Maintenance of mixed mating after the loss of self-incompatibility in a long-lived perennial herb

Abstract

Background and Aims Many hermaphroditic plants avoid self-fertilization by means of a molecular selfincompatibility (SI) system, a complex trait that is difficult to evolve but relatively easy to lose. Loss of SI is a prerequisite for an evolutionary transition from obligate outcrossing to self-fertilization, which may bring about rapid changes in the genetic diversity and structure of populations. Loss of SI is also often followed by the evolution of a 'selfing syndrome', with plants having small flowers, little nectar and few pollen grains per ovule. Here, we document the loss of SI in the long-lived Spanish toadflax Linaria cavanillesii, which has led to mixed mating rather than a transition to a high rate of selfing and in which an outcrossing syndrome has been maintained.Methods We performed crosses within and among six populations of L. cavanillesii in the glasshouse, measured floral traits in a common-garden experiment, performed a pollen-limitation experiment in the field and conducted population genetic analyses using microsatellites markers.Key Results Controlled crosses revealed variation in SI from fully SI through intermediate SI to fully selfcompatible (SC). Flowers of SC individuals showed no evidence of a selfing syndrome. Although the SC population of L. cavanillesii had lower within-population genetic diversity than SI populations, as expected, population differentiation among all populations was extreme and represents an F ST outlier in the distribution for both selfing and outcrossing species of flowering plants.Conclusions Together, our results suggest that the transition to SC in L. cavanillesii has probably been very recent, and may have been aided by selection during or following a colonization bottleneck rather than in the absence of pollinators. We find little indication that the transition to SC has been driven by selection for reproductive assurance under conditions currently prevailing in natural populations.

The divergence history of the perennial plant Linaria cavanillesii confirms a recent loss of self‐incompatibility

“…We used ABC simulations to compare the fit of alternative demographic models of divergence to empirical data of the plant L . cavanillesii , a species with among‐population variation in its SI status (Voillemot & Pannell, ). Overall, our analyses are consistent with a scenario where the lineage ancestral to COV (a mixed‐mating population that has lost its SI system) has been diverging from ancestral SI populations for an estimated 2810 generations.…”

“…As noted in the Introduction, the autonomous SC population of L. cavanillesii shows no evidence for the evolution of a selfing syndrome (Voillemot & Pannell, ), that is a reduction in pollen production or allocation to attracting and rewarding pollinators (Ornduff, ; Sicard & Lenhard, ). One explanation could be that genetic variation in the SC lineage of L. cavanillesii was low, for example as a result of population bottlenecks, and that it was thus unresponsive to selection.…”

“…Geographical range of Linaria cavanillesii in Spain (grey oval), and the populations that have been studied in detail (Voillemot & Pannell, ). Three northern populations ( COV , DEN and BER ) were used in the ABC simulations presented here.…”

Rapid loss of self‐incompatibility in experimental populations of the perennial outcrossing plantLinaria cavanillesii

“…Linaria cavanillesii is a long‐lived perennial herb that grows on north‐northwest‐facing limestone cliffs in southeastern Spain. Plants flower from April to June and are visited mainly by bees and bumblebees, producing large leafy inflorescences of yellow flowers with long nectar spurs (Voillemot and Pannell ). Fruits typically mature approximately 30 days after fertilization (producing between about 100 and 150 seeds maximum), and seeds are dispersed passively when capsules open.…”

“…), but populations are in fact mostly SI (with a gametophytic system). Only one fully SC population is known, although some populations show a small degree of “leaky” self‐incompatibily (Voillemot and Pannell ). We carried out our study using seeds from two close‐by SI populations (BER and DEN) and the single known SC population (COV), all from the Alicante region in southeastern Spain (Fig.…”