Whole genome analysis of clouded leopard species reveals an ancient divergence and distinct demographic histories

Bursell, Madeline G.; Dikow, Rebecca B.; Figueiró, Henrique V.; Dudchenko, Olga; Flanagan, Joseph P.; Aiden, E; Goossens, Benoît; Nathan, Senthilvel K. S. S.; Johnson, Warren E.; Koepfli, Klaus‐Peter; Frandsen, Paul B.

doi:10.1016/j.isci.2022.105647

Cited by 6 publications

(7 citation statements)

References 67 publications

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“…However, the clouded leopards’ highly arboreal adaptations have limited their distribution to tropical forests ( 23 ), which is consistent with the limited fossil record ( 7 , 24 ). The estimated divergence between Neofelis species (1.39 to 3.27 Ma) agrees with the previous estimates based on both nuclear and mitochondrial datasets ( 1 , 15 ) but challenges a recent study ( 25 ). The earliest clouded leopard fossils are reported from late the Pleistocene and Holocene ( 3 ) of Southeast Asia and Central China ( 26 ).…”

Section: Resultssupporting

confidence: 81%

How genomic insights into the evolutionary history of clouded leopards inform their conservation

Yuan,

Wang,

Zhao

et al. 2023

Sci. Adv.

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Clouded leopards ( Neofelis spp.), a morphologically and ecologically distinct lineage of big cats, are severely threatened by habitat loss and fragmentation, targeted hunting, and other human activities. The long-held poor understanding of their genetics and evolution has undermined the effectiveness of conservation actions. Here, we report a comprehensive investigation of the whole genomes, population genetics, and adaptive evolution of Neofelis . Our results indicate the genus Neofelis arose during the Pleistocene, coinciding with glacial-induced climate changes to the distributions of savannas and rainforests, and signatures of natural selection associated with genes functioning in tooth, pigmentation, and tail development, associated with clouded leopards’ unique adaptations. Our study highlights high-altitude adaptation as the main factor driving nontaxonomic population differentiation in Neofelis nebulosa . Population declines and inbreeding have led to reduced genetic diversity and the accumulation of deleterious variation that likely affect reproduction of clouded leopards, highlighting the urgent need for effective conservation efforts.

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Section: Resultssupporting

confidence: 81%

How genomic insights into the evolutionary history of clouded leopards inform their conservation

Yuan,

Wang,

Zhao

et al. 2023

Sci. Adv.

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“…Tiger trios were mapped to the GenTig1.0 (Armstrong et al 2022) and PanTigT.MC.v3 (GCA_021130815.1; Shukla et al 2022) genomes. Clouded leopards were mapped to three genome assemblies: a short-read assembly (SaMing-1434 [GCA_027422525.1; Bursell et al 2022]) and two long-read assemblies (SNNU_Nneo_1 [GCA_030324275.1; Yuan et al 2023] and the primary haplotype assembly of mNeoNeb1 [GCA_028018385.1; Vertebrate Genomes Project 2023]). Leopard, snow leopard, and jaguar data were mapped to the most contiguous reference genome available for each respective species (leopard: Ppardus1 [GCA_024362965.1; Armstrong et al 2022]; snow leopard: PanUnc1.0 [GCF_023721935.1; Armstrong et al 2022]; jaguar: Panthera_onca_HiC [GCF_028533385.1; DNAzoo.org, Dudchenko et al 2017; Dudchenko et al 2018].…”

Section: Methodsmentioning

confidence: 99%

“…Library quality was assessed with an Agilent 4200 Tapestation and Lightcycler quantitative PCR (Roche Life Science, St. Louis, MO) and then paired-end sequenced (2 × 150 bp) to a minimum depth of 20x on an Illumina NovaSeq 6000 instrument. The genome of an additional offspring (“Sa Ming”, SB1434, brother of “Ta Moon”) was previously reported in Bursell et al 2022 (NCBI accession SRR13774417) and included in the analyses.…”

Section: Methodsmentioning

confidence: 99%

“…Generation time was set to five years for each lineage. Though we recognize these may vary based on the interpretation of generation time and various field data, we selected a generation time of five years to be consistent with previous publications which inferred demographic history using this method in the Pantherinae (Liu et al 2018; Armstrong et al 2020; Armstrong et al 2021; Bursell et al 2022; Solari et al 2023). Bin size was set to 100.…”

Section: Methodsmentioning

confidence: 99%

“…There has been significant discussion in the scientific literature regarding the timing and order of the divergence of species in the Panthera - Neofelis clade. Recent estimates suggest that the split between Panthera and Neofelis occurred roughly between 4 and 6 million years ago (Li et al 2016; Bursell et al 2022; Yuan et al 2023). However, pinpointing the exact timing of these divergence events and resolving the relationships among the species have proven difficult.…”

Section: Introductionmentioning

confidence: 99%

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Parameterizing Pantherinae: de novo mutation rate estimates from Panthera and Neofelis pedigrees

Armstrong,

Carey,

Harkess

et al. 2024

Preprint

Self Cite

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Estimates of de novo mutation rates are essential for phylogenetic and demographic analyses, but their inference has previously been impeded by high error rates in sequence data and uncertainty in the fossil record. Here, we directly estimate de novo germline mutation rates for all extant members of Panthera, as well as the closely related outgroup Neofelis nebulosa, using pedigrees. We use a previously validated pipeline (RatesTools) to calculate mutation rate for each species and subsequently explore the impacts of the novel rates on historic effective population size estimates in each of these charismatic felids of conservation concern. Importantly, we find that the choice of reference genome, the data type and coverage, and the individual all impact estimates of the mutation rate. Despite these stochastic effects, we inferred that base pair mutation rates for all species fell between 0.5 and 1.4e-08 per generation per base pair (mean 0.81e-08 +/- 0.35-08 across Pantherinae). Our results provide a cautionary view on inter-species mutation rate comparisons, given the error associated with the reference genome choice and sequencing depth of coverage of the individuals.

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Red, gold, and green: comparative genomics of polymorphic leopards from South Africa

Lagcher,

Lensing,

Bosse

et al. 2024

Evolution

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An important goal of comparative and functional genomics is to connect genetic polymorphisms to phenotypic variation. Leopards (Panthera pardus) from northern South Africa are particularly diverse, as here a unique colour morph occurs, as well as two deeply diverged southern (SA) and central African (CA) mitochondrial clades, stemming from Pleistocene refugia. Here, we present the first whole genomes of a red leopard and a black (captive) leopard, and wildtypes belonging to the CA and SA mitochondrial clades, to evaluate genome-wide diversity, divergence, and high impact mutations that may relate to their phenotype. In the black leopard, we found long runs of homozygosity (ROHs), low nucleotide diversity across the genome, and a large number of homozygous structural variants, likely resulting from inbreeding to maintain this colour morph in captivity. In red leopards, ROHs were slightly longer compared to wildtype leopards, with potential deleterious mutations relating to its phenotype, including impaired vision. When assessing population structure, we found no divergence between CA and SA leopards and the rest of Africa, whether comparing single nucleotide or structural variants. This illustrates the homogenizing effect of introgression, and highlights that although leopards in northern South Africa may be phenotypically unique, they are not genetically different.

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Whole genome analysis of clouded leopard species reveals an ancient divergence and distinct demographic histories

Cited by 6 publications

References 67 publications

How genomic insights into the evolutionary history of clouded leopards inform their conservation

How genomic insights into the evolutionary history of clouded leopards inform their conservation

Parameterizing Pantherinae: de novo mutation rate estimates from Panthera and Neofelis pedigrees

Red, gold, and green: comparative genomics of polymorphic leopards from South Africa

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