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In a number of animal species, divergent natural selection repeatedly and independently drove the evolution of reproductive isolation between populations adapted to contrasting, but not to similar environments. This process is known as parallel ecological speciation, and examples in plants are enigmatically rare. Here, we perform a comprehensive test of the ecological speciation hypothesis in an Australian wildflower where parapatric populations found in coastal sand dunes (Dune ecotype) and headlands (Headland ecotype) have repeatedly and independently diverged in growth habit. Consistent with a role for divergent natural selection driving the evolution of reproductive isolation, we found that Dune populations with erect growth habit were easy to transplant across sand dunes, were largely interfertile despite half-a-million years of divergence, and were reproductively isolated from equally divergent Headland populations with prostrate growth habit. However, we unexpectedly discovered that both extrinsic and intrinsic reproductive isolation evolved between prostrate Headland populations, suggesting that populations evolving convergent phenotypes can also become new species rapidly. Mutation-order speciation, where the random accumulation of adaptive alleles create genetic incompatibilities between populations inhabiting similar habitats, provides a compelling explanation for these complex patterns of reproductive isolation, and is consistent with the increasingly common observation that there are multiple biochemical avenues to create convergent phenotypes. Our results suggest that natural selection can drive speciation effectively, but environmental and genetic complexity might make parallel ecological speciation uncommon in plants despite strong morphological convergence.
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