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. 2020 Dec 21;30(24):5018-5025.e5.
doi: 10.1016/j.cub.2020.09.051. Epub 2020 Oct 15.

Genomic Adaptations and Evolutionary History of the Extinct Scimitar-Toothed Cat, Homotherium latidens

Ross Barnett  1 , Michael V Westbury  2 , Marcela Sandoval-Velasco  1 , Filipe Garrett Vieira  1 , Sungwon Jeon  3 , Grant Zazula  4 , Michael D Martin  5 , Simon Y W Ho  6 , Niklas Mather  6 , Shyam Gopalakrishnan  7 , Jazmín Ramos-Madrigal  7 , Marc de Manuel  8 , M Lisandra Zepeda-Mendoza  9 , Agostinho Antunes  10 , Aldo Carmona Baez  1 , Binia De Cahsan  1 , Greger Larson  11 , Stephen J O'Brien  12 , Eduardo Eizirik  13 , Warren E Johnson  14 , Klaus-Peter Koepfli  15 , Andreas Wilting  16 , Jörns Fickel  17 , Love Dalén  18 , Eline D Lorenzen  7 , Tomas Marques-Bonet  19 , Anders J Hansen  20 , Guojie Zhang  21 , Jong Bhak  22 , Nobuyuki Yamaguchi  23 , M Thomas P Gilbert  24
Affiliations

Genomic Adaptations and Evolutionary History of the Extinct Scimitar-Toothed Cat, Homotherium latidens

Ross Barnett et al. Curr Biol. .

Abstract

Homotherium was a genus of large-bodied scimitar-toothed cats, morphologically distinct from any extant felid species, that went extinct at the end of the Pleistocene [1-4]. They possessed large, saber-form serrated canine teeth, powerful forelimbs, a sloping back, and an enlarged optic bulb, all of which were key characteristics for predation on Pleistocene megafauna [5]. Previous mitochondrial DNA phylogenies suggested that it was a highly divergent sister lineage to all extant cat species [6-8]. However, mitochondrial phylogenies can be misled by hybridization [9], incomplete lineage sorting (ILS), or sex-biased dispersal patterns [10], which might be especially relevant for Homotherium since widespread mito-nuclear discrepancies have been uncovered in modern cats [10]. To examine the evolutionary history of Homotherium, we generated a ∼7x nuclear genome and a ∼38x exome from H. latidens using shotgun and target-capture sequencing approaches. Phylogenetic analyses reveal Homotherium as highly divergent (∼22.5 Ma) from living cat species, with no detectable signs of gene flow. Comparative genomic analyses found signatures of positive selection in several genes, including those involved in vision, cognitive function, and energy consumption, putatively consistent with diurnal activity, well-developed social behavior, and cursorial hunting [5]. Finally, we uncover relatively high levels of genetic diversity, suggesting that Homotherium may have been more abundant than the limited fossil record suggests [3, 4, 11-14]. Our findings complement and extend previous inferences from both the fossil record and initial molecular studies, enhancing our understanding of the evolution and ecology of this remarkable lineage.

Keywords: Homotherium; adaptation; ancient DNA; comparative genomes; diversity; genomics; palaeogenome; paleogenome; phylogeny; selection.

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Conflict of interest statement

Declaration of Interests The authors declare no competing interests.

Figures

None
Graphical abstract
Figure 1
Figure 1
Evolutionary Time-Tree of 17 Cats and Two Hyenas Tree topology inferred using both RAxML and ASTRAL-II, with node ages estimated using a Bayesian relaxed-clock analysis of concatenated sequences of 21,034 exons (total length 29,216,712 bp) (Figure S1). A separate correlated-rates relaxed clock was applied to each of the three codon positions. Relative frequencies of the three possible bipartitions (possible arrangements of a quartet on an unrooted tree) are shown for the internal branch containing Homotherium (branch 12) and the remaining nodes in Figure S2. Dashed lines show the threshold value of one-third, shown theoretically to be the minimum frequency for a true bipartition. Relevant branch labels have been given based on those in Figure S2. Blue horizontal bars represent 95% credibility intervals of node times. Blue circles indicate internal nodes with fossil-based age constraints. A geological timescale is shown below the tree (Q. = Quaternary, Pl. = Pliocene, Ps. = Pleistocene). Ages of key nodes in the phylogeny can be found in Table S1.
Figure 2
Figure 2
Depiction of 18 of the 31 Genes under Positive Selection with High Values (Free Ratio > 2) in the Homotherium Genome Hypothetical functions and the adaptive insights that these provide on the species’ behavior, morphology, and functional adaptations are also shown. Additional genes not depicted here are likely involved in cellular processes such as apoptosis, protein synthesis, and protein signaling, as well as immunity/cancer, olfaction, and reproduction (Table S3). All genes showing significant signs of positive selection can be seen in Table S2.
Figure 3
Figure 3
Autosome-wide Heterozygosity Estimates for Each Species Included in the Current Study Variance was estimated by calculating the average heterozygosity for each scaffold independently. Colors represent the genus that each individual belongs to (red: Homotherium; cyan: Acinonyx; green: Caracal; yellow: Felis; gray: Lynx; white: Neofelis; blue: Panthera; pink: Prionailurus). Exome-wide heterozygosity can be seen in Figure S3.
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References

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    1. Rawn-Schatzinger V. Illinois State Museum Reports of Investigations; 1992. The scimitar cat, Homotherium serum cope: osteology, functional morphology, and predatory behavior. pp. 1–80.

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