Life habits and evolutionary biology of new two-winged long-proboscid scorpionflies from mid-Cretaceous Myanmar amber

Abstract

Long-proboscid scorpionflies are enigmatic, mid-Mesozoic insects associated with gymnosperm pollination. One major lineage, Aneuretopsychina, consists of four families plus two haustellate clades, Diptera and Siphonaptera. One clade, Pseudopolycentropodidae, from mid-Cretaceous Myanmar amber, contains Parapolycentropus. Here, we newly establish Dualula, assigned to Dualulidae, constituting the fifth lineage. Parapolycentropus and Dualula lineages are small, two-winged, with unique siphonate mouthparts for imbibing pollination drops. A cibarial pump provides siphonal food inflow; in Dualula, the siphon base surrounds a hypopharynx housing a small, valved pump constricted to a narrow salivary duct supplying outgoing enzymes for food fluidization. Indirect evidence links long-proboscid mouthpart structure with contemporaneous tubulate ovulate organs. Direct evidence of gymnospermous Cycadopites pollen is associated with one Parapolycentropus specimen. Parapolycentropus and Dualula exhibit hind-wing reduction that would precede haltere formation, likely caused by Ultrabithorax. Distinctive, male Aneuretopsychina genitalia are evident from specimens in copulo, supplemented by mixed-sex individuals of likely male mating swarms.

Fig. 1

Results of the phylogenetic analysis by NONA. a Strict consensus tree of 93 maximum parsimony trees from NONA. b The twenty-fourth maximum parsimony tree from the NONA analysis. Open circles are plesiomorphic characters; solid black circles are apomorphic characters. The numbers above branches are characters; numbers below the branches are character states; and magenta numbers below the branches are bootstrap values in a and b. Colored arrows refer to the following clades or lineages: magenta = Aneuretopsychina sensu lato; green = Aneuretopsychidae + (Mesopsychidae + Nedubroviidae); blue = (Parapolycentropus + Dualulidae) + (basal Diptera + Siphonaptera); brown = Parapolycentropus + Dualulidae; black = basal Diptera and Siphonaptera

Fig. 2

Photos and line drawings of holotype with details of the proboscis and genitalia. Dualula kachinensis gen. et sp. nov., CNU-MEC-MA-2014001, female. a Holotype in dorsal view. b Holotype in ventral view. c Details of setae on the margin and membrane of the left forewing, enlarged from blue template in a. d Overlay drawing of holotype in dorsal view. e Line drawing of forewings. Above is the right forewing and below is the left forewing. f Female genitalia in ventral view, enlarged from green template in a. g Proboscis terminus, with details in ventral view, enlarged from the larger magenta template in b. h Proboscis midsection in ventral view, enlarged from the smaller magenta template in b. i Overlay drawings of the head and proboscis tip details, based on a. Ant antenna, CE compound eye, Cl clypeus, fc food canal, La labrum, mp maxillary palp, and Pr proboscis. Scale bars represent 2 mm in a, b, d and e; 0.5 mm in f and i; 0.2 mm in g; 0.1 mm in c and h; and 0.05 mm in proboscis tip from i

Fig. 3

Hind wings of holotype Dualula kachinensis gen. et sp. nov. of CNU-MEC-MA-2014001. a Thorax in dorsal view. b Thorax in ventral view. c Right hind wing in ventral view, enlarged from blue template in b. d Left hind wing in ventral view, enlarged from green template in b. e Line drawings of left hind wing, above in dorsal view and below in ventral view. f Left hind calypter in dorsal view, enlarged from the red template in a. Scale bars represent 0.2 mm in a‒f

Fig. 4

Reconstruction of head and mouthparts of male Dualula kachinensis gen. et sp. nov. The drawing is based mostly on specimen CNU-MEC-MA-2017017, supplemented by CNU-MEC-MA-2014001 and CNU-MEC-MA-2017016. A section representing the upper proximal third of the galeae has been removed to reveal features below of the pharyngeal pump. This subfigure was created from microscope photographs of the amber specimen by Conrad Labandeira as a hand drawing modified in Adobe Photoshop CC by Xiaodan Lin. Scale bar represents 0.5 mm

Fig. 5

Nano-CT and Micro-CT images of Parapolycentropus paraburmiticus head and associated pollen grain. Specimen CNU-MEC-MA-2015054; new material, male. a Insect in right lateral view. b Insect in left lateral view. c Head and mouthparts in dorsal view. d Nano-CT images of the proboscis base in ventral view, from the blue template in c. e Nano-CT images of a likely pollen grain near the right galea from the red template in c. f Nano-CT images of the left galeal tip from the green template in c. g Nano-CT images of the hypopharynx tip and associated external ornament in dorsal view, from the black template in c. h Line drawing of the head and proboscis in c. i 3-D reconstruction of head in lateral view from a micro-CT scan. j The same 3-D reconstruction of head in i, except in ventral view. Images i and j are from Micro-CT scanning, reconstructed in Amira software. Cl clypeus, ga galea, hy hypopharynx, La labrum, mp maxillary palp, sc bands sclerotized proboscis bands. Scale bars represent 1 mm in a and b; 0.2 mm in c and h; 30 μm in d; 10 μm in e; 15 μm in f; and 20 μm in g. Scale bars are absent in i and j

Fig. 6

A male Parapolycentropus paraburmiticus associated with Cycadopites sp. pollen grains. Concentrations of pollen surround the mouthparts, antennae, legs and wings (CNU-MEC-MA-2017012, new material). a The insect specimen. b Line drawing of the entire insect in a surrounded by Cycadopites pollen grains, shown as tiny red dots. c Plot of Cycadopites dimensions, shown as length (L) along the horizontal axis and corresponding width (W) along the vertical axis. The pollen-grain measurement data is from a and b, available in Supplementary Data 3. d Head, prothorax and proximal forelegs, enlarged from template in a. e Proboscis tip with galeae and hypopharynx surrounded by pollen grains, enlarged from d. Enlargement of several pollen grains near the proboscis tip at right. f Enlargement of right foreleg in d, with arrows pointing to nearby Cycadopites grains and clumps. g Enlargement of the right middle and hind legs in a, showing adjacent pollen indicated by arrows. h Pollen grains near the antennal tip outlined in a. i Proximal aspect of the proboscis and associated mouthparts with three pollen grains indicated by arrows. j Tarsus of right hind leg, indicted in a, with adjacent pollen indicated by arrows. Scale bars represent 0.5 mm in a and b; 0.1 mm in e‒g and j; 0.2 mm in d; 50 μm in h and i; and 20 μm in-group of pollen grains from e

Fig. 7

Photos and line drawings of a female four-winged Parapolycentropus. CNU-MEC-MA-2017006, new material with the redrawn images of forewings of two species of Parapolycentropus. a Specimen in right lateral view. b Same specimen at a in left lateral view. c Line drawings of right wings. d Line drawings of left wings. e Reconstructed forewing of P. burmiticus. f Reconstructed forewing of P. paraburmiticus. In c and d, forewings are black and hind wings are blue. Wings e and f, based on a published reconstruction in figure 8b and 8d of Grimaldi et al.. Scale bars represent 1 mm in a and b, and 0.5 mm in c, d Subfigures e and f lack scale bars