Abstract

In 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, three-dimensional imaging, and physiological measurements, we show that natural selection helps counteract homogenizing effects of gene exchange. 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 these in turn can maintain species, highlighting the importance of natural selection in speciation.Natural selection is an important driver of genetic and phenotypic differentiation between species. For species in which potential gene flow is high but realized gene flow is low, adaptation via natural selection may be a particularly important force maintaining species. 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 Encelia species hybridize at ecologically divergent parapatric boundaries, such mechanisms may maintain species boundaries throughout Encelia.Code used in analysis is available in GitHub (https://github.com/singhal/encelia_transplant) (77). Raw ddRAD reads are available in Sequence Read Archive BioProject (accession no. PRJNA675657) (78). Individual genotypes and phenotypes from each hybrid zone are available in Figshare (https://doi.org/10.6084/m9.figshare.13211036.v1) (79).

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