Insect pollination of cycads

Abstract

Most cycads have intimate associations with their insect pollinators that parallel those of well-known flowering plants, such as sexually deceptive orchids and the male wasps and bees they deceive. Despite this, the mistaken belief that cycads are mostly wind-pollinated is still commonly expressed. Perhaps as a consequence, cycad-pollinator systems are rarely exemplified in studies of the role of pollinators in plant evolution and diversification. Although first recognised more than a century ago, specialised associations between cycads and their insect pollinators have been elucidated experimentally only in the past few decades. This review covers the history of understanding pollination in cycads, the advances that have been made since the 1980s using field observations and experiments, and analyses of molecular data from the population to phylum level. We outline areas for future research to address how such interactions might have affected speciation and extinctions. We stress that inclusion of cycads in broader considerations of the role of pollinators in plant diversification is important because they are phylogenetically distant from flowering plants and their pollination systems might have evolved independently of one another. This review is timely because cycads are a globally threatened group that might be vulnerable to co-extinction with pollinator loss.

Reproductive biology of the South American cycad Zamia boliviana, involving brood‐site pollination

“…The reliance on specialized and obligatory biotic vectors for reproduction increases the risks of reproductive failure for both plant and pollinator. The reproductive biology of the Zamiaceae family (Cycadales) is characterized by cross‐pollination and predominantly obligatory and specialized mutualistic interactions between pollinators and their host plants, in some cases described as a cycad brood‐site pollination mutualism (Hall, Walter, Bergstrom, & Machin, 2004; Norstog & Fawcett, 1989; Norstog, Stevenson, & Niklas, 1986; Segalla et al, 2019; Suinyuy, Donaldson, & Johnson, 2009; Tang, 1987; Terry, 2001; Terry et al, 2005; Toon, Terry, Tang, Walter, & Cook, 2020; Valencia‐Montoya, Tuberquia, Guzmán, & Cardona‐Duque, 2017; Vovides, 1991).…”

Opsin Evolution in Flower-Visiting Beetles

“…Such sensory adaptations can be seen in the flabellate (fan-shaped) antennae of Macrosiagon limbatum (Ripiphoridae). Additionally, if odor was a primary cue in ancient cycads, as in modern species (Toon et al, 2020), lineages such as the false oil beetles (Oedemeridae) may have initially established olfactory rather than visual specializations that persisted after they transitioned to angiosperm hosts (Peris et al, 2017). A UVgreen color channel system may be adequate to detect floral cues commonly attractive to beetles, e.g., white and yellow (Reverté et al, 2016), but wavelength sensitivity expansion may be advantageous to detect floral cues that fall outside this spectral range (e.g., pink or violet).…”

“…Beetles were some of the earliest pollinators and remain the primary pollinators of ancient plant group, gymnosperms (Toon et al, 2020), while also functioning as common pollinators of more recent angiosperm (flowering plant) radiations. Angiosperm radiations during the Cretaceous cooccurred with accelerated diversification among the holometabolous insects that comprise the dominant insect pollinators: hymenopterans, lepidopterans, dipterans and coleopterans (Doyle, 2012;Misof et al, 2014).…”

Plants Are the Drivers of Geographic Variation of Floral Scents in a Highly Specialized Pollination Mutualism: a Study of Ficus Hirta in China

“…Brood site pollination mutualisms are diversi ed as to the resource on which pollinator offspring feed. They may develop feeding on young seeds (Yucca [20], Phyllanthaceae [21]), galled plant ovules (Ficus [22]), pollen (Castilla [23]), decaying stamens (Cyclanthaceae [24]), decaying male in orescences or post anthesis male in orescence structures (Cycadales [25], Cyclanthaceae [24], Arecaceae [17]), fungi growing on male in orescences (Artocarpus [26]), or nectar produced by oral bracts (Macaranga [27]).…”

“…For instance, in most obligate brood site pollination mutualisms, owers are inconspicuous, with yuccas a notable exception, and chemical signalling by the plants constitutes the main cue used by pollinators to locate receptive owers [18]. The attractive odours may be emitted by receptive owers (Phyllanthaceae [19]), in orescences (Ficus [20], Cycadales [21], Araceae [22]), or even leaves (Chamaropsis [18]), providing a diversity of ontogenic and evolutionary origins of signalling. Despite the central role played by odours in these systems, little is known about micro and macro-evolutionary patterns and processes of oral odour evolution and few predictions about their evolution have been made.…”