Natural selection maintains species despite widespread hybridization in the desert shrub Encelia

Abstract

Natural selection is an important driver of genetic and phenotypic differentiation between species. A powerful way to test the role of natural selection in the formation and maintenance of species is to study species complexes in which potential gene flow is high but realized gene flow is low. For a recent radiation of New World desert shrubs (Encelia: Asteraceae), we use fine-scale geographic sampling and population genomics to determine patterns of gene flow across two hybrid zones formed between two independent pairs of species with parapatric distributions. After finding evidence for extremely strong selection at both hybrid zones, we use a combination of field experiments, high-resolution imaging, and physiological measurements to determine the ecological basis for selection at one of the hybrid zones. Our results identify multiple ecological mechanisms of selection (drought, salinity, herbivory, and burial) that together are sufficient to maintain species boundaries despite high rates of hybridization. Given that multiple pairs of species hybridize at ecologically divergent parapatric boundaries in the adaptive radiation of Encelia, such mechanisms may maintain species boundaries throughout this group. SIGNIFICANCE STATEMENTIn Baja California, the deserts meet the coastal dunes in a narrow transition visible even from satellite images. We study two species pairs of desert shrubs (Encelia) that occur across this transition. Although these species can interbreed, they remain distinct. Using a combination of genetics, field experiments, 3D-imaging, and physiological measurements, we show that natural selection counteracts the homogenizing effects of gene exchange. The different habitats of these species create multiple mechanisms of selection - drought, salinity, herbivory, and burial, which together maintain these species in their native habitats and their hybrids in intermediate habitats. This study illustrates how environmental factors influence traits and fitness and how this in turn maintain species, highlighting the importance of natural selection in speciation.