Global phylogeography and invasion history of the spotted lanternfly revealed by mitochondrial phylogenomics

Abstract

Biological invasion has been a serious global threat due to increasing international trade and population movements. Tracking the source and route of invasive species and evaluating the genetic differences in their native regions have great significance for the effective monitoring and management, and further resolving the invasive mechanism. The spotted lanternfly Lycorma delicatula is native to China and invaded South Korea, Japan, and the United States during the last decade, causing severe damages to the fruits and timber industries. However, its global phylogeographic pattern and invasion history are not clearly understood. We applied high-throughput sequencing to obtain 392 whole mitochondrial genome sequences from four countries to ascertain the origin, dispersal, and invasion history of the spotted lanternfly. Phylogenomic analyses revealed that the spotted lanternfly originated from southwestern China, diverged into six phylogeographic lineages, and experienced northward expansion across the Yangtze River in the late Pleistocene. South Korea populations were derived from multiple invasions from eastern China and Japan with two different genetic sources of northwestern (Loess Plateau) and eastern (East Plain) lineages in China, whereas the each of Japan and the United States had only one. The United States populations originated through single invasive event from South Korea, which served as a bridgehead of invasion. The environmental conditions, especially the distribution of host Ailanthus trees, and adaptability possibly account for the rapid spread of the spotted lanternfly in the native and introduced regions.

Keywords: Lycorma delicatula; invasion history; mitochondrial genome; phylogeography.

FIGURE 1

Geographical distribution of 40 sample populations in East Asia and United States. The colors of the circles represent the six phylogeographic lineages referring to Figure 3b, and the area of the circle is proportional to the number of individuals except YNPB. See Table 1 for population codes. The boundaries of six topographical areas are shown with dashed lines

FIGURE 2

Phylogenetic topology based on mitogenomic haplotypes. The taxa labels describe all individuals sharing haplotypes. The nodal supports of major branches are bootstrap percentages and posterior probabilities. Red circles represent the nodes with bootstrap values larger than 70. The phylogeographic lineages and introduced countries are also shown. The branches with invasive haplotypes are labeled with different colors and geometric figures. The phylogenetic tree with branch length and detailed clades referred by two yellow stars are shown in Figure S2

FIGURE 3

Clustering of individuals of 40 populations and estimated divergence time of the six phylogeographic lineages. (a) Different colors represent the five BAPS (Bayesian analysis of population structure)‐divided groups, with the EP (East Plain), and SB (Sichuan Basin) lineages clustered together. The populations were partitioned into six regions (see Figure 1) with the divisions indicated. (b) The values show the mean estimated time with 95% highest posterior density intervals in the brackets, as indicated by purple bars

FIGURE 4

Median‐joining networks for three phylogeographic lineages. Colored circles represent different haplotypes, black circles represent missing haplotypes that were not observed, and solid lines between haplotypes represent mutation steps. The area of the circle is proportional to the number of haplotypes. See Tables S3–S5 for haplotype frequencies

FIGURE 5

Mismatch distributions and Bayesian skyline plots for the six phylogeographic lineages. The vertical bars represent the observed mismatch distribution, and the red lines represent the expected distribution under the expansion model. For Bayesian skyline plots, the mean estimated effective population sizes (lines) are enclosed within the 95% highest posterior density intervals (shaded areas)