Ancient DNA reveals multiple origins and migration waves of extinct Japanese brown bear lineages

Abstract

Little is known about how mammalian biogeography on islands was affected by sea-level fluctuations. In the Japanese Archipelago, brown bears ( Ursus arctos ) currently inhabit only Hokkaido, the northern island, but Pleistocene fossils indicate a past distribution throughout Honshu, Japan's largest island. However, the difficulty of recovering ancient DNA from fossils in temperate East Asia has limited our understanding of their evolutionary history. Here, we analysed mitochondrial DNA from a 32 500-year-old brown bear fossil from Honshu. Our results show that this individual belonged to a previously unknown lineage that split approximately 160 Ka from its sister lineage, the southern Hokkaido clade. This divergence time and fossil record suggest that brown bears migrated from the Eurasian continent to Honshu at least twice; the first population was an early-diverging lineage (greater than 340 Ka), and the second migrated via Hokkaido after approximately 160 Ka, during the ice age. Thus, glacial-age sea-level falls might have facilitated migrations of large mammals more frequently than previously thought, which may have had a substantial impact on ecosystem dynamics in these isolated islands.

The origins and diversification of Holarctic brown bear populations inferred from genomes of past and present populations

“…This suggests population continuity in these regions over at least the last 11,000 to 50,000 years. Population continuity in North America and Japan is in contrast with previous hypotheses of multiple migration events based on mitochondrial genomes [9,11]. However, as we uncovered large after the end of the Pleistocene, and before the mid-Holocene.…”

“…In contemporary North American brown bears, three genetically divergent mitochondrial lineages have been described, leading to the hypothesis of three independent colonisation events from Eurasia [9]. In addition, independent colonisation events have also been hypothesised for Asia; timing of divergence estimated from mitochondrial genomes retrieved from Japanese brown bears have led to suggestions that brown bears migrated from mainland Eurasia to Japan at least twice [11]. However, the mitochondrial genome represents just a single loci, is exclusively maternally inherited, and may be heavily confounded by gene flow and incomplete lineage sorting [12,13], which can lead to erroneous inferences.…”

Complex population history affects admixture analyses in nine‐spined sticklebacks

“…An accurate picture of the historical relationships among contemporary populations is the foundation for all evolutionary inference. Due to climatic oscillations, multiple waves of colonization and admixture are common in the wild (Hudson et al, 2021 ; Marques, Lucek, et al, 2019 ; Schenekar et al, 2014 ; Segawa et al, 2021 ; Shirsekar et al, 2021 ) and many analytical methods can be seriously misled unless the resulting population structure and demographic history are correctly accounted for (Gompert & Buerkle, 2016 ; Lange, 2021 ; Scerri et al, 2018 ; Theunert & Slatkin, 2017 ; Vitti et al, 2013 ). The results of the current study provide a case in point: our analyses uncovered an unexpectedly complicated history of northern European sticklebacks pointing to multiple historical invasions and admixture events.…”

Paleogenomics reveals independent and hybrid origins of two morphologically distinct wolf lineages endemic to Japan

“…Similar to the above-mentioned possibility that wolf populations expanded into the Japanese archipelago several times, it was recently reported that the now-extinct Honshu brown bear also came into existence on Honshu via multiple migrations of ancient lineages from Eurasia to Honshu. 43 Thus, the mammalian fauna of the Japanese archipelago may have ''multi-layered'' histories of migrations as a consequence of the land connections that formed intermittently between the Japanese islands and Eurasia during the Pleistocene, and this is one of the most important topics of ongoing research with ancient DNA.…”