Genome-wide SNPs of vegetable leafminer, Liriomyza sativae: Insights into the recent Australian invasion

Abstract

Liriomyza sativae, the vegetable leafminer, is an important agricultural pest originally from the Americas, which has now colonized all continents except Antarctica. In 2015, L. sativae arrived on the Australian mainland and established on the Cape York Peninsula in the northeast of the country near the Torres Strait, which provides a possible pathway for pests to enter Australia and evade biosecurity efforts. Here, we assessed genetic variation in L. sativae based on genome-wide single nucleotide polymorphisms (SNPs) generated by double digest restriction-site-associated DNA sequencing (ddRAD-seq), aiming to uncover the potential origin(s) of this pest in Australia and contribute to reconstructing its global invasion history. Our fineRADstructure results and principal component analysis suggest Australian mainland populations were genetically close to populations from the Torres Strait, whereas populations from Asia, Africa, and Papua New Guinea (PNG) were more distantly related. Hawaiian populations were genetically distinct from all other populations of L. sativae included in our study. Admixture analyses further revealed that L. sativae from the Torres Strait may have genetic variation originating from multiple sources including Indonesia and PNG, and which has now spread to the Australian mainland. The L. sativae lineages from Asia and Africa appear closely related. Isolation-by-distance (IBD) was found at a broad global scale, but not within small regions, suggesting that human-mediated factors likely contribute to the local spread of this pest. Overall, our findings suggest that an exotic Liriomyza pest invaded Australia through the Indo-Papuan conduit, highlighting the importance of biosecurity programs aimed at restricting the movement of pests and diseases through this corridor.

Keywords: biological invasions; ddRAD; gene flow; genome‐wide SNPs; leafminers; population genetics.

FIGURE 1

(a) Sampling locations of Liriomyza sativae in this study. Colors indicate different populations, and the size of circles reflects the relative sizes of each sample. The dotted rectangle represents the local geography around northern Australia, as detailed in (b). QLD = Queensland; PNG = Papua New Guinea

FIGURE 2

Principal component analysis (PCA) of 193 Liriomyza sativae individuals collected from 24 populations based on 7379 SNPs. The variances explained by PC1 and PC2 are given. Each dot represents sampled individuals, with populations from the same country merged except for the Australian populations (Boigu Island, Masig Island, Seisia, and Thursday Island). PNG = Papua New Guinea

FIGURE 3

FineRADstructure plot with co‐ancestry map and phylogenetic tree. The color scale bar indicates estimated co‐ancestry, with light yellow suggesting low co‐ancestry and darker yellow, orange, and red indicating progressively higher co‐ancestry. The Australian populations formed a clade (labeled in red), which is shown in the solid black square. See Figure S1 for full‐size figure

FIGURE 4

Population structure of Liriomyza sativae based on 193 individuals inferred using admixture analysis. The minimum cross‐validation error was found when K = 5. PNG = Papua New Guinea

FIGURE 5

(a) Association between genetic distances (F _ST) and geographic distances (km) for the 21 Liriomyza sativae populations (Mantel test, p = 0.002; correlation = 0.412; R ² = 0.166). (b) Association between genetic distances (F _ST) and geographic distances (km) for the 8 L. sativae populations associated with the Australian incursion (Mantel test, p = 0.216). The line in the picture is a linear model fitted to the data, and the shading represents the associated 95% confidence interval