the complete absence of cones and results in complete colourblindness with poor visual acuity in dim-light and total blindness in bright-light conditions. Green, frameshift deletion; yellow, frameshift insertion; blue, premature stop codon; purple, splice site mutation; red, P23L missense mutation. We used BLASTN to search the publically available genomes of Dasypus novemcinctus nine-banded armadillo and Choloepus hoffmanni Hoffmann's two-toed sloth for DNA sequences of cone and rod phototransduction genes, other cone- and rod-specific genes and genes expressed in both rods and cones electronic supplementary material, dataset S1. Sequences with splice site mutations alone were not considered pseudogenes owing to the possibility of functional splice variants. Dasypus novemcinctus , C. Using genomic and phylogenetic methods, we tested the hypotheses that xenarthrans are rod monochromats and that this condition was inherited from a common ancestor. We concluded that a stem xenarthran became an long-wavelength sensitive-cone monochromat following a missense mutation at a critical residue in SWS1 , and a stem cingulate armadillos, glyptodonts and pampatheres and stem pilosan sloths and anteaters independently acquired rod monochromacy early in their evolutionary history following the inactivation of LWS and PDE6C , respectively. Colours of horizontal and vertical bars correspond to the colours of the geological strata at the bottom of the figure. After aligning exon sequences for D. By contrast, all rod-specific genes are intact electronic supplementary material, table S1. Only recently have genomic studies confirmed rod monochromacy in mammals [ 6 , 7 ], suggesting that this is a plausible phenotype for xenarthrans. As a result, xenarthrans probably use vision only at night, twilight and in burrows, though species that dwell in the understory of South America's rainforests may experience low enough levels of light during the day to facilitate limited vision. Consistent with this hypothesis, it has only been discovered in deep-sea fishes [ 59 ], deep diving whales [ 6 ] and subterranean vertebrates [ 7 , 60 ]. Choloepus , Choloepus hoffmanni , unless otherwise noted. Dasypus novemcinctus and C. For the comparison groups, M. Blue and red symbols correspond to intact and inactivated cone phototransduction genes, respectively. Choloepus hoffmanni , M. Dashed branches arbitrarily connect to the earliest occurrence of extinct taxa and should not be interpreted as divergence time estimates. Journal List Proc Biol Sci v. To test this hypothesis, we performed PCR and successfully sequenced exons 4 and 5 in 10 and 9 xenarthrans, respectively. Xenarthrans armadillos Cingulata , sloths Folivora and anteaters Vermilingua have been overlooked in vision research, despite being an ancient and evolutionarily distinct lineage of mammals [ 8 — 11 ]. As inactivated PDE6C leads to rod monochromacy in vertebrates [ 41 — 43 ], these shared mutations suggest that rod monochromacy originated in an ancestor to Xenarthra. The numbering of the nucleotide positions corresponds to those in the electronic supplementary material, dataset S1, and includes artificial gaps after frameshift insertions to maintain the original reading frame. Our results suggest that xenarthrans have a long history of rod monochromacy and that the most recent common ancestor of Xenarthra was at most an LWS-cone monochromat. National Center for Biotechnology Information , U. Specifically, rod monochromacy and modifications to the postcranium related to fossoriality probably prevented diversification into various locomotory types e. The morphological and palaeontological evidence of ancestral fossoriality, coupled with the loss of SWS1 and GRK7 in a stem xenarthran and rod monochromacy in early cingulates and pilosans, argues for a subterranean lifestyle in the earliest xenarthrans. Black symbols correspond to rod phototransduction proteins. We searched the genomes of Dasypus novemcinctus nine-banded armadillo , Choloepus hoffmanni Hoffmann's two-toed sloth and Mylodon darwinii extinct ground sloth for retinal photoreceptor genes and examined them for inactivating mutations. Burrowing armadillos, ground sloths and pampatheres might have been pre-adapted to the low-light conditions underground. The exceptions are PDE6H [ 44 ] and GNB3 cone transducin beta subunit; [ 45 ] , which lead to partial rod monochromacy and reduced light-sensitivity in their respective absence. Cone photoreceptors—responsible for high acuity, colour vision in bright light—typically possess one of four spectral classes of photopigment called opsins. Examples of inactivating mutations for all retinal genes found to be inactivated in one or more xenarthrans. Rod monochromacy is a rare condition in vertebrates characterized by the absence of cone photoreceptor cells. Though pure-rod retinae have long been described in mammals [ 20 ], these reports have typically been refuted by the results of molecular and genetic studies e. Fossoriality in Mesozoic mammals is not without precedent and several lineages of Mesozoic synapsids are inferred to have exhibited burrowing behaviour [ 62 — 65 ]. Yet xenarthrans represent the only extant lineage of mammals that appear to have disposed of SWS1 prior to the end of the Mesozoic approximately A timetree depicting the loss of photoreceptor genes in xenarthrans. Small vertical bars correspond to the averaged inactivation estimates for each gene electronic supplementary material, table S4. The rod monochromats B. These losses presumably are a consequence of inhabiting dim-light niches in which colour discrimination is limited and provide well-documented cases of convergent, regressive evolution [ 2 , 3 , 6 , 7 ]. We hypothesize that rod monochromacy in armadillos and pilosans evolved as an adaptation to a subterranean habitat in the early history of Xenarthra. Besides xenarthrans, the latter character is present only in the subterranean Mesozoic mammal Fruitafossor [ 64 ]. Owing to the relatively high frequency of GC as an alternative splice donor in mammals [ 29 ], this variant was not considered an inactivating mutation. The retention of all other rod-specific genes in C. The origins of crown armadillos, sloths and anteaters are indicated by the vertical widening of the branches leading to their representative taxa. This provides evidence of the earliest acquisition of LWS-cone monochromacy in mammals electronic supplementary material, table S5. Contig assembly was performed in G eneious using the M uscle alignment tool [ 28 ]. However, the putative shared mutations appear to be convergent as they are absent in all armadillos that were examined except D. We thank four anonymous reviewers for comments on an earlier stage of our manuscript. All putative mutations were compared to outgroups to determine whether they were uniquely derived. Early reports of xenarthrans armadillos, sloths and anteaters suggest that they are rod monochromats, but this has not been tested with genomic data. A proline is present in all opsins across vertebrates [ 49 ], with missense mutations in rod opsin RH1 resulting in a non-functional pigment in vitro P23H [ 50 ] , progressive photoreceptor degeneration in vivo P23H [ 51 , 52 ] , reduction in chromophore yield owing to a decrease in cell-surface transportation P23H, P23L [ 53 ] and high amounts of misfolding, with P23L having the highest degree of misfolding among seven RH1 mutants [ 54 ]. These results, combined with previous studies [ 7 , 32 ], confirm that rod monochromats are unique in having inactivated cone phototransduction genes, with the exception of SWS1 in LWS-cone monochromats figure 2. Species not reported on in this paper are from references [ 7 , 32 ]. The presence of multiple cone opsins allows for the comparison of different wavelengths of light, whereas the dim-light sensitive rod photoreceptors possess a single type of opsin, precluding hue discrimination. Extinct glyptodonts might have compensated for their presumed inability to see approaching predators with their tough carapace and enormous size. The resulting phenotype is colourblindness and low acuity vision in dim-light and blindness in bright-light conditions. We were unable to amplify the exon containing this mutation in two anteaters Myrmecophaga tridactyla giant anteater and Tamandua tetradactyla southern tamandua , but confirmed that SWS1 is pseudogenic in these species electronic supplementary material, tables S2 and S3. We suggest that passage through this hypothesized subterranean bottleneck is a historical contingency that constrained xenarthran evolution. Rod monochromacy is characterized by low acuity and a complete lack of colour discrimination in dim-light, and blindness during the day hemeralopia , as rod cells become saturated in bright light.