Evolutionary history of the buildup and breakdown of the heterostylous syndrome in Plumbaginaceae

Abstract

The evolutionary pathways leading to the heterostylous syndrome are not well understood, and models concerning the origins of distyly differ in the order in which reciprocal herkogamy and self-incompatibility evolve. We investigated the evolution and breakdown of distyly in Plumbaginaceae, a family with considerable diversity of floral traits and reproductive systems.Using Bayesian Markov chain Monte Carlo analyses and stochastic character mapping, we examined the evolutionary assembly and breakdown of the heterostylous syndrome based on a well-resolved phylogeny of 121 species of Plumbaginaceae and six outgroup taxa using five nuclear and plastid gene regions. We used the distribution of reproductive traits and reconstructed ancestral characters across phylogenies to evaluate competing models for the evolution of distyly.The most likely common ancestor of Plumbaginaceae was self-incompatible and monomorphic for sex-organ arrangement and pollen-stigma characters. Character state reconstructions indicated that reciprocal herkogamy evolved at least three times and that shifts to selfing and apomixis occurred on multiple occasions.Our results provide comparative support for the early ideas of H. G. Baker on evolutionary pathways in Plumbaginaceae, and the more recent selfing avoidance model by D. & B. Charlesworth in which distyly evolves from self-incompatible ancestors.

The ecology, evolution, and genetics of plant reproductive systems

“…Costa et al . (, in this issue pp. 1278–1289) conducted comparative analyses of mating system transitions in Plumbaginaceae and report that the most likely common ancestor of the group was self‐incompatible and monomorphic, a finding that supports one of two competing models for the evolution of heterostyly, the ‘selfing avoidance’ model of B. Charlesworth & D. Charlesworth ().…”

‘A most complex marriage arrangement’: recent advances on heterostyly and unresolved questions

“…But this stylar polymorphism is absent from most heterostylous groups (Barrett et al ., ), perhaps because in lineages with heteromorphic incompatibility it is an ephemeral state. Reconstructions of the evolutionary history of distyly in Plumbaginaceae indicate that reciprocal herkogamy evolved after the establishment of heteromorphic incompatibility (Costa et al ., ), the sequence predicted in the D. Charlesworth & Charlesworth () model. This polarity is also evident in Narcissus (Graham & Barrett, ) and some lineages of Boraginaceae (Cohen, ).…”

Reproductive Output and Insect Behavior in Hybrids and Apomicts from Limonium ovalifolium and L. binervosum Complexes (Plumbaginaceae) in an Open Cross-Pollination Experiment

“…(sea lavenders Plumbaginaceae), plants characteristically show striking flower polymorphisms linked to a sporophytic self-incompatibility system, which is associated with distinct reproductive modes, sexual and/or apomixis (agamospermy, asexual reproduction through seeds) [1][2][3][4][5][6][7][8]. Most species show ancillary pollen (e.g., differences in pollen production, size, shape, and exine sculpturing) and stigma heteromorphisms (e.g., papillae size and morphology) generally linked with heterostyly (pistils' and stamens' sizes in alternate morphs) that prevents self and intramorph mating [1][2][3]5,[7][8][9]. Some Limonium species are heterostylous (e.g., Limonium vulgare) [2,3,[9][10][11], despite most of them being non-heterostylous but with pollen-stigma polymorphisms [2,[7][8][9]12].…”

“…Most species show ancillary pollen (e.g., differences in pollen production, size, shape, and exine sculpturing) and stigma heteromorphisms (e.g., papillae size and morphology) generally linked with heterostyly (pistils' and stamens' sizes in alternate morphs) that prevents self and intramorph mating [1][2][3]5,[7][8][9]. Some Limonium species are heterostylous (e.g., Limonium vulgare) [2,3,[9][10][11], despite most of them being non-heterostylous but with pollen-stigma polymorphisms [2,[7][8][9]12].…”