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The most cosmopolitan animal migration: phylogeography and population genomics of the butterfly Vanessa cardui

Final Report Summary - MIGRATION (The most cosmopolitan animal migration: phylogeography and population genomics of the butterfly Vanessa cardui)

Animal migration is an evolutionary response to heterogeneity in both space and time, since it functions as a strategy for exploiting temporary resources associated with non-permanent habitats. Insects of several taxonomic groups are well-known migrators, and have relevant consequences for the global economy, with examples including the pollination of agricultural systems, the association with pest outbreaks and the spread of infectious diseases. However, insect migration is still poorly understood, partly because of the difficulty of globally tracking continuous migratory movements. The MIGRATION project aims to bring together genomic-based phylogeography and ecology to understand the population dynamics of the most cosmopolitan of the insects that performs long-range migrations, the painted lady butterfly Vanessa cardui.

MIGRATION started on 1st of February 2015, through collaboration between the Institute of Evolutionary Biology (CSIC-UPF) in Barcelona, Spain (IBE) and Harvard University, USA. The primary goal of the project was to unravel what are the zones where the main migratory pools occur along the planet at different times of the year, and how these interact with the changing environment. Through intensive field work and support from numerous colleagues, the scientists have first gathered the most comprehensive dataset of specimens ever assembled for V. cardui, with ~3500 samples involving ~60 countries worldwide. This dataset likely represents the largest population study ever assembled for natural populations of a widely distributed migratory species.

Next, the researchers have conducted exhaustive molecular work to assess the genetic connectivity of the different populations collected over the world. To do that, ddRAD libraries for ~1200 specimens from ~60 countries have been sequenced at 2x125 bp in Illumina. The result is a unique reference dataset in population genomics both for its size and diversity. Also, ~200 specimens of closely related Vanessa species with diverse distributional ranges and biologies have been sequenced for population structure comparisons. Full genomes have been also sequenced and assembled for representative specimens on the different continents, thus contributing with a reference genome for this emerging model system. On a following phase, genomic-based phylogeographic approaches are being performed to deeply understand how genetic diversity is maintained in a highly mobile species, and how this is shaped geographically.

The population genomics data is complemented by the ecological study, including natural history data, ecological niche modelling, stable isotope ecology and behavioural tests. In this regard, the work conducted by the researchers has led to the discovery that European autumn migrants travel into Africa massively crossing the Sahara Desert and breed in the African savannah (Talavera & Vila 2016; Stefanescu, Soto, Talavera, Vila & Hobson 2016). It has also been proved that the populations in Tropical Africa undertake a return migration across the Sahara to the temperate zone in spring (Talavera, Bataille, et al. In review). These migrations entail distances of >4000 km in single flights and a migration range twice the size than was previously presumed. Such a scenario elucidates a new spatiotemporal model where the species’ latitudinal migratory range encompasses the temperate region (with seasonality determined by temperature) from March to November and the tropical region (with seasonality determined by rainfall) from September to February. This model broadly coincides with the Palaearctic-African bird migration system, where approximately 350 species and c. 3000 million birds annually migrate between tropical Africa and Europe. This situation suggests potential evolutionary convergence between birds and insects in adopting synchronic migratory routes to exploit the same temporary resources and climatic conditions in tropical Africa, or possibly for the insectivore birds to feed on the migrating insects. Patterns equivalent to those between Africa and Europe are being investigated in North America and Asia.

A novel technique has been developed to track insect migratory paths through molecular identifications of carrying pollen grains. Pollen metabarcoding techniques have proved useful at detecting pollen from plants alien to the collecting sites. Studying spring butterflies in the Mediterranean, it has been proved that the approach can detect signal of migrants that flew thousands of km away across the Sahara (Suchan, Talavera et al. In review).

Through the worldwide RAD libraries and the full genomes assembled, MIGRATION has provided a high resolution map of genetic diversity for an insect with a huge distributional range and large population sizes. This dataset represents a very valuable resource and has numerous applications, ranging from the study of insect demography in pest control, the evolutionary understanding of the transitioning between migratory and non-migratory states, to the identification of preferential hotspots for migrants concentrating highest genetic diversity values.

The MIGRATION project has been disseminated in conferences, seminars and public outreach, and has been highlighted by renowned publishers as National Geographic, BBC Earth, ScienceNews and The Guardian. A divulgation video showing the research and the main findings done so far have been created and made public through different channels (e.g. https://www.youtube.com/watch?v=4E9Wb35_t6I). The project website can be visited at: http://carduimigration.weebly.com.

The main goals of the MIGRATION project have been successfully achieved. With the knowledge and datasets generated, V. cardui is truly emerging as a model system in ecology and genomics. The research lines here initiated are having continuity with new grants awarded, multiple collaborations and it has become the main research topic for the researcher.