Reconstructing the global invasion routes of the cabbage white butterfly using citizen science assisted genomics

AbstractA major goal of invasion and climate change biology research is to understand the ecological and evolutionary responses of organisms to anthropogenic disturbance, especially over large spatial and temporal scales. One significant, and sometimes unattainable, challenge of these studies is garnering sufficient numbers of relevant specimens, especially for species spread across multiple continents. We developed a citizen science project, “Pieris Project”, to successfully amass thousands of specimens of the invasive agricultural pest Pieris rapae, the small cabbage white butterfly, from 32 countries worldwide. We then generated and analyzed genomic (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. The spread of P. rapae over the last ∼160 years followed a linear series of at least four founding events, with each introduced population serving as the source for the next. We provide the first molecular evidence supporting the hypothesis that the ongoing divergence of the European and Asian subspecies of P. rapae (∼1,200 yrBP) coincides with the domestication of brassicaceous crops. Finally, the international success of the Pieris Project allowed us to nearly double the geographic scope of our sampling (i.e., add >1,000 specimens from 13 countries), demonstrating the power of the public to aid scientists in collections-based research addressing important questions in ecology and evolutionary biology.Non-technical summaryWe provide genetic evidence that the success of the small cabbage white butterfly—its rise to one of the most widespread and abundant butterflies on the planet— was largely facilitated by human activities, through the domestication of its food plants and the accidental movement of the butterfly by means of trade and human movement (migration). Through an international citizen science project—Pieris Project—people from around the world helped to unravel the global invasion history of this agricultural pest butterfly by collecting samples for DNA analysis. The success of this citizen science project demonstrates the power of the public to aid in collections-based research that address important questions related to ecology and evolutionary biology.

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Unravelling the global invasion routes of a worldwide invader, the red swamp crayfish (Procambarus clarkii)

Freshwater Biology ◽

10.1111/fwb.13312 ◽

2019 ◽

Vol 64 (8) ◽

pp. 1382-1400 ◽

Cited By ~ 14

Author(s):

Francisco J. Oficialdegui ◽

Miguel Clavero ◽

Marta I. Sánchez ◽

Andy J. Green ◽

Luz Boyero ◽

...

Keyword(s):

Procambarus Clarkii ◽

Red Swamp Crayfish ◽

Invasion Routes ◽

Global Invasion

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The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest

BMC Biology ◽

10.1186/s12915-020-00820-5 ◽

2020 ◽

Vol 18 (1) ◽

Cited By ~ 4

Author(s):

Claude Rispe ◽

Fabrice Legeai ◽

Paul D. Nabity ◽

Rosa Fernández ◽

Arinder K. Arora ◽

...

Keyword(s):

North America ◽

Mississippi River ◽

Grape Phylloxera ◽

The Past ◽

Plant Feeding ◽

Metabolic Genes ◽

Effector Genes ◽

Genetic Stocks ◽

Invasion Routes ◽

Global Invasion

Abstract Background Although native to North America, the invasion of the aphid-like grape phylloxera Daktulosphaira vitifoliae across the globe altered the course of grape cultivation. For the past 150 years, viticulture relied on grafting-resistant North American Vitis species as rootstocks, thereby limiting genetic stocks tolerant to other stressors such as pathogens and climate change. Limited understanding of the insect genetics resulted in successive outbreaks across the globe when rootstocks failed. Here we report the 294-Mb genome of D. vitifoliae as a basic tool to understand host plant manipulation, nutritional endosymbiosis, and enhance global viticulture. Results Using a combination of genome, RNA, and population resequencing, we found grape phylloxera showed high duplication rates since its common ancestor with aphids, but similarity in most metabolic genes, despite lacking obligate nutritional symbioses and feeding from parenchyma. Similarly, no enrichment occurred in development genes in relation to viviparity. However, phylloxera evolved > 2700 unique genes that resemble putative effectors and are active during feeding. Population sequencing revealed the global invasion began from the upper Mississippi River in North America, spread to Europe and from there to the rest of the world. Conclusions The grape phylloxera genome reveals genetic architecture relative to the evolution of nutritional endosymbiosis, viviparity, and herbivory. The extraordinary expansion in effector genes also suggests novel adaptations to plant feeding and how insects induce complex plant phenotypes, for instance galls. Finally, our understanding of the origin of this invasive species and its genome provide genetics resources to alleviate rootstock bottlenecks restricting the advancement of viticulture.

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

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1907492116 ◽

2019 ◽

Vol 116 (40) ◽

pp. 20015-20024 ◽

Cited By ~ 10

Author(s):

Sean F. Ryan ◽

Eric Lombaert ◽

Anne Espeset ◽

Roger Vila ◽

Gerard Talavera ◽

...

Keyword(s):

Citizen Science ◽

Pieris Rapae ◽

Sequence Data ◽

Invasion Biology ◽

Human Movement ◽

Molecular Evidence ◽

Invasion History ◽

Agricultural Pest ◽

History Of ◽

Global Invasion

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.

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