From near extinction to diversification by means of a shift in pollination mechanism in the gymnosperm relictEphedra(Ephedraceae, Gnetales)

Abstract

Pollination in gymnosperms is usually accomplished by means of wind, but some groups are insect-pollinated. We show that wind and insect pollination occur in the morphologically uniform genus Ephedra (Gnetales). Based on field experiments over several years, we demonstrate distinct differences between two Ephedra species that grow in sympatry in Greece in pollen dispersal and clump formation, insect visitations and embryo formation when insects are denied access to cones. Ephedra distachya, nested in the core clade of Ephedra, is anemophilous, which is probably the prevailing state in Ephedra. Ephedra foeminea, sister to the remaining species of the genus, is entomophilous and pollinated by a range of diurnal and nocturnal insects. The generalist entomophilous system of E. foeminea, with distinct but infrequent insect visitations, is in many respects similar to that reported for Gnetum and Welwitschia and appears ancestral in Gnetales. The Ephedra lineage is well documented already from the Early Cretaceous, but the diversity declined dramatically during the Late Cretaceous, possibly to near extinction around the Cretaceous-Palaeogene boundary. The clade imbalance between insect-and wind-pollinated lineages is larger than expected by chance and the shift in pollination mode may explain why Ephedra escaped extinction and began to diversify again.

Pleistocene refugia in the Chihuahuan Desert: the phylogeographic and demographic history of the gymnosperm Ephedra compacta

“…Frugivorous birds disperse the seeds of E. compacta, which are enclosed in the red fleshy seed cones (Hollander & Vander Wall, 2009;Ickert-Bond & Wojciechowski, 2004). In contrast, pollination is mediated by wind (Bolinder et al, 2016;Niklas & Buchmann, 1987). Unlike other gymnosperms (e.g.…”

The Gnetales: Recent insights on their morphology, reproductive biology, chromosome numbers, biogeography, and divergence times

“…K). Pollen ultrastructure in Ephedra appears to relate to pollination biology (Bolinder et al, ; Bolinder et al, ). Using both wind‐ and insect‐ pollinated species of Ephedra , Bolinder and colleagues experimentally confirmed that the three‐parted ectexine, composed of an undulating tectum, a granular infratectum and a narrow foot layer, influences grains' settling velocity.…”

“…The organization of the bisexual cones differs among the three genera: in Welwitschia the male cones are made up of reproductive units that are structurally bisexual, with microsporophylls and a sterile ovule, whereas in Ephedra foeminea (the only Ephedra species with bisexual cones) and most species of Gnetum the male cones are made up of separate male reproductive units and sterile female reproductive units. It appears that the presence of sterile ovules with pollination formation in the male cones is linked to pollinator nectar rewards, and insect pollination may be the ancestral condition in the Gnetales (Jörgensen & Rydin, ; Rydin & Bolinder, ; Bolinder et al, ).…”

“…Two of the three published chromosome counts in Gnetum appear to reflect tetraploidy (Gnetum montanum, 2n ¼ 44; Hizume et al, 1993;Gnetum ula, 2n ¼ 22;Ohri & Khoshoo, 1986;Gnetum gnemon, 2n ¼ 44, Ickert-Bond et al, 2015). Bolinder et al (2016) argue for a shift to wind pollination within crown-group Ephedra that could explain the puzzling geological history of the Ephedra lineage (see below Recent studies of the fossil record). Initially, in the Early Cretaceous, insect-pollinated stem relatives diversified, subsequently declined to near-extinction in the Late Cretaceous, and after a shift to wind pollination early in diversification of the crown group in the Tertiary the Ephedra lineage resurged (Bolinder et al, 2016).…”

New perspectives in nectar evolution and ecology: simple alimentary reward or a complex multiorganism interaction?

“…Pollination drops, i.e., sugary secretions produced by ovules, occur in most gymnosperms and their primary functions are pollen capture and nourishment. Although most gymnosperms are wind pollinated, insect contribution to pollination is also reported in several Gnetophyta [9][10][11][12][13]. When insects are involved, they generally feed on the pollination drops, as they do with angiosperm floral nectar.…”