The role of pollinators as ecological drivers of diversification in the Drakensberg mountain centre endemic genus glumicalyx (Scrophulariaceae, limoselleae)

Abstract

The role of pollinators as ecological drivers of diversification in the Drakensberg Mountain Centre (DMC) endemic genus Glumicalyx was investigated here. The DMC comprises the Drakensberg Mountains of eastern South Africa and the Maloti Mountains of Lesotho. It forms a biodiversity hotspot as a result of its high species richness and endemism. Speciation in the DMC is predicted to be due to ecological factors, due to the topographic and edaphic variation resulting in a multitude of microhabitats available to both plants and their pollinators in the region. Vicariance due to tectonic uplift and subsequent large-scale erosion creating novel high altitude habitats and fragmenting species ranges is likely to have also played a role (Bentley et al. 2014). Diversification of the DMC endemic lineages is predicted to be relatively young, within the last 5 My, and was likely initiated by tectonic uplift creating novel habitats, including the modern alpine zone. Glumicalyx (Limoselleae, Scrophulariaceae) is the largest of the DMC endemic genera, with six closely-allied species. Glumicalyx is distributed across the DMC with its centre in the Lesotho Maloti Mountains. The aim of this study was to investigate the evolutionary trends and speciation in Glumicalyx, specifically exploring the role of pollinators and habitat as likely ecological drivers. With further investigation of the comparative reproductive biology of three co-occurring species of Glumicalyx. To investigate the speciation and evolution of the genus a molecular phylogeny was produced using both nuclear (ETS and ITS) and plastid (matK and psbA-trnH) DNA regions. The phylogeny supports the monophyly of the genus, although there was supported incongruence between the nuclear and plastid phylogenies. The phylogenies (nuclear and plastid) require better resolution, as there was insufficient variation to fully resolve the species relationships in Glumicalyx. The widely distributed species G. nutans is paraphyletic, with the Lesotho endemic G. lesuticus nested within G. nutans. Glumicalyx lesuticus most likely diverged from G. nutans in sympatry, as the distribution of G. nutans overlaps with G. lesuticus and the species often co-occur. The incongruence between the phylogenies makes conclusions about the modes of speciation between sister taxa challenging. The genus appears to have speciated ecologically both in sympatry and allopatry, as the species exhibit variation in morphological traits and habitat preference. Differences in floral traits among closely related species often reflects a difference in pollinators. Pollinators play an important role in promoting reproductive isolation and thereby speciation. The reproductive biology of three co-occurring species of Glumicalyx, representative of the floral morphology in the genus, are investigated. This study provides the first account of the breeding system and pollination in Glumicalyx. All three species are dependent on pollinators for successful reproduction, although G. montanus is partially self-compatible. Glumicalyx goseloides was the only species found to be pollen limited, a finding that was supported by the lack of effective pollinators observed. Glumicalyx nutans was pollinated by noctuid moths based on the analysis of pollen loads and plant-pollinator fit. Glumicalyx montanus was mostly likely pollinated by short-tongued flies and noctuid moths, based on visitation and analysis of pollen loads. Among the three species there is substantial variation in floral morphology (corolla tube length and width) and floral traits that act to attract (floral colour and scent) and reward (nectar) pollinators. Floral scent composition varied between species and between day and night sampling, with significant increases in scent emission rate at night. Although effective pollinators were not observed for G. goseloides, the long, narrow corolla tube, floral scent and nectar production indicate specialized pollination. To further explore the role of pollinators as ecological drivers of diversification in Glumicalyx, a more resolved phylogeny in combination with a more extensive study of the reproductive biology of the genus is needed.