The collision of two genomes threatens global food security

Abstract

Human activity alters selection pressures and redistributes biodiversity, creating opportunities for hybridization when dilerent species come into secondary contact. It is now well-established that ancient hybridization plays an important role in adaptive radiation 1, but its role in recent anthropogenic adaptation remains unclear. We investigated this in a study of hybridizing native and invasive Helicoverpa moths in Brazil, which are among the most economically damaging crop pests globally. Native H. zea has recently evolved Bt resistance and is better adapted to maize as a host plant, while invasive H. armigera is resistant to pyrethroid pesticides and is better adapted to soybean. Using a decade-long time series of 975 genomes from both species, we demonstrate rapid, bidirectional adaptive introgression of structural variants that cause resistance to two distinct pesticides. In one direction, a pyrethroid resistance gene from H. armigera (CYP337B3) is now almost fixed in native H. zea. In the other direction, ~30% of recently-sampled invasive H. armigera carry a H. zea-derived trypsin repeat cluster. Using controlled crosses, we show that this trypsin repeat cluster confers resistance to Bt (Cry1Ac) soy in the H. armigera genomic background. Thus, hybridization has combined H. armigera adaptation to soy with H. zea Cry1Ac resistance to facilitate exploitation of Brazilian Bt soy monoculture -- a vast anthropogenic habitat exceeding the area of Germany. Our results show that the combinatorial mechanisms that produce biodiversity can also drive rapid anthropogenic adaptation on ecological timescales, with consequences for global food security.