Hyena paleogenomes reveal a complex evolutionary history of cross-continental gene flow between spotted and cave hyena

Abstract

The genus Crocuta (African spotted and Eurasian cave hyenas) includes several closely related extinct and extant lineages. The relationships among these lineages, however, are contentious. Through the generation of population-level paleogenomes from late Pleistocene Eurasian cave hyena and genomes from modern African spotted hyena, we reveal the cross-continental evolutionary relationships between these enigmatic hyena lineages. We find a deep divergence (~2.5 Ma) between African and Eurasian Crocuta populations, suggesting that ancestral Crocuta left Africa around the same time as early Homo. Moreover, we find discordance between nuclear and mitochondrial phylogenies and evidence for bidirectional gene flow between African and Eurasian Crocuta after the lineages split, which may have complicated prior taxonomic classifications. Last, we find a number of introgressed loci that attained high frequencies within the recipient lineage, suggesting some level of adaptive advantage from admixture.

Palaeoproteomic analysis of Pleistocene cave hyenas from east Asia

“…With more samples analyzed in the future, the phylogenetic relationships between modern spotted hyenas and east Asian cave hyenas could be confirmed or modified. The Bayesian analysis carried out in BEAST indicates that all the analyzed spotted hyenas, including modern individuals from northern and southern Africa and fossils from east Asia, share the most recent common ancestor (tMRCA) at ~ 2.77 Ma, which agrees well with the time estimated from nuclear genomes 12 . Furthermore, based on the divergence time between the SYZ and the northern African individuals (Fig.…”

“…The phylogenies constructed from both of our proteomic datasets indicate the Namibian individual as a basal lineage, which agrees with the result of gene flow analysis, i.e. the Namibian individual contained the fewest windows of gene flow from cave hyenas compared with other modern individuals12 . Moreover, considering the amino acid substitutions in the Crocuta populations (seeSupplementary Information), the Namibian individual represented the ancestral type of amino acid (Isoleucine, i.e.…”

“…www.nature.com/scientificreports/ and mitochondrial phylogenies was interpreted as putative gene flow12 , which could also fit the case of east Asia here. The phylogenies constructed from both of our proteomic datasets indicate the Namibian individual as a basal lineage, which agrees with the result of gene flow analysis, i.e.…”

“…As no annotated complete genome of the Hyaenidae species was available online at the time, a homologous proteome from domestic cat (Felis catus; GenBank assembly accession: GCA_000181335; number of protein sequences = 32,891) was downloaded from Uniprot as a reference database to obtain the bone and dentine proteomes of these Pleistocene samples. The raw data were run against the entire domestic cat proteome database with the addition of a selected group of common bone and dentine proteins from Carnivora, especially the family Hyaenidae, which were manually translated from published genomes 12,57 . Common contaminants were included in the database as well.…”

Early Pleistocene origin and extensive intra-species diversity of the extinct cave lion

“…Our results suggest that cave lions diverged from present-day lions early during the Pleistocene, a period that appears to be important in the diversification of a number of other megafaunal species (e.g. cave bears from their sister clade, the brown and polar bears, 1.59 mya 17 ; the main mammoth clades, ~ 2.0–1.0 mya 18 ; the split between African and Eurasian hyena populations, ~ 2.5 mya, 19 ). This result is in line with previous studies that have hypothesised that cave lions and modern lions are distinct species, based on morphological 5 and genetic data 9 .…”