Environmental Heterogeneity Leads to Spatial Differences in Genetic Diversity and Demographic Structure of Acer caudatifolium

Abstract

Under climate fluctuation, species dispersal may be disturbed by terrain and local climate, resulting in uneven spatial-genetic structure. In addition, organisms at different latitudes may be differentially susceptible to climate change. Here, we tracked the seed dispersal of Acer caudatifolium using chloroplast DNA to explore the relationships of terrain and local climate heterogeneity with range shifts and demography in Taiwan. Our results showed that the extant populations have shifted upward and northward to the mountains since the Last Glacial Maximum. The distributional upshift of A. caudatifolium is in contrast to the downward expansion of its closest relative in Taiwan, A. morrisonense. The northern populations of A. caudatifolium have acquired multiple-source chlorotypes and harbor high genetic diversity. However, effective gene flow between the north and south is interrupted by topography, geographic distance, north-south differences in October rainfall, and other climate heterogeneities, blocking southward genetic rescue. In addition, winter monsoon-driven rainfall may cause regional differences in the phenological schedule, resulting in adaptive effects on the timing of range shift and the genetic draft of chlorotype distribution. Terrain, distance, and local climate also differentiate the northernmost populations from the others, supporting the previous taxonomic treatment of Acer kawakamii var. taitonmontanum as an independent variety.

Different Roles of Introgression on the Demographic Change in Two Snakebark Maples, Acer caudatifolium and A. morrisonense, with Contrasted Postglacial Expansion Routes

“…This continued introgression is not surprising, as A. caudatifolium and A. morrisonense bloom synchronously from March to April within a confined space of an island. Since these two island maples were allopatrically distributed during the LGM until the middle-Holocene range overlapping [ 22 , 23 ], we speculate that the recent introgression is due to the secondary contact since postglacial expansion.…”

“…The founder effect of colonizing Taiwan also explains the severe population decline from t 1 to t 2 inferred by ABC. Although previous studies only backtracked paleo-distributions in LGM [ 22 , 23 ], these two species might also be confined within refugia since the earlier stage of the Quaternary LGP because of the continuous cold and aridity. However, we detected high frequencies of private alleles ( Table 1 ), implying a rapid recovery of population size.…”

“…Therefore, the hypothesis of genetic rescue by introgression could be rejected, and the abundant private alleles were alternatively explained by the rapid range expansion after LGM. Especially for A. caudatifolium , the positive association of private allele with altitude reflects its post-LGM upward expansion [ 22 ] because of the higher mutation rate in the wavefront of expanding populations [ 39 ].…”

“…Besides, the two species dramatically changed in spatial and genetic distributions from the Last Glacial Maximum (LGM) to the present [ 22 , 23 ]. During the LGM, A. morrisonense was distributed at higher-elevational refugia, and A. caudatifolium was confined in the low mountains of southern Taiwan ( Figure 2 ).…”

“…Then, the postglacial warming relaxed the pressure of harsh environments on their survival, leading to rapid expansion. Acer morrisonense was downward shifting in range [ 23 ], while A. caudatifolium was upward- and northward-moving after the LGM [ 22 ]. The postglacial range shifts cause elevational overlap in the distribution of these two maples ( Figure 2 ), leading to the probability of hybridization or introgression.…”