Genetic structure and trait variation within a maple hybrid zone underscore North China as an overlooked diversity hotspot

Abstract

Tertiary relict flora in East Asia can be divided into northern and southern regions. North China is a diversity hotspot because it can be the secondary contact zone of ancient lineages from the two regions. To test the extent of ancient lineages hybridization and distinguish between the putative species pair Acer pictum subsp. mono and Acer truncatum, we conducted genetic and ecological studies within a maple hybrid zone in North China. Our results suggest that the two lineages of Acer coexist in the hybrid zone and that adult and offspring populations show typical bimodal genetic patterns. Hybrid individuals are established at intermediate altitudes between the two parental lineages. Flowering phenology is divergent between lineages, whereas the complex sexual system of Acer may ensure pollination among lineages. Leaf and fruit morphologies are different between the northern and southern origin lineages, corresponding to A. pictum subsp. mono and A. truncatum, respectively. Reduced gene flow between lineages suggests that they should be considered as two species. However, large morphological variations within each species and the existence of hybrids offer low reliability of species identification based solely on morphological traits. Our study underscores North China as an overlooked diversity hotspot that requires further study in the future.

Figure 1

Geographical range of NEA-SEA lineages area and the sampling population locations in North China from GUO et al. 2014. (a) Geographical range of two Tertiary relict regions [Southern East Asia (SEA) and Northern East Asia (NEA)] for temperate flora in East Asia, according to Milne and Abbott. The red and green points indicate SEA and NEA Acer population locations sampled by Guo et al.. (b) An enlarged representation of the area demarcated by the red border in (a) showing the geography of North China, which is a key secondary contact zone for tertiary relict NEA and SEA lineages. Colored circles indicate the locations of Acer populations. The pie charts of the sampled populations are STRUCTURE results based on a whole-range dataset (see text), with the red and green sectors representing the SEA and NEA lineages, respectively. The numbers adjacent to the circles denote the altitudinal range in meters for all sampled individuals in the population. The focal population in the Daheishan National Nature Reserve examined in this study is indicated by the yellow star. ArcGIS 10.1 software was used for mapping (https://www.esri.com/en-us/arcgis/about-arcgis/overview).

Figure 2

Genetic structure of the parental and offspring population. (a) Bar plots illustrating the genetic composition of the adult (leaf) and offspring (fruit) populations in the Daheishan National Nature Reserve (DHS). Each individual is represented by a line partitioned into color segments corresponding to its ancestral proportion. Red color represents the ancestral proportion of Southern East Asia lineage. Green color represents the ancestral proportion of Northern East Asia lineage. Black lines in bar plots of leaf population separate individuals with ancestral proportion (q value) bigger than 0.9 or smaller than 0.1 from hybrids (0.1 < q < 0.9). Black lines in bar plots of fruit population separate individuals from different maternal genetic types. (b) Frequency distributions of q value in adult (gray) and offspring (colored) populations. Different colors represent the maternal genetic types of fruits. (c) Principal coordinates analysis results obtained for the adult population. (d) The q value of 70 Acer trees is positively correlated with altitude (Pearson r = 0.83, p = 0.000). Different colors or filled/empty of circles represent individuals used for different analysis in the study. The legend abbreviates adult/offspring genetic structure as adult/offspring, flowering phenology as phenology, leaf/fruit morphology as leaf/fruit. SEA-DHS: Southern East Asia lineage of the Acer species complex in the DHS; NEA-DHS: Northern East Asia lineage of the Acer species complex in the DHS; Hybrid-DHS: hybrids between SEA-DHS and NEA-DHS lineages.

Figure 3

Morphological variation in the leaves (a) and fruits (b) of southern and northern East Asia lineages of the Acer species complex in the Daheishan National Nature Reserve based on principal component analysis. SEA-DHS: Southern East Asia lineage of the Acer species complex in the DHS; NEA-DHS: Northern East Asia lineage of the Acer species complex in the DHS; Hybrid-DHS: hybrids between SEA-DHS and NEA-DHS lineages.