Global invasion history of the agricultural pest butterfly Pieris rapae revealed with genomics and citizen science

Ryan et al., 2019

 Over the last few thousand years, the seemingly inconspicuous cabbage white butterfly, Pieris rapae, has become one of the most abundant and destructive butterflies in the world. Here, we assessed variation at thousands of genetic markers from butterflies collected across 32 countries by over 150 volunteer scientists and citizens to reconstruct the global spread of this agricultural pest. Our results suggest this butterfly spread out from eastern Europe to occupy every continent except South America and Antarctica, with the timing of many of these events coinciding with human activities—migration, trade, and the development of crop cultivars that serve as food plants for the butterfly larvae. Interestingly, many of these invasions were hugely successful despite repeated losses of genetic diversity.

he small cabbage white butterfly, Pieris rapae, is a major agricultural pest of cruciferous crops and has been introduced to every continent except South America and Antarctica as a result of human activities. In an effort to reconstruct the near-global invasion history of P. rapae, we developed a citizen science project, the “Pieris Project,” and successfully amassed thousands of specimens from 32 countries worldwide. We then generated and analyzed nuclear (double-digest restriction site-associated DNA fragment procedure [ddRAD]) and mitochondrial DNA sequence data for these samples to reconstruct and compare different global invasion history scenarios. Our results bolster historical accounts of the global spread and timing of P. rapae introductions. We provide molecular evidence supporting the hypothesis that the ongoing divergence of the European and Asian subspecies of P. rapae (∼1,200 y B.P.) coincides with the diversification of brassicaceous crops and the development of human trade routes such as the Silk Route (Silk Road). The further spread of P. rapae over the last ∼160 y was facilitated by human movement and trade, resulting in an almost linear series of at least 4 founding events, with each introduced population going through a severe bottleneck and serving as the source for the next introduction. Management efforts of this agricultural pest may need to consider the current existence of multiple genetically distinct populations. Finally, the international success of the Pieris Project demonstrates the power of the public to aid scientists in collections-based research addressing important questions in invasion biology, and in ecology and evolutionary biology more broadly.

Global invasion history and patterns of genetic structure and diversity of P. rapae. (A) Genetic ancestry assignments based on the program ADMIXTURE. (B) Rooted neighbor-joining tree based on Nei’s genetic distance. (C) Among population genetic differentiation based on Weir and Cockerham’s F_ST, New Zealand and Australia are treated separately. (D) Graphical illustration of divergence scenario chosen in ABC-RF analysis. (E) Geographic representation of divergence scenario with the highest likelihood based on ABC-RF analysis; points are colored based on their population assignment using ADMIXTURE as in A, and dates represent median estimates from ABC-RF analysis. All analyses are based on 558 individuals genotyped for 17,917 ddRADseq SNPs. Explore these data further through interactive data visualizations

https://www.pnas.org/content/116/40/20015

.