Abstract

The transition to self-compatibility from self-incompatibility is often associated with high rates of self-fertilization, which can restrict gene flow among populations and cause reproductive isolation of self-compatible (SC) lineages. Secondary contact between SC and self-incompatible (SI) lineages might re-establish gene flow if SC lineages remain capable of outcrossing. By contrast, intrinsic features of SC plants that reinforce high rates of self-fertilization could maintain evolutionary divergence between lineages. Arabidopsis lyrata subsp. lyrata is characterized by multiple origins of self-compatibility and high rates of self-fertilization in SC-dominated populations. It is unclear whether these high rates of selfing by SC plants have intrinsic or extrinsic causes. We estimated outcrossing rates and examined patterns of pollinator movement for 38 SC and 40 SI maternal parents sampled from an admixed array of 1509 plants sourced from six SC and six SI populations grown under uniform density. Although plants from SI populations had higher outcrossing rates (mean tm = 0.78 ± 0.05 SE) than plants from SC populations (mean tm = 0.56 ± 0.06 SE), outcrossing rates among SC plants were substantially higher than previous estimates from natural populations. Patterns of pollinator movement appeared to contribute to lower outcrossing rates for SC plants; we estimated that 40% of floral visits were geitonogamous (between flowers of the same plant). The relatively high rates of outcrossing for SC plants under standardized conditions indicate that selfing rates in natural SC populations of A. lyrata are facultative and driven by extrinsic features of A. lyrata, including patterns of pollinator movement.

Highlights

  • The shift from self-incompatibility to self-compatibility is one of the most frequent evolutionary transitions in flowering plants (Barrett 2002; Wright et al 2013)

  • There was substantial variation in rates of outcrossing among SC plants and average outcrossing rates for SC plants exceeded those found in natural populations of SC A. lyrata

  • Average outcrossing rates for SI plants in our experiment fell within the range of those reported from entirely SI populations (Foxe et al 2010)

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Summary

Introduction

The shift from self-incompatibility to self-compatibility is one of the most frequent evolutionary transitions in flowering plants (Barrett 2002; Wright et al 2013). Strong genetic differentiation between SC and SI populations of Linaria cavanillesii appears to have been driven by historical events, including population bottlenecks, rather than by restricted gene flow arising from high rates of selfing (Voillemot and Pannell 2017). The breakdown of self-incompatibility has been followed by phenotypic changes to flowers and inflorescences that reinforce assortative mating within newly-arisen SC lineages. These phenotypic features include reduced flower size, reduced investment in pollinator attraction, and reduced spatial separation between male and female sex organs within flowers, that together represent components of the “selfing syndrome” (Sicard and Lenhard 2011) and that promote reproductive isolation between SC and SI plants (Cutter 2019). Understanding whether reproductive isolation is caused by assortative mating following the transition to SC, or by ancillary features (e.g., traits associated with the selfing syndrome) will clarify the mechanisms underlying high rates of diversification following transitions from SI to SC

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