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

Abstract

The 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.

From Pavement to Population Genomics: Characterizing a Long-Established Non-native Ant in North America Through Citizen Science and ddRADseq

“…Partnerships between these two disciplines can both engage the public in the tools and methods of modern evolutionary biology and, simultaneously, permit evolutionary biologists to address questions on a scale that would be difficult to impossible without the assistance of public participants. Relatively inexpensive genomics and informatics tools have the potential to powerfully enhance the research and educational impacts associated with the rich diversity of questions, subjects, and modes of participation that citizen science projects address (Pocock et al, 2017;Ryan et al, 2019). We hope the results presented here encourage collaboration among scientists and educators as this proven framework for rapid and cost-effective population genomics can be used to characterize other nonmodel species.…”

“…Whereas, observational data have been used effectively for mapping phenotypic, phenological, and geographic traits, the collection and preservation of physical specimens are necessary for genetic research (Pimm et al, 2015;McKinley et al, 2017). To date, a limited number of studies have combined these two approaches (Lyons et al, 2012;Kerkvliet et al, 2017;Ryan et al, 2019), and the value of public participatory research for characterizing introduction histories of non-native, urban species remains to be widely demonstrated empirically.…”

Risk assessment of the entry of Pantoea stewartii subsp. stewartii on maize seed imported by the EU from the USA

“…stewartii so as to pinpoint likely pathways of past introductions (invasion history) of the pathogen to regions where it is not endemic, as recently done for other plant pests (e.g. Anoplophora glabripennis : Javal et al., ; Cryphonectria parasitic a: Demené et al., ; Phytophthora cinnamomi : Socorro Serrano et al., ; Pieris rapae : Ryan et al., ; Seiridium cardinale : Della Rocca et al., ). Furthermore, it would be useful to clarify the origin of the seed associated with current outbreaks in Italy and Slovenia.…”

Europe as a bridgehead in the worldwide invasion history of grapevine downy mildew,Plasmopara viticola

“…In ABC-RF, genetic data are simulated under different demographic scenarios, and summary statistics from the resulting simulated data are statistically compared with those obtained from the observed data (43)(44)(45). We used an iterative process to infer the various invasion events while keeping a tractable number of scenarios to be compared with the ABC-RF (46). We first identified the most likely demographic scenario(s) composed of bifurcation and admixture events considering the native populations and the invasive populations that corresponded to the most ancient introduction events (i.e., with dates of first disease records outside the native range between 1878 and 1889, Fig.…”