Pollen limitation and autonomous selfing ability interact to shape variation in outcrossing rate across a species range

Abstract

Hermaphroditic plants commonly reproduce through a mixture of selfing and outcrossing. The degree to which outcrossing rates reflect the availability of outcross pollen, genetic differentiation in the ability to autonomously self-fertilize, or both is often unclear. Despite the potential for autonomy and the pollination environment to jointly influence outcrossing, this interaction is rarely studied. METHODS: We reviewed studies from the literature that tested whether the pollination environment or floral traits that cause autonomous selfing predict variation in outcrossing rate among populations. We also measured outcrossing rates in 23 populations of Campanula americana and examined associations with the pollination environment, autonomy, and their interaction. RESULTS: Our review revealed that traits that facilitate selfing were often negatively associated with outcrossing rates whereas most aspects of the pollination environment poorly predicted outcrossing. Populations of C. americana varied from mixed mating to highly outcrossing, but variation was unrelated to population size, density, pollen limitation, or autonomous selfing ability. Outcrossing rate was significantly influenced by an interaction between autonomous selfing ability and pollen limitation. Across highly autonomous populations, elevated pollen limitation was associated with reduced outcrossing, while there was no relationship for less autonomous populations. CONCLUSIONS: Both the ability to self autonomously and pollen limitation interact to shape outcrossing rates in C. americana. This work suggests that autonomy affords mating-system flexibility, though it is not ubiquitous in all populations across the species range. Interactions between traits influencing autonomy and pollen limitation are likely to explain variation in outcrossing rates among populations of flowering plants.

Selfing ability and drift load evolve with range expansion

“…; Koski et al. ). Although the extent of pollen limitation during the Pleistocene is little known, plants at the leading edge of the geographic range expansion likely encountered few mates or pollinators.…”

“…In contrast to these historical arguments, autonomy neither causes elevated homozygosity nor influences the outcrossing rate of contemporary C. americana populations (Koski et al. ). There is also little apparent geographic structure to mate or pollinator availability across the species' geographic range (Koski et al.…”

“…; Koski et al. ), its mating system is flexible depending on the pollination environment (Leibman et al. ).…”

“…The ability to self without a pollinator (i.e., autonomously) is a key component of the mating system. Contemporary C. americana populations with greater autonomy modify their selfing rate in response to the pollen limitation, whereas those with lower autonomy do not (Leibman et al 2018;Koski et al 2019).…”

“…This species is native to Eastern North America and its showy protandrous flowers are bee pollinated. Although largely outcrossing in natural populations (Galloway et al 2003;Koski et al 2019), its mating system is flexible depending on the pollination environment (Leibman et al 2018). Populations vary substantially in their ability to produce autonomously self-fertilized fruits because of variation in the overlap of male and female sexual functions, and the timing of pollen germinability ).…”