Diverse Mesozoic thrips carrying pollen during the gymnosperm-to-angiosperm plant-host ecological shift

Abstract

Insects are important pollinators, and entomophilous pollination of gymnosperms occurred long before the Cretaceous radiation of angiosperms, but most extant pollination systems involve angiosperms. We studied four thrips of the extinct genus Tethysthrips present in Albian (Early Cretaceous) Spanish amber, one of which carried a patch of gymnosperm Cycadopites pollen grains, some of them attached around the mouthparts, providing direct fossil evidence of pollinivory and pollination. We describe the new species Tethysthrips attenboroughi, which belongs to the extant family Thripidae (suborder Terebrantia). In addition, we studied a Cycadopites pollen load in one specimen belonging to stem group Phlaeothripidae (suborder Tubulifera), from Cenomanian Burmese amber. This illustrates an ancient stage of gymnosperm plant host that most likely favored the later stage involving angiosperms. The absence of extant pollinators of gymnosperms in Thripidae and Phlaeothripidae, and in the terebrantian family Melanthripidae, which contain Cretaceous pollinators of gymnosperms, indicates impoverishment in their gymnosperm relationship.

Keywords: Evolutionary history; Evolutionary processes; Paleontology.

Graphical abstract

Figure 1

Anatomical features of holotype of Tethysthrips attenboroughi nov. sp. (Thripidae), Museo de Ciencias Naturales de Álava (MCNA) 12629a, female, in an amber fragment from upper Albian Peñacerrada I outcrop (Moraza, Burgos, Spain) (A) Dorsal habitus. (B) Antennal segments III and IV showing sensoria elongate and forked (pairs of arrows). (C) Head in ventral view showing mouthparts and pollen grains attached; see camera lucida drawing in Figure 2D. (D) Head in dorsal view showing three pairs of post-ocular setae (asterisks) and ommatidia. (E) Chaetotaxy on pronotum and pollen grains attached to posteroangular setae (right). (F) Right forewings and hind wings in ventral view (arrow indicates tenuous longitudinal vein of hind wing). Scale bars 0.1 mm (A and F), 0.05 mm (B–E). All are image compositions (Photoshop CS2, version 9.0; www.adobe.com). See also Figures S3 and S4.

Figure 2

Holotype, MCNA 12629a, female, and paratype, MCNA 12629a, female, of Tethysthrips attenboroughi nov. sp. (Thripidae) in same amber fragment from upper Albian Peñacerrada I outcrop (Moraza, Burgos, Spain) (A) Holotype and paratype in dorsal views. (B) Drawing of holotype habitus with Cycadopites pollen grains (red colored) observed in dorsal view, some of them forming groups by contact (two main groups encircled) indicating clumping due to stickiness (forewing venations and margins gray colored). (C) Holotype and paratype in ventral views. (D) Drawing of holotype head and anterior part of thorax with Cycadopites pollen grains (red colored) observed in ventral view, several of them in contact or very close to mouthparts (antennal sensoria and palps gray colored). Scale bars 0.5 mm (A and C), 0.1 mm (B and D). (A) and (C) are image compositions (Photoshop CS2, version 9.0; www.adobe.com).

Figure 3

Load of Cycadopites pollen grains on or close to the Tethysthrips attenboroughi nov. sp. body, holotype (female), piece MCNA 12629, found in upper Albian Peñacerrada I amber (Moraza, Burgos, Spain) (A) Cluster attached to thorax surface and to one of its posteroangular setae showing broad sulci at their equatorial areas. (B) Detached cluster close body showing sulci wider at its ends and evidencing clumping due to stickiness. (C) Prolate grain entangled between fringe cilia of wings with narrow, elongate sulcus. (D) Detached, isolated pollen grain close to forewing with oval sulcus broad at equatorial area. (E) Portion of a stele of detached pollen grains well-showing their 3-dimension morphology (insets with three selected grains enlarged). Scale bars 20 μm (A and B), 50 μm (C–E). (B) and (E) are image compositions with thin black lines separating micrographs of the same view but taken at different focal planes (Photoshop CS2, version 9.0; www.adobe.com).

Figure 4

Insect pollinivory evidence in the fossil record segregated between gymnosperm (blue area) and angiosperm (orange area) pollen and detail of five Cretaceous thysanopteran species having gymnosperm pollen loads constituted by the form genus Cycadopites The 15 insect groups represented as silhouettes showing fossil evidence of pollinivory (and perhaps pollination as well) are from the bottom and left to right (silhouettes not at the same scale): Permian, Sojanidelia florea (Paoliidae), Tschekardaenigma pollinivorum (Grylloblattodea family indet.), Parapsocidium uralicum (Psocidiidae), Idelopsocus diradiatus (Hypoperlidae), and Sellardsiopsis conspicua (Palaeomanteidae); Jurassic, Aboilus amplus and Aboilus sp. aff. dilutus (Prophalangopsidae); Cretaceous, the three Albian terebrantian thrips species represented in detail on the right, Prosphex anthophilos (Aculeata indet.), Psocorrhyncha burmitica (Archipsyllidae), and the two Cenomanian thrips species represented in detail on the right, one terebrantian and one tubuliferan (encircled); and Paleogene, Hirmoneura messelense (Nemestrinidae). The five thysanopterans represented on the right are four species in three genera of three Terebrantia families from upper Albian Peñacerrada I amber (Spain) and Cenomanian Burmese amber (Myanmar) and the only known species of a Tubulifera with direct evidence of pollination, from Burmese amber. Coloration of the five thrips species and pollen grains are conjectural. Arrows indicate some patches of pollen grains adhered to the bodies based on the amber records available. The five species reconstructions are of females, despite the stenurothripid specimen with a load being a male. The thrips are at the same scale, and the enlarged pollen grains (these last represented with their average sizes) as well.