False Blister Beetles and the Expansion of Gymnosperm-Insect Pollination Modes before Angiosperm Dominance

Abstract

During the mid-Cretaceous, angiosperms diversified from several nondiverse lineages to their current global domination [1], replacing earlier gymnosperm lineages [2]. Several hypotheses explain this extensive radiation [3], one of which involves proliferation of insect pollinator associations in the transition from gymnosperm to angiosperm dominance. However, most evidence supports gymnosperm-insect pollinator associations, buttressed by direct evidence of pollen on insect bodies, currently established for four groups: Thysanoptera (thrips), Neuroptera (lacewings), Diptera (flies), and now Coleoptera (beetles). Each group represents a distinctive pollination mode linked to a unique mouthpart type and feeding guild [4-9]. Extensive indirect evidence, based on specialized head and mouthpart morphology, is present for one of these pollinator types, the long-proboscid pollination mode [10], representing minimally ten family-level lineages of Neuroptera, Mecoptera (scorpionflies), and Diptera [8, 10, 11]. A recurring feature uniting these pollinator modes is host associations with ginkgoalean, cycad, conifer, and bennettitalean gymnosperms. Pollinator lineages bearing these pollination modes were categorized into four evolutionary cohorts during the 35-million-year-long angiosperm radiation, each defined by its host-plant associations (gymnosperm or angiosperm) and evolutionary pattern (extinction, continuation, or origination) during this interval [12]. Here, we provide the first direct evidence for one cohort, exemplified by the beetle Darwinylus marcosi, family Oedemeridae (false blister beetles), that had an earlier gymnosperm (most likely cycad) host association, later transitioning onto angiosperms [13]. This association constitutes one of four patterns explaining the plateau of family-level plant lineages generally and pollinating insects specifically during the mid-Cretaceous angiosperm radiation [12].

Beetle Pollination of Cycads in the Mesozoic

“…Although it is well documented that cycads were diverse and abundant during the mid-Mesozoic, little is known about their biogeography and pollination before the rise of angiosperms. Direct fossil evidence illuminating the evolutionary history of cycads is extremely rare [4,5]. Here we report a specialized beetle-mediated pollination mode from the mid-Cretaceous of Myanmar, wherein a new boganiid beetle, Cretoparacucujus cycadophilus, with specialized pollen-feeding adaptations in its mouthparts and legs, was associated with many pollen grains of Cycadopites.…”

“…Like boganiids, the present global distribution of pollinating erotylids in Africa, Asia, Australia, and North and Central America [3] suggests an early development of an erotylid-cycad relationship before late-Mesozoic continental drift [35]. Collectively, the preliminary cycad-insect associations are probably ancient, extending to the Triassic or earlier [28], whereas insect pollination of cycads may be as early as the Early Jurassic [4,9,12], long before the origin and diversification of major groups of angiosperms and the concomitant diversification of angiosperm pollinators such as moths, flies, and bees later in the Cretaceous [5,6,36,37]. Moreover, such an ancient association was probably widespread at least Figure S3 and Table S1.…”

Early Cenomanian palynofloras and inferred resiniferous forests and vegetation types in Charentes (southwestern France)

“…previously underestimated high variability of climatic parameters (Berner, 2003;Keller et al, 2011;Littler et al, 2011;Fiedrich et al, 2012;Hay and Floegel, 2012), affected trophic networks and faunal clades (Labandeira, 2006;Kergoat et al, 2014;Peris et al, 2017) and irreversibly altered the composition of the overall terrestrial ecosystems (Meredith et al, 2011).…”

Pollinator Diversity: Distribution, Ecological Function, and Conservation

“…Fossil insects from China, Spain and Russia have revealed ancient groups of insects that appear, based on interpretations of their mouthparts and associated pollen grains, to have been pollinators; examples include mid-Mesozoic thrips (Thysanoptera), flies (Diptera), lacewings (Neuroptera), scorpionflies (Mecoptera) and beetles (Coleoptera) (Ren 1998;Ren et al 2009;Labandeira 2010;Labandeira et al, 2007Labandeira et al, , 2016Peñalver et al 2012Peñalver et al , 2015Peris et al in press). It is notable that lacewings and scorpionflies are no longer significant pollinators (in terms of diversity) compared to groups such as the bees (Hymenoptera) and butterflies and moths (Lepidoptera) that have replaced them over time (see section 2.1).…”