Abstract

Hybridization is a common phenomenon, yet its evolutionary outcomes remain debated. Here, we ask whether hybridization can speed adaptive evolution using resynthesized hybrids between two species of Texas sunflowers (Helianthus annuus and H. debilis) that form a natural hybrid in the wild (H. annuus ssp. texanus). We established separate control and hybrid populations and allowed them to evolve naturally in a field evolutionary experiment. In a final common-garden, we measured fitness and a suite of key traits for these lineages. We show that hybrid fitness evolved in just seven generations, with fitness of the hybrid lines exceeding that of the controls by 14% and 51% by the end of the experiment, though only the latter represents a significant increase. More traits evolved significantly in hybrids relative to controls, and hybrid evolution was faster for most traits. Some traits in both hybrid and control lineages evolved in an adaptive manner consistent with the direction of phenotypic selection. These findings show a causal pathway from hybridization to rapid adaptation and suggest an explanation for the frequently noted association between hybridization and adaptive radiation, range expansion, and invasion.

Highlights

  • IntroductionHistorically regarded as a transitory or rare phenomenon[1,2,3], natural hybridization is currently recognized as common in plants (occurring globally in 40% of families[4] and involving up to 25% of species in some floras)[5], important in animals (frequency of interbreeding species: 0.1–3%)[6] with up to 25% in some groups[5], and increasingly found in fungi (reviewed in[7])

  • Historically regarded as a transitory or rare phenomenon[1,2,3], natural hybridization is currently recognized as common in plants[5], important in animals[6] with up to 25% in some groups[5], and increasingly found in fungi

  • We used an eight-year field experiment to examine adaptive evolution in initial, multiple intermediate, and final generations of control and resynthesized hybrid (H. debilis × H. a. annuus backcrossed to H. a. annuus) populations in a common-garden setting

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Summary

Introduction

Historically regarded as a transitory or rare phenomenon[1,2,3], natural hybridization is currently recognized as common in plants (occurring globally in 40% of families[4] and involving up to 25% of species in some floras)[5], important in animals (frequency of interbreeding species: 0.1–3%)[6] with up to 25% in some groups[5], and increasingly found in fungi (reviewed in[7]). They can address many questions, including those related to adaptation, evolutionary tradeoffs, population genetic parameters, and other lineage-specific evolutionary hypotheses[26,27,28] Conducting these experiments in a field setting allows for the assessment of changes under realistic conditions that include multidimensional selective pressures and relevant genotype-by-environment interactions[29]. Such studies (those that take place in the field, involve some type of manipulation, and last for multiple generations in situ) on the effects of hybridization have so far been carried out exclusively in crop-wild systems. We ask: (1) does hybrid fitness evolve compared to controls? (2) do key traits evolve more rapidly in hybrids relative to controls?, and (3) can trait evolution be predicted by initial phenotypic distance from the locally-adapted phenotype?

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