New data from the Middle Jurassic of China shed light on the phylogeny and origin of the proboscis in the Mesopsychidae (Insecta: Mecoptera)

Abstract

Background: The Mesopsychidae is an extinct family of Mecoptera, comprising eleven described genera from Upper Permian to Lower Cretaceous deposits. In 2009, several well-preserved mesopsychids with long proboscides were reported from the mid Mesozoic of Northeastern China, suggesting the presence of pollination mutualisms with gymnosperm plants and highlighting their elevated genus-level diversity. Since that time, additional mesopsychid taxa have been described. However, the phylogeny of genera within Mesopsychidae has not been studied formally, attributable to the limited number of well-preserved fossils.

Results: Here, we describe two new species, Lichnomesopsyche prochorista sp. nov. and Vitimopsyche pristina sp. nov. and revise the diagnosis of Lichnomesopsyche daohugouensis Ren, Labandeira and Shih, 2010, based on ten specimens from the latest Middle Jurassic Jiulongshan Formation of Inner Mongolia, China. After compiling data from these new fossil species and previously reported representative taxa, we conducted phylogenetic analyses and geometric morphometric studies that now shed light on the taxonomy and phylogeny of Mesopsychidae. We also evaluate the recurring origin of the siphonate proboscis in the Mecoptera and propose an evolutionary developmental model for its multiple origins.

Conclusions: Phylogenetic and geometric morphometric results confirm the establishment of two new species, each to Lichnomesopsyche and Vitimopsyche. Vitimopsyche pristina sp. nov. extends the existence of the genus Vitimopsyche Novokshonov and Sukacheva, 2001, from the mid Lower Cretaceous to the latest Middle Jurassic. Two methods of analyses indicate an affiliation of Mesopsyche dobrokhotovae Novokshonov, 1997 with Permopsyche Bashkuev, 2011. A phylogenetic analysis of the Mesopsychidae supports: 1), Mesopsychidae as a monophyletic group; 2), Mesopsyche as a paraphyletic group, to be revised pending future examination of additional material; and 3), the independent origin of the proboscis in the Pseudopolycentropodidae, its subsequent loss in earliest Mesopsychidae such as Epicharmesopsyche, its re-origination in the common ancestor (or perhaps independently) in the Vitimopsyche and Lichnomesopsyche clades of the Mesopsychidae. The third conclusion indicates that the proboscis originated four or five times within early Mecoptera, whose origin is explained by an evolutionary developmental model.

Fig. 1

Line drawings of forewing samples for 14 representative species used in analyses. a Permopsyche rasnitsyni, from Bashkuev, 2011 [22]. b Permopsyche issadensis, from Bashkuev, 2011 [22]. c Permopsyche belmontensis, from Riek, 1953 [16] and Bashkuev, 2011 [22]. d Mesopsyche triareolata, from Bashkuev, 2011 [22] and Lambkin, 2014 [24]. e Mesopsyche dobrokhotovae, from Novokshonov, 1997 [18] and Bashkuev, 2011 [22]. f Mesopsyche shcherbakovi, from Novokshonov, 1997 [18]. g Lichnomesopsyche gloriae, from Ren, Labandeira, and Shih, 2010 [21]. h Lichnomesopsyche daohugouensis, from Ren, Labandeira, and Shih, 2010 [21]. i Epicharmesopsyche pentavenulosa, from Shih, Qiao, Labandeira, and Ren, 2013 [23]. j Vitimopsyche kozlovi from Ren, Labandeira, and Shih, 2010 [21] (one crossvein [between MP2 and MP3] estimated using other two species of the same genus). k Vitimopsyche torta, from Novokshonov and Sukacheva, 2001 [19] (two landmarks [for endings of 1A and 2A] estimated using average of the other two species of the genus). l Permopanorpa inaequalis, from Beckemeyer and Hall, 2007 [51]. m Protopanorpa longicubitalis, from Bashkuev, 2010 [39]. n Pseudopolycentropus janeannae, from Ren et al., 2010 [8]. Scale bars represent 5 mm in (e) and (g–m), 1 mm in (a–c), and 3 mm in (d), (f) and (n)

Fig. 2

The landmark numbers of the four forewing samples for the case of 38 landmarks. a Vitimopsyche pristina sp. nov. (original). b Epicharmesopsyche pentavenulosa, from Shih, Qiao, Labandeira, and Ren, 2013 [23]. c Permopanorpa inaequalis, R. J. Tillyard, 1926 [37]. d Pseudopolycentropus janeannae, from Ren et al., 2010 [8]. Not to scale

Fig. 3

The landmark numbers of the four forewing samples for the case of 42 landmarks. a Vitimopsyche pristina sp. nov. (original). b Permopanorpa inaequalis, R. J. Tillyard (1926) [37]. c Protopanorpa longicubitalis, from Bashkuev (2010) [39]. d Pseudopolycentropus janeannae, from Ren et al. (2010) [8]. Not to scale

Fig. 4

Lichnomesopsyche prochorista sp. nov., holotype specimen CNU-MEC-NN-2015002p/c. a Photograph of part. b Photograph of counterpart. c Overlay drawing of part. d Line drawings of right fore and hind wings. Scale bars represent 5 mm in (a–d)

Fig. 5

Detail structures of Lichnomesopsyche prochorista sp. nov., holotype specimen CNU-MEC-NN-2015002p. a Photograph under ethanol of head and antennae. b Overlay drawing of the head and antennae. c Photograph of genitalia with vestiture in dorsal view, under alcohol. d Overlay drawing of female genitalia in dorsal view. e Photograph under ethanol of the proboscis base. f Photograph under ethanol of tarsi and associated two claws of right foreleg. Scale bars represent 1 mm in (a–d) and (f), 0.5 mm in (e). Corresponding abbreviations are: A7: the seventh segment of the abdomen; A8: the eighth segment of the abdomen; A9: the ninth segment of abdomen; A10: the tenth segment of the abdomen

Fig. 6

Lichnomesopsyche prochorista sp. nov., paratype specimen CNU-MEC-NN-2015008. a Photograph of specimen. b Overlay drawing of habitus. c Photograph under ethanol of male genitalia with vestiture in dorsal view. d Photograph under ethanol of head and part of thorax in dorsal view. Scale bars represent 5 mm in (a) and (b), 1 mm in (c), and 2 mm in (d). Corresponding abbreviations are: A7: the seventh segment of the abdomen; A8: the eighth segment of the abdomen; A9–10: the nine to tenth segments of the abdomen

Fig. 7

Lichnomesopsyche prochorista sp. nov., paratype specimens CNU-MEC-NN-2015001p/c and CNU-MEC-NN-2015016p/c. Specimen CNU-MEC-NN-2015001p: a Photograph of part. b Overlay drawing of right forewing. c Overlay drawing of right hind wing. Specimen CNU-MEC-NN-2015016p: d Photograph of part. e Overlay drawing of right forewing. f Overlay drawing of right hind wing. Scale bars represent 5 mm in (a–f)

Fig. 8

Lichnomesopsyche daohugouensis Ren, Labandeira and Shih, 2010, new specimen CNU-MEC-NN-2015003p/c. a Photograph of part. b Photograph of counterpart. c Overlay drawing of part. d Overlay drawings of hind wings. Scale bars represent 5 mm in (a–c), 3 mm in (d)

Fig. 9

Lichnomesopsyche daohugouensis Ren, Labandeira and Shih, 2010, new specimen CNU-MEC-NN-2015011p/c. a Photograph of part. b Photograph of counterpart. c Overlay drawing of part. d Overlay drawings of right fore and hind wings. Scale bars represent 5 mm in (a–d)

Fig. 10

Vitimopsyche pristina sp. nov., holotype CNU-MEC-NN-2015009. a Photograph of specimen CNU-MEC-NN-2015009. b Overlay drawing of CNU-MEC-NN-2015009. c Photograph under ethanol of head and proboscis. d Photograph under ethanol of female genitalia. e Overlay drawing of left fore and hind wings. Scale bars represent 5 mm in (a) and (b), 2 mm in (c), 1 mm in (d), and 3 mm in (e)

Fig. 11

Results of phylogenetic analyses (NONA and PAUP). a The most parsimonious tree with bootstrap support by NONA. b The consensus tree by PAUP. White circles indicate homoplasious characters, and the black circles indicate non-homoplasious characters. The numbers above branches are character numbers, below branches are character states, and the red numbers below the branches are bootstrap values in (a)

Fig. 12

Resulting Trees for the geometric morphometric analyses. a Tree 1 for 38 landmarks (including 3 outgroups, no crossvein characters). b Tree 2 for 42 landmarks (including 3 outgroups, two crossvein characters)

Fig. 13

An adult mouthpart phenotype with medial fusion of labial palps in Tribolium castaneum resulting from larval RNAi knockdown of the genes homothorax (hth) and extradenticle (ext). The example represents a more severe case in the transformation of the loss of labial glossa and paraglossal elements, significant size reduction of the mentum (mnt) and prementum, and fusion of the labial palps into a single medial structure. Abbreviations for maxillary elements are: crd, cardo; stp, stipes; plf, palpiger; lac, lacinia; and gal, galea. Abbreviations for labium are: plg, paliger, lp3 labial palp segment 3. This figure was redrawn from Fig. 1P of Smith and Jockusch (2014) [53]