Holocene deglaciation drove rapid genetic diversification of Atlantic walrus

Abstract

Rapid global warming is severely impacting Arctic ecosystems and is predicted to transform the abundance, distribution and genetic diversity of Arctic species, though these linkages are poorly understood. We address this gap in knowledge using palaeogenomics to examine how earlier periods of global warming influenced the genetic diversity of Atlantic walrus (Odobenus rosmarus rosmarus), a species closely associated with sea ice and shallow-water habitats. We analysed 82 ancient and historical Atlantic walrus mitochondrial genomes (mitogenomes), including now-extinct populations in Iceland and the Canadian Maritimes, to reconstruct the Atlantic walrus' response to Arctic deglaciation. Our results demonstrate that the phylogeography and genetic diversity of Atlantic walrus populations was initially shaped by the last glacial maximum (LGM), surviving in distinct glacial refugia, and subsequently expanding rapidly in multiple migration waves during the late Pleistocene and early Holocene. The timing of diversification and establishment of distinct populations corresponds closely with the chronology of the glacial retreat, pointing to a strong link between walrus phylogeography and sea ice. Our results indicate that accelerated ice loss in the modern Arctic may trigger further dispersal events, likely increasing the connectivity of northern stocks while isolating more southerly stocks putatively caught in small pockets of suitable habitat.

Keywords: Arctic; Odobenus rosmarus rosmarus; ancient DNA; environmental change; marine mammals; palaeogenetics.

Figure 1.

The divergence and radiation of the Atlantic walrus. Time-calibrated Bayesian phylogeny for 82 ancient and historical Atlantic walrus mitogenomes. Tips are colour-coded according to geographical origin corresponding to the map insert and placed in the phylogeny according to the age of the specimen. Posterior probability values are provided at each node with nodes greater than 80% of posterior support marked by black dots. The Pacific walrus was included as an outgroup and putative clade names (e.g. E1) are provided as reference for the discussion. Numbers 1–7 on the time scale refer to key climatic events in the North Atlantic. Walrus illustration by Elena Kakoshina (artkakos.com). All sample information is listed in electronic supplementary material, table S1, and additional details on the phylogenetic analyses provided in electronic supplementary material, figure S1 and tables S2–S4.

Figure 2.

Hypothesized glacial refugia and Holocene expansion of walrus. Hypothesized LGM refugia for Atlantic walrus in the eastern, western and northwestern Atlantic (grey circles) and subsequent Holocene expansion and diversification (full arrows), coloured according to sample origins in the phylogeny. A 0 kya map reflects their current distribution based on [57,67,68,79,80]. The alternative to a Northwest refugia is an early migration from east to west (stippled arrow). Ice sheet time series adapted from [–66] with basemaps from ETOPO1 Arc-Minute Global Relief Model available at https://www.ngdc.noaa.gov/mgg/global/ and modified using Inkscape (https://inkscape.org/). Additional time periods provided in electronic supplementary material, figure S3.

Figure 3.

Demographic history and genetic diversity in the Atlantic walrus. (a) Haplotype network of 82 ancient and historical walrus mitogenomes. Circles are sized according to the number of individuals sharing the same haplotype, and the number of mutations between each haplotype is defined by the hatched lines. (b,c) Bayesian skyline plots (BSP) for the western clade (n = 36) and for the eastern clade (n = 39), respectively. (d,e) Mitochondrial nucleotide and haplotype diversity estimated for each of the seven main walrus populations. Error bars indicate standard deviations. Colours in a, d and e reflect geographical origin.