Intercontinental panmixia despite distinct migration distances in the trans-Saharan butterfly migrant Vanessa cardui

Abstract

The painted lady butterfly Vanessa cardui is renowned for its virtually cosmopolitan distribution and the remarkable long-distance migrations that are part of its annual, multi-generational migratory cycle. In the autumn, V. cardui individuals are found north and south of the Sahara, suggesting distinct migratory behaviours within the species. However, the evolutionary and ecological factors shaping these differences in migratory behaviour remain largely unexplored. Here, we performed whole-genome resequencing and analysed the hydrogen and strontium isotopic signatures of 40 V. cardui individuals simultaneously collected in the autumn from regions both north and south of the Sahara. Our investigation revealed two main migratory groups: (i) short-distance migrants, journeying from temperate Europe to the circum-Mediterranean region and (ii) long-distance migrants, originating from temperate Europe, crossing the Mediterranean Sea and Sahara, and reaching West Africa, covering a distance of up to over 4,000 km. Despite these stark differences in migration distance, a genome-wide analysis of 813,810 single nucleotide polymorphisms (SNPs) revealed that both short- and long-distance migrants belong to a single intercontinental panmictic population extending from northern Europe to sub-Saharan Africa. Contrary to common biogeographic patterns, the Sahara is not a catalyst for population substructuring in this species. No significant genetic differentiation or signs of adaptation and selection were observed between the two migratory phenotypes (pairwise FST = 0.001 ± 0.006). Nonetheless, two individuals, belonging to the early arrivals to the Afrotropical region and covering longer migration distances, exhibited some genetic differentiation. The lack of genetic structure between short- and long-distance migrants suggests that migration distance in V. cardui is a plastic response to environmental conditions.