Multiple glacial refugia for cool‐temperate deciduous trees in northern East Asia: the Mongolian oak as a case study

Abstract

In East Asia, temperate forests are predicted to have retracted southward to c. 30° N during the last glacial maximum (LGM) based on fossil pollen data, whereas phylogeographic studies have often suggested glacial in situ survival of cool-temperate deciduous trees in their modern northern ranges. Here we report a study of the genetic diversity and structure of 29 natural Mongolian oak (Quercus mongolica) populations using 19 nuclear simple sequence repeat (nSSR) loci and four chloroplast DNA fragments. Bayesian clustering analysis with nSSRs revealed five groups, which were inferred by approximate Bayesian computation (ABC) to have diverged in multiple refugia through multiple glacial-interglacial cycles. Analysis of chloroplast DNA variation revealed four lineages that were largely but incompletely geographically disjunct. Ecological niche modelling (ENMs) indicated a southward range shift of the oak's distribution at the LGM, although high suitability scores were also evident in the Changbai Mts. (Northeast China), the Korean Peninsula, areas surrounding the Bohai Sea, and along the coast of the Russian Far East. In addition, endemic chloroplast DNA haplotypes and nuclear lineages occurred in high-latitude northern areas where the ENM predicted no suitable habitat. The combined evidence from nuclear and chloroplast DNA, and the results of the ENM clearly demonstrate that multiple northern refugia, including cryptic ones, were maintained across the current distributional range of the Mongolian oak during the LGM or earlier glacial periods. Though spatially limited, postglacial expansions from these refugia have led to a pattern of decreased genetic diversity with increasing latitude.

Phylogeography of postglacial range expansion in Juglans mandshurica (Juglandaceae) reveals no evidence of bottleneck, loss of genetic diversity, or isolation by distance in the leading-edge populations

“…In the Mongolian oak, high nuclear diversity, especially the private allelic richness, was found in one population of this same region, suggesting a possible cryptic refugium during the LGM (Zeng et al 2015). Our ENMs did not predict a suitable habitat in this region (Fig.…”

“…The Changbai Mountains in Northeast China as a northern refugium for cool-temperate trees has been demonstrated by several phylogeographic studies, such as Fraxinus mandshurica (Hu et al, 2008), Acer mono (Liu et al, 2014), and Quercus mongolica (Zeng et al 2015). Zhao et al (2013) investigated the chloroplast phylogeography of a temperate-deciduous forest-restricted perennial herb (Bupleurum longiradiatum) and found strong evidence for the Changbai Mountains as a long-term glacial refugium of temperate deciduous forests.…”

“…Three populations in the Korean Peninsula were fixed for one endemic chloroplast haplotype, indicating that an independent glacial refugium existed. The Baek-un-san Mountains of the Korean Peninsula, where our current JLW population is located, has already been hypothesized as a putative refugium of East Asian temperate forests (Qiu et al, 2011) despite limited available evidence due to a dearth of samples in this region (Hu et al 2008;Bai et al 2010;Liu et al 2014;Zeng et al 2015). In the most recent study of the Mongolian oak populations in continental Northeast China and the Korean Peninsula, Zeng et al (2015) found a disjunct distribution of chloroplast lineages and distinct nuclear lineages in the continental Northeast China and the Korean Peninsula, indicating the existence of a phylogeographic break between these two regions during the glacials.…”

“…Initially, temperate forests in the Northern Hemisphere were thought to have retreated southward during the glacial periods and then to have re-colonized the previously uninhabitable northern regions at the warm and wet interglacials (Hewitt, 2000(Hewitt, , 2004. However, recent phylogeographic studies of cool-temperate trees in continental East Asia have clearly shown that this southern refuge model does not apply: cool-temperate trees survived the ice ages in situ rather than moved to the south (Bai et al, 2010;Hu et al, 2008;Liu et al, 2014;Tian et al, 2009;Zeng et al, 2011;Zeng et al, 2015). Consequently, postglacial range expansions of the eastern Asian temperate trees were necessarily spatially limited compared to the southern refuge model.…”

“…Extensive pollen flow among populations can eliminate the genetic imprints of the Pleistocene refugial isolation, particularly in wind-pollinated tree species (Bai et al, 2014;Liepelt et al, 2002). Using both nuclear and chloroplast DNA markers, Zeng et al (2015) scrutinized the genetic structure of the Mongolian oak, a dominant cool-temperate species in mainland East Asia, and they found convincing evidence for multiple glacial refugia in this region. Up to now, empirical evidence for the multiple-refugia hypothesis (Tian et al, 2009) has been quite limited, let alone evidence of asymmetric gene flow via pollen and seed, which typically results in a cytoplasmic-nuclear discordance in the population structure.…”