A New Genus and Species of Lophocateridae from Mid-Cretaceous Amber of Myanmar (Coleoptera)

Simple Summary Lophocateridae are a small family of Cleroidea and their taxonomic rank has changed several times. The fossil record of Lophocateridae from Mesozoic deposits is sparse. Here, we figure and describe a new lophocaterid fossil, Gracilenticrus burmiticus, from the mid-Cretaceous amber of Myanmar. The new taxa broaden the generic and species diversity of lophocaterids and provide additional information for understanding the early evolution of Cleroidea. Abstract A new genus and species of the cleroid family Lophocateridae are described and illustrated from the mid-Cretaceous amber of northern Myanmar. Gracilenticrus burmiticus Yu, Kolibáč & Ślipiński gen. et sp. nov. is unique among Lophocateridae in the tiny body size, frontoclypeal suture and antennal grooves absent, symmetrical antennal clubs, protrochantin reduced, tarsal claws small and widened at base. A key to the species of Mesozoic Lophocateridae is also provided. Morphological characters of the newly discovered Gracilenticrus were analyzed together with representatives of 43 extant genera of Cleroidea (broadly defined Trogossitidae) in a matrix of 91 characters. Gracilenticrus burmiticus was resolved as a member of Lophocateridae. The discovery of a diverse fauna of Lophocateridae in the mid-Cretaceous sheds a new light on the early evolution of superfamily Cleroidea.


Introduction
The family Lophocateridae are a small cosmopolitan family of cleroid beetles, comprising approximately 120 extant species in about 17 genera [1][2][3]. This group was assigned as a subfamily or tribe of Trogossitidae in previous studies [4][5][6][7][8][9]. However, the traditional broadly defined Trogossitidae are widely presumed to be paraphyly or polyphyletic by many molecular analyses [10][11][12][13][14][15], and the placement of this group is ambiguous. Recently Lophocateridae were re-elevated to the family level and revised to include Parapeltis and Colydiopeltis formerly in Peltinae: Colydiopeltini, and exclude Decamerini based on the most comprehensive molecular analysis by Gimmel et al. [1]. The tribe-level classification of the former Lophocaterinae were also shown to be somewhat problematic [1]. The revised Lophocateridae have been strongly supported as monophyletic. The genus Grynocharis Thomson (formerly in Lophocaterini) was placed as sister to the remainder of the family. ParapeltisŚlipiński, Eronyxa Reitter and Trichocateres Kolibáč occupied relatively basal positions, although their relationships were not fully resovled. The remaining sampled genera (Ancyronini and part of Lophocaterini) constitute a large clade within the family by Gimmel's study [1].
The fossil record of Lophocateridae from Mesozoic deposits is sparse. The only three previously described members of Lophocateridae from mid-Cretaceous Burmese amber are Burmacateres longicoxa Kolibáč & Peris and Parayixianteres parvus Yu, Leschen & Slipiński and Zaiwa pankowskiorum Lyubarsky et al. [16][17][18]. Here, we report another newly discovered genus based on a well preserved inclusion in the Cretaceous Burmese amber, which implies that the family was already diverse by the Cretaceous.

Material and Methods
The Burmese amber specimens studied herein originated from amber mines near Noije Bum, Hukawng Valley, Kachin State, northern Myanmar. Burmese amber is one of the most important of the fossiliferous resins from the Mesozoic, with its paleobiotic diversity reviewed by Ross et al. [19][20][21], and is renowned for yielding rich and exquisitely preserved fauna including well-preserved insects [22][23][24][25]. The age of the amber deposits is considered to be mid-Cretaceous based on U-Pb zircon dating [26,27]. The holotype of Gracilenticrus burmiticus sp. nov. is deposited at the Key Laboratory of Insect Evolution and Environmental Changes, Capital Normal University (CNU), Beijing, China. The amber piece was prepared using a razor table, ground with emery papers with different grit sizes and finally polished with polishing powder.
The specimen was examined under a Leica M205C stereomicroscope (Leica, Wetzlar, Germany). Photographs under incident light were mainly taken with a Canon EOS 5D Mark II camera and a MP-E 65mm f/2.8 1-5X Macro lens (Canon, Tokyo, Japan). Widefield fluorescence images were captured with a Zeiss Axio Imager 2 light microscope combined with a fluorescence imaging system (Zeiss, Jena, Germany). Confocal images were obtained with a Zeiss LSM710 confocal laser scanning microscope, using the 488 nm Argon laser excitation line (Zeiss, Jena, Germany). Images under incident light and widefield fluorescence were stacked in Helicon Focus 7.0.2 or Zerene Stacker 1.04. Confocal images were stacked with color coding for depth in ZEN 2.3 (Blue Edition). Images were further processed in Adobe Photoshop CS6 to enhance contrast.
The morphological terminology follows Lawrence et al. [28] and the classification of families and subfamilies of Cleroidea follows Lawrence et al. [29] with amendments by Gimmel et al. [1].
To evaluate the systematic placement of the new genus, a morphological phylogenetic analysis was performed. The data matrix (Supplemental Material Datas S1-S3) was derived from a previously published dataset [30,31], and includes 91 morphological characters of both adults and larvae. Gracilenticrus gen. nov. was analyzed together with representatives of 43 extant genera of the traditional broadly defined Trogossitidae. Rentonium Crowson (now classified in family Rentoniidae) was selected as the outgroup taxon. The assembled data matrix was analyzed by TNT v. 1.5 software [32] under parsimony, using the implicit enumeration algorithm criterion with all characters unordered. Parsimony analysis using implied weighting (K = 12, as recommended by Goloboff et al. [33] and Smith [34]) yielded a single most parsimonious tree with a step length of 501, a consistency index (CI) of 0.29, and a retention index (RI) of 0.58 (Figure 1).
Diagnosis. As for the genus. Description (based on holotype). Body weakly convex, elongate-oval, with dense pubescence composed of inclined short setae, lateral margins of pronotum broadly explanate, elytra narrowly explanate.
Prothorax transverse, about 0.67 times as long as wide, widest along base, narrowed anteriorly; anterior angles very slightly prominent, blunt; posterior ones also blunt; lateral carinae complete, slightly crenulate; anterior edge and posterior edge slightly produced at middle, sinuate. Pronotal disc weakly convex; conspicuously but sparsely granulate. Procoxal cavities transverse, broadly open externally; prosternal process narrow, parallel, extending well behind procoxae, acute apically with a longitudinal carinae in the middle. Procoxae conspicuously transverse, weakly projecting; protrochantin reduced. Mesoventrite wide and transverse, slightly convex; mesepimeron and mesanepisternum triangular. Mesocoxal cavities slightly oblique and open to mesepimeron. Mesocoxae nearly spherical and narrowly separated, slightly projecting. Metaventrite wide, with complete discrimen, metanepisternum broad. Metacoxae large, flat and extending laterally to meet elytra.    Scutellum weakly transverse, rounded apically. Elytra 1.60 times as long as width combined, 2.67 times as long as pronotum length, oblong, approximately parallel-sided (weakly narrowed at basal third), completely covering abdomen, their humeral portion subequal with pronotal base. Epipleuron moderately broad and apparently complete to apex, widest at humeral portion, gradually narrowed apically. Each elytron with 5 narrow and black costae separated by two rows of punctures bearing posteriorly inclined, somewhat squamiform setae; each costa bears setae similar to those on interstrial punctures; lateral portion of elytra beyond last costa with dense and rather irregular setiferous punctures.

Phylogenetic Results
Previous studies have shown that morphological information alone is not sufficient to solve the phylogeny of traditional trogossitid taxa [1,31]. However, the phylogenetic analysis may still provide some helpful information for the placement of our fossil. In our analysis, the newly discovered fossil, Gracilenticrus burmiticus, was nested within a clade comprising Peltis, Calitys and traditional Lophocaterinae. This clade contains all of the modern Lophocateridae defined by Gimmel et al. [1] except for Colydiopeltis and Parapeltis. Within the clade, the following relationships were recovered: (i) the genus Gracilenticrus gen. nov. was placed as sister to the remainder of the clade; (ii) Calitys (Trogossitidae: Calitynae) and Peltis (Peltidae) formed a grade of early branches; (iii) the remaining part of this clade was split into two groups, with the first group including genera from Lophocateridae, Protopeltidae and Thymalidae, and the second group consisting of eleven Lophocateridae genera. Unfortunately, most terminals in this clade, including Gracilenticrus, have large number of characters coded as uncertain because critical parts were not preserved and larval characters have not been observed. As a result, the position of Gracilenticrus in this cladogram is only tentative and cannot be regarded as firmly solved.

Discussion
Although the placement of Gracilenticrus is not firmly solved by the phylogenetic analysis, it is apparent that Gracilenticrus is closely related to the Lophocateridae group. Based on the detailed examination of morphological characters, the genus can be unequivocally assigned to Lophocateridae. As a member of the Lophocateridae, Gracilenticrus has the weakly convex body with explanate sides, the strongly transverse procoxae, open procoxal cavities and laterally expanded metacoxae reaching the elytral epipleura. On the other hand, Gracilenticrus differs from all other members of Lophocateridae in the absence of frontoclypeal suture, eyes moderate, antennal club symmetrical and protibia with robust spines along edge.
While most of the lophocaterid genera including Ancyrona, Antillipeltis, Colydiopeltis, Grynocharina, Grynoma, Leptonyxa, Lycoptis, Neaspis, Parapeltis, Peltonyxa have 10 or fewer antennomeres, Gracilenticrus has 11-segmented antennae. Based on the characters of anterior pronotal angles and elytra, we can easily distinguish Gracilenticrus from Afrocyrona, Indopeltis and Eronyxa, since Afrocyrona has a distinctly produced forward anterior pronotal angles and elytral scales present; Indopeltis has acute anterior pronotal angles and each elytron having six carinae that are interrupted; and Eronyxa has the anterior pronotal angles not produced forward and elytral carinae reduced. The new genus differs from Trichocateres in the lack of two sharp grooves on the prosternal process and upper surfaces without tufts of long and light-colored hairs. Gracilenticrus is also different from Grynocharis in the absence of antennal grooves, smaller body size, slightly crenulate lateral pronotal carinae (simple in Grynocharis) and each elytron having five carinae (six in Grynocharis). The new genus can be easily distinguished from Lophocateres due to the flat body shape, presence of antennal grooves, absence of denticle on claws, and each elytron with seven carinae of the latter. The new genus seems to be most similar to Promanus in appearance, but the latter has a larger body size and flat body shape, with antennal grooves present and denticles on claws absent. With respect to fossils, Gracilenticrus can be distinguished from Sinosoronia Zhang, Cretamerus Peris, Kolibáč & Delclòs and Promanodes Kolibáč, Schmied, Wappler & Kubisz by having antennae 11-segmented, elytra with distinct longitudinal carinae and regular punctures, and abdomen with five ventrites [35][36][37]. Gracilenticrus also differs from Yixianteres Yu,Ślipiński, Leschen, Ren & Pang and Paracretocateres Yu, Slipiński, Leschen, Ren & Pang in having a smaller and setose body [38]. The previously reported lophocaterid genera from Burmese amber, Parayixianteres Yu, Leschen &Ślipiński and Burmacateres Kolibáč & Peris, differ distinctly from Gracilenticrus in having relatively flattened body, frontoclypeal suture present, slightly asymmetrical antennal club, strongly prominent forward anterior angles and exposed protrochantins. Another lophocaterid genus known from Burmese amber, Zaiwa, has 10-segmented antennae with apical segment more than twice as long as the preceding two, pronotum about 1.8 times as wide as long and elytral without costae, and therefore can be easily distinguished from Gracilenticrus. A key of the Mesozoic Lophocateridae is provided in Appendix A.
Previous studies suggest that the more primitive cleroids were mainly fungus-feeding and predatory followed by later shifts to flower-feeding [1,39]. The weakly convex body form of Gracilenticrus indicates it is probably not fungivorous. Since distinctly erect vestiture is mostly known in predatory surface dwellers in Cleroidea [16], we speculate the habits of this new genus also predatory.

Conclusions
The Mesozoic taxon Gracilenticrus Yu, Kolibáč &Ślipiński shares many important characters with the extant lophocaterids to support its placement in Lophocateridae. Our discovery of this new genus and new species from the mid-Cretaceous amber of northern Myanmar reflect an already strong diversification of the family during the Cretaceous period.