The first queen-worker association for Cretaceous Formicidae: the winged caste of Haidomyrmex cerberus

Abstract Two queen ant specimens, one alate and one dealate, from mid-Cretaceous (Late Albian–Early Cenomanian) Burmese amber are herein reported as belonging Haidomyrmex cerberus Dlussky, 1996. This is the first discovery and documentation of an alate queen in Haidomyrmex. Compared with workers of Haidomyrmex cerberus, alate and dealate queens are larger in body size, have smaller compound eyes, a longer antennal scape, more complex mandibles, and a relatively large-sized metasoma. It is hypothesized that these differences are due to caste differences.


Introduction
Mandibles, as the main structures used for foraging, predation, food handling, defense and brood care (Hölldobler and Wilson 1990), are vital to the biology, taxonomy and evolutionary development of ants. For example, haidomyrmecine and zigrasimeciine ants with unique mandibles have been reported in mid-Cretaceous amber deposits from Myanmar (Dlussky 1996; Grimaldi 2012, 2013;Perrichot 2014;Perrichot et al. 2016Perrichot et al. , 2020Miao and Wang 2019;Cao et al. 2020a, b, c;Lattke and Melo 2020). To date, ten genera and sixteen species of haidomyrmecine ants from Cretaceous amber deposits from France, Canada and Myanmar have been described. Haidomyrmex, as the type genus of the extinct subfamily Haidomyrmecinae, has been frequently discussed in relation to the other genera. In 1996, Haidomyrmex cerberus Dlussky, 1996, with a peculiar cranio-mandibular morphology, was found in Burmese amber and described. The combination of its bizarre mandibles and head capsule suggested that this ant might have been a specialized predator (Dlussky 1996). However, parts of the antennae, legs and gaster were not preserved in the type specimen whereas some key characters, especially those of the head, were obscured due to the turbidity of the amber piece. Cao et al. (2020a) provided a more detailed description of this species based on two additional worker specimens, including some characters of the antennae, head, legs and gaster. Based on some key characters, such as antennal length, size of compound eyes, location of trigger hairs, and mandible morphology, Lattke and Melo (2020) provided a key for identifying species of Haidomyrmex. Unfortunately, until now there was no description of alate queens in Haidomyrmex. Barden and Grimaldi (2012) described the only previously-known dealate queen, for the species Haidomyrmex scimitarus Barden & Grimaldi. In this study, we report two queen ant specimens of Haidomyrmex cerberus: one dealate and one alate, which represents the first discovery of a winged caste in Haidomyrmex. Comparing their morphological characters with those of the known dealate queen and workers provides insights into caste differences in Haidomyrmex ants.

Material and methods
This study is based on two new amber specimens from the Hukawng Valley in the Kachin State of northern Myanmar, at the north end of Noije Bum at 26°15'N, 96°34'E, some 18 km south-west of the town of Tanai (Grimaldi et al. 2002;Cruickshank and Ko 2003). The deposit is dated to 98.79 ± 0.62 Mya based on radiometric uranium-lead dating (Shi et al. 2012). The recent finding of an ammonite embedded in amber and assignable to Puzosia (Bhimaites) supports a Late Albian-Early Cenomanian age of the amber (Yu et al. 2019). The newly-reported amber specimens are housed in the Key Lab of Insect Evolution and Environmental Changes, College of Life Sciences and Academy for Multidisciplinary Studies, Capital Normal University (CNUB), Beijing, China.
Specimens No. CNU-HYM-MA2015010 and No. CNU-HYM-MA2015011 are separately preserved in two yellow amber pieces with organic particles, tiny bubbles and dust covering the cuticle in places. Specimens were examined and photographed by using a Nikon SMZ 25 microscope equipped with a Nikon DS-Ri 2 digital camera. The line drawing and figure plates were prepared by using the Adobe Illustrator CC and Adobe Photoshop CC graphics software. Measurements were obtained using the measurement tool of the Nikon software. All measurements are provided in millimeters (mm). Measurements used in the descriptions, including their abbreviations, are detailed in Table 1. Diagnosis. Alate and dealate queens. Antenna with scape distinctly longer than pedicel and the two following flagellomeres combined, FII (second flagellomere) longer than each of the other flagellomeres. Labrum with two long setae curved upward. Mandibles long, internal surface of curved portion with a row of longitudinal serrations on the apical quarter; apical portion tapered to a blunt tip, external margin of apex each with a short erect and suberect seta. Maxillary palps distinctly elongate, formed of 6 segments; labial palps relatively short, formed of 4 segments. Propleuron well developed, with dorsal portion exposed and visible dorsally.

Taxonomy
Description of alate and dealate queens. Based on CNU-HYM-MA2015011, alate queen, with differential characters from CNU-HYM-MA2015010, dealate queen in square brackets. Apex of scape slightly broadened, its margin bearing short and erect setae; FI with a long and curved seta on median ventral surface. Clypeal process a small lobe moderately protruding between bases of antennae, with short peg-like denticles above and longer, dense, stiff   spine-like setae arranged in longitudinal rows on ventral half. Ventral surface of clypeus with one visible pair of long, fine trigger hairs [trigger hairs invisible]. Labrum with two long setae curved upward. Mandible long, scythe-shaped, internal surface of curved portion with 1-2 short setae near apex and a row of longitudinal serrations on apical quarter; apical portion tapered to a blunt tip, apex reaching clypeal lobe and each with one short, erect and suberect seta; ventral corner between basal and curved portion bearing a triangular blade, apparently symmetrical and with a single tooth; ventral margin of corner with sparsely fine setae from base to apex, becoming gradually shorter and thinner [with dense fine setae from base to one third of external surface of curved portion]. Maxillary palp exposed length 0.53, with 4 visible segments [length 0.86, with 6 obvious segments]. Labial palp is invisible [length 0.30, with 4 segments].

Conclusion
Most workers and queens of modern ants are known and the castes can be differentiated by body size and by minor aspects of the mandibular morphology (Hölldobler and Wilson 1990). It is highly probable that all the differences between the two queens described herein and the workers of H. cerberus revised by Cao et al. (2020a) are simply due to the difference in caste. The two queens can be differentiated from workers of H. cerberus by 1) the larger body of 6.3-7.8 mm (vs. 4.5-5.0 mm body lengths for workers); 2) the obviously longer scape, distinctly longer than the pedicel and two following flagellomeres combined (vs. scape as long as the pedicel and two following flagellomeres combined) and ca. 6-9 times as long as pedicel (vs. ca. 4 times as long as pedicel); 3) the more complex shape of the mandibles, with inner surface with a row of longitudinal serrations near the apex, and triangular blade clearly longer and sharper; 4) metasoma relatively large in proportion to total body size (ca. 0.36 times as long as body vs. ca. 0.32 times as long as body), because of flight muscles. Queens of modern species usually have larger eyes relative to head size compared to workers. Surprisingly, the queens of H. cerberus have smaller compound eyes (diameters of 0.24 mm and 0.28 mm) than those of workers (0.30 mm). Documentation of these differences con-tributes to a better understanding of the Cretaceous Formicidae and shows differences among castes of Haidomyrmex cerberus for the first time.