Gerontoformica gracilis, (BARDEN & GRIMALDI, 2014)

Boudinot, Brendon E., Richter, Adrian, Katzke, Julian, Chaul, Júlio C. M., Keller, Roberto A., Economo, Evan P., Beutel, Rolf Georg & Yamamoto, Shûhei, 2022, Evidence for the evolution of eusociality in stem ants and a systematic revision of † Gerontoformica (Hymenoptera: Formicidae), Zoological Journal of the Linnean Society 195, pp. 1355-1389 : 1369-1377

† GERONTOFORMICA GRACILIS ( BARDEN & GRIMALDI, 2014)

( FIGS 1A, B , 2A, B, D, E, G, H, J, K , 8 , 9 , 10 , 11 (1’-2), 12(7-1); SUPPORTING INFORMATION, FIG. S3 )

† Sphecomyrmodes gracilis Barden & Grimaldi, 2014: 4–7 , figs 2, 10B, 11C, D (wingless female, Kachin amber, JZC-Bu324A, AMNH).

Combination in † Gerontoformica: Barden & Grimaldi (2016) : 518, suppl. info. p. 16.

Diagnosis (wingless female)

Similarly identifiable as † G. sternorhabda to the genus † Gerontoformica (I–III above), including absence of the anteromedian lobate clypeal process [Note 1]. For the diagnosis and redescription, see Figures 2 , 8 and 10 primarily.

I. Among † Gerontoformica , with the following unique character: (1) proximal labial palpomere with a distinct, apicomedially situated lobate process ( Fig. 7A, B ) [Note 2];

II. Within † Gerontoformica , identifiable as a member of the gracilis species group: (2)

mesoscutum without distinct, raised transverse carina separating mesoscutal and mesoscutellar regions ( Fig. 10A ); (3) tergum of petiolar node anteroposteriorly longer than dorsoventrally tall (high); and (4) abdominal segment IV without cinctus dividing the tergum and sternum into pre- and postsclerites;

III. Within the gracilis species group, identified by the following: (5) petiole bun-like, with anteroposteriorly long node; vs. subsquamiform, with anteroposteriorly narrow node († G. cretacica and † G. occidentalis ); (6) meso- and metanota bulging, with their dorsal silhouette bihumped; vs. meso- and metanota not bulging, with their dorsal silhouette forming an almost straight line († G.robusta );(7)transverse dorsal sulci of mesosoma broad, separating the meso- and metanota and the metanotum and propodeum by at least one tarsomere width; vs. these sulci not as broad, with the meso- and metanota and the metanotum and propodeum separated by less than one tarsomeral width († G. spiralis , † G. subcuspis ) [Note 1]; and (8) propodeal spiracle covered anteriorly by an anterior flange which is directed posterolaterally; vs. spiracle not flanged († G. spiralis , † G. subcuspis ; state uncertain for † G. robusta ) [Note 3].

Notes on the diagnosis

Note 1: † Gerontoformica gracilis is quite similar overall to † G. spiralis and † G. subcuspis . The primary structural distinction is the width of the dorsal transverse sulci that divide the mesonotal and metanotal regions, and the metanotal region and the propodeum, as well as development of an anterior flange around the propodeal spiracles. The character used by Barden & Grimaldi (2014) to distinguish † G. spiralis and † G. gracilis was the distance between the pro- and mesocoxae (their couplet 9); this is certainly a matter of preservation, as the prothorax of the holotype of † G. gracilis is elevated relative to the mesothorax, and the coxae are promoted anteriorly. Such pronotal elevation is possible in ant species with a mobile promesonotal articulation. The defining feature of † G. subcuspis provided by Barden & Grimaldi (2014) is the form of the subpetiolar process, which has an almost vertically oriented anterior margin in profile view. The process of † G. gracilis is more evenly rounded from posterior to anterior, while that of † G. spiralis is not visible. These distinctions should be re-evaluated in future study. See also Note 3 on the synopsis of † Gerontoformica classification above.

Note 2: We do not know the distribution of the process of the proximal labial palpomere across † Gerontoformica , with the exception of its absence in † G. sternorhabda . Despite this, we note the development of these processes as they are unique to our knowledge of both extant and extinct species. Because of the difficulty of evaluating proximal palpomeres for ants in general, and especially for fossil ants, we strongly recommend the application of µ-CT methods to determine the phylogenetic extent of this obvious apomorphy. Note that it is possible that the holotype lacks this condition, as we discovered this character after our chance to directly examine the type specimen.

Note 3: The anterior flange or hood of the propodeal spiracle is present in most † Gerontoformica examined, with the exception of † G. spiralis and † G. subcuspis . The flange could not be evaluated for † G. magna or † G. robusta .

Measurements and indices

Adult, specimen C-32: HWed = 0.71; HWev = 0.78; EWl = 0.17; HD = 0.62; ML = 1.49; PnLi = 0.59; PnWa = 0.18; MnL = 0.35; AIIILm = 0.52; AIIILl = 0.65; HPI = 0.99; HSI = 0.47; AIIILI = 0.80.

Pupa, specimen C-31: HWed = 0.72; HWev = 0.71; EWl = 0.18; HD = 0.62; ML = 1.62; PnLi = 0.60; PnWa = 0.25; MnL = 0.34; AIIILm = 0.62; AIIILl = 0.73; HPI = 0.86; HSI = 0.44; AIIILI = 0.85.

Redescription: adult

Head: The head is narrow in facial view, i.e. it is lateromedially narrower than anteroposteriorly long as measured from the anterior clypeal margin to the apparent posterior head margin ( Fig. 2K ); in posterior and lateral view, the head is dorsoventrally broad, with the vertexal region dome-like; standing setae are most conspicuous on the clypeus. The compound eyes are situated in the posterior third of the head; they bulge laterally, breaking the silhouette of the lateral head margins in facial view; their height mesonotal carina; mspct, mesopectus; mtbt, metabasitarsus; mtcx, metacoxa; mtfm, metafemur; mtnt, metanotum; mtpfm, metaprefemur; mtplglvf, ventral flange of the metapleural gland; mtptc, metapretarsal claw; mttbsa, anterior spur of metatibia; mttbsp, posterior spur of metatibia; mttr, metatrochanter; pd, pedicel; pl, labial palp; pm, maxillary palp; pbt, probasitarsus; pnt, pronotum; ppd, propodeum; ppdsf, anterior flange of propodeal spiracle; pptc, propretarsal claw; pt, petiole; ptn, petiolar node; pts, petiolar sternum; ptsp, subpetiolar process; sc, scape; tgl, laterotergite; to, antennal torulus. above the surrounding surfaces of the cranium is comparatively high; their ommatidia count appears similar to that of † G. sternorhabda ; they are apparently glabrous, i.e. lacking interstitial setation. The three ocelli are completely developed. The frontal carinae diverge posterolaterally toward but not reaching the compound eyes; they are circular in form, i.e. curving evenly from their anterior termini to their posterior termini which are directed anterolaterally, rather than posterolaterally; their anterior termini are distant from the epistomal line; the minimum distance between the frontal carinae is about 0.26× maximum head width as measured in full face view. The antennal scrobes are anteroposteriorly short and encircled by the frontal carina. The antennal toruli are distant from the posterior clypeal margin; they are in the form of a low, more-or-less even ring. The antennae are 12-merous. The scapes are somewhat flattened and curved; they are about four times as long as their maximum width; their length is somewhat more than half the width of the head, and somewhat less than half the length of the head; they lack standing setae along their shafts. The pedicels are slightly longer than twice their width; they are about one-third the length of the scapes, and about half the length of the third antennomere; they apparently lack standing setae. The flagellae are longer than the mesosoma and are simple, i.e. not thickening distally; they bear a range of standing and appressed setae; flagellomeres I are the longest, being somewhat more than four times as long as wide and about three fourths the length of the scape; flagellomeres II–IX are all longer than the pedicel; flagellomeres X are longer than each pair of flagellomeres from II to IX. The clypeus is about three times as wide lateromedially as long anteroposteriorly, with the length measured from the midpoints of the anterior and posterior clypeal margins and the width measured between the lateralmost points of the clypeus. The lateroclypeal areas are formed as lateral lobes. The medioclypeal area is anteriorly convex; its length at the midline of the head is about 0.21× head length also at midline, as measured in full-face view; it bears an array of standing (rather than appressed) setae on its disc and is margined anteriorly by chaetae. The mandibles are simple and apically bidentate. The maxillary palps are 6-merous ( Figs 2B, H , 7A–D ) [Note 1]; they are elongate, being almost as long as the head and longer than the scapes and mandibles; the proximal palpomeres are short compared to the others; the second palpomeres are dorsoventrally flattened and lobate apicomedially; the third through sixth palpomeres are long, thin, and cylindrical. The labial palps are 4-merous ( Figs 2B, H , 7A–D ) [Note 1]; they are short, being less than half the length of the maxillary palps, and with their individual lengths shorter than each of the maxillary palpomeres with the exception of the proximal maxillary ones; the proximal labial palpomere is narrow proximally and bears a distinct lobate process medially at about its apical third, with this process being about as long as wide; the second and third palpomeres are thickened medially; the fourth palpomeres are relatively more cylindrical.

Mesosoma: The pronotum bears an anteromedian neck process, and lateral and posteromedian flanges; these flanges are not flared; the muscular node or ‘disc’ of the pronotum is hemispherical as observed in lateral view and almost elliptical in dorsal view, being distinctly longer than tall in lateral (profile) view, thus appearing narrow; setation was not observed on the pronotum [Note 2]. The pronotal lobes are well developed ( Fig. 6E ). The mesonotum is not divided into an anterior mesoscutal area and a posterior mesoscutellar area, i.e. the transverse mesonotal carina is not developed; the notum is convex in lateral view and is almost flattened along most of its length. The mesopectus is not clearly divided into dorsal and ventral areas; its dorsoventral height is almost 1.5× that of its anteroposterior length. The transverse mesonotal sulcus is anteroposteriorly long/broad. The metanotum is developed as a distinct and almost evenly convex bulge. The transverse metanotopropodeal sulcus is anteroposteriorly broad and continues ventrally toward the base of the mesocoxa, completely separating the lateral metapectal area from the lateral mesopectal area. The metapleural gland orifice is small and not remarkably hairy ( Fig. 6F ); it does not have a distinct bulla; it is margined dorsally and ventrally by flanges, including the ventral metapleural gland flange. The propodeum is rounded, with the dorsal and posterior margins curving broadly into one another in lateral view; its posterior surface is convex; it does not, apparently, bear standing setae. The propodeal spiracles are situated distant from the metanotum and below the dorsal propodeal margin as seen in lateral view, but they are located in the anterodorsal fourth of the sclerite. The propodeal lobes are apparently not developed.

Legs: The legs are developed as expected for the Formicidae , with some notable characters and states. With the exception of the tibial apex and tarsi, they appear almost entirely glabrous. The state of the apical protibial foramina is uncertain. The mesoprefemora and metaprefemora are welldeveloped and are broader ventrally than dorsally. The protibia bears and anterior brush of dense suberect setae in their apical third, near the calcar. Each of the mesotibia and metatibia bear a pair of apicoventral spurs; the anterior tibial spurs are barbirulate; the posterior tibial spurs are simple. The calcar is apparently bifid apically, with one point being the apex of the elongate velum and the other point being a small array of hairs; two stout setae are developed posterior to the calcar. The plantar lobes of the tarsi are well developed, the ventral setation is sparse, and the apical row of chaetae is thinner. The fourth tarsomeres are only weakly notched distally, thus appearing cylindrical in dorsal view. The pretarsal claw teeth are well developed and located just past the midlength of their respective claws. The aroliae are well developed and comparatively large ( Fig. 8D ); they are nearly as long as the pretarsal claws.

Metasoma: The petiole is nodiform and lacks tergosternal fusion between its postsclerites. The petiolar tergum is anteroposteriorly longer than dorsoventrally tall; it is asymmetrically convex, being somewhat longer anteriorly than posteriorly. The developmental state of the laterotergites is uncertain. The petiolar sternum is anteriorly flat; its main portion is at least twice as long as tall; it is narrowly convex in cross-section at its midpoint; it is weakly produced anteroventrally as a low, lobate subpetiolar process, which is shorter dorsoventrally than wide anteroposteriorly; posteriorly, the sternum is not distinctly concave or notched. The helcium is narrow relative to the third abdominal postsclerites; the helcial tergite conceals the helcial sternite in lateral view. The abdominal posttergite III is not constricted posteriorly and is not fused with the third poststernite; it is not necked or shouldered anteriorly, as the tergum evenly curves from its anterior base to posterior margin in lateral view. The abdominal tergosternal margin III is weakly curved, without distinct ‘shouldering’ as observed in various Formicinae and Dolichoderinae. The abdominal poststernite III is not constricted posteriorly, but is weakly angled lateromedially, and bears the prora anteroventrally. The prora is lip-like in lateral view, being anteroposteriorly short and moreor-less transverse in ventral view. The abdominal segments IV, V, and VI are not divided into pre- and postsclerites by a cinctus; they are homonomous in form, i.e. highly similar in shape, size and other qualities of appearance. The seventh abdominal tergum is somewhat dome-like. The seventh abdominal sternum is lateromedially cupped and narrowed distally. The sting is long and narrow. The third valvulae are digitate in form and highly exserted as preserved.

Preservation: The specimen CASENT0741232 is exceptionally well preserved internally, particularly the head and mesosoma ( Fig. 9 ). The metasoma is, however, less well preserved, and has some apparent fungal growth or decay bubbling emanating from between the third and fourth abdominal segments. There are several fractures around the specimen, including on the dorsal surface of the head, the ventral right side of the head, across the left side of the mesosoma, and across the petiole and the left side of the third and fourth abdominal segments. The right side of the face, opposite from where the scape is held, is indented, thus appearing to have a longitudinal scrobe ( Fig. 10 ); this is definitely an artefact, as it is not symmetrically present on the left side of the face where the scape is preserved in a position that is distant from the head capsule. Similarly, the mesosoma is indented where the legs are in close proximity ( Fig. 10 ). The left metatrochanter appears distorted in shape.

Notes on description

Note 1: The original description recognized 4-merous maxillary palps and did not state a labial palpomere count. A 6, 4 palp formula (sensu Bolton, 1994, 2003) was determined here based on direct examination of the holotype, and from our microphotographs and digital renders. As noted in the diagnosis, the process of the proximal labial palpomere is unique among † Gerontoformica , given our current knowledge.

Note 2: We are not certain whether † G. gracilis is largely glabrous or whether it has appressed pubescence in various places. At the least we expect pubescence on inter-sclerite contact surfaces.

Description: pupa

The pupa ( Figs 2A, D, G, J , 7 , 10 ) is encased in a cocoon with a black meconium at the caudal end ( Fig. 1A ). Most structures of species-level identificatory value are incompletely developed, including the frontal carinae, perioral sclerites, mesosomal dorsum and anterior metasoma. The preservation of the specimen is fine externally but is poor internally, with the body cavity filled with a single, solid mass, despite apparent distinctions as seen from light microscopy. In overall appearance, the specimen is relatively bubbly or puffy looking, and has the propodeum crushed and incompletely differentiated from the petiole. Those metasomal segments which are posterior to the petiole are bulging, thus they appear slightly constricted as with a cinctus, but cincti are apparently absent. The metanotal and propodeal spiracles are visible externally, but those of the metasoma are not.

Features of note include the following: The head is longer anteroposteriorly than broad lateromedially; the mandibles are contacting one another apically; the maxillolabial complex is exserted, with the palps and glossa clearly visible in ventral view; the maxillary palps are 6-merous; the labial palps are 4-merous; the antennae are directed caudally and reach the posterior margin of the third abdominal segment; the pronotum is longer than tall in lateral view; and the mesonotum lacks a transverse ridge, thus is not divided into anterior mesoscutal and posterior mesoscutellar regions.

The pupa differs from the synincluded adults of both species as follows: The antennae appear wideset; the clypeus is anteroposteriorly longer, apparently with an additional band of cuticle along the anterior m a r g i n; t h e m a n d i b l e s a r e o b l i q u e l y o r i e n t e d relative to head length, converging anterad (vs. perpendicular to the long axis of the head at closure); and the labrum is apically notched and with distinct paramedian lobes.

Remarks on the pupa

Because little comparative work on pupal morphology has been done in Formicidae , it is basically unknown what the polarity of the ‘general features of note’ is within the family. Further, because there are no developmental series of anatomy available for pupal transformation, we cannot be certain of the stage that this specimen was preserved. The conditions listed above which differ between the pupa and adults are especially interesting, as they suggest that there are intermediate stages in the structural rearrangement of the body. For example, the wideset toruli and exceptionally long clypeus are hard to explain without an atlas of developmental transformation. We note the apically bilobate labrum, in particular, as the labra of the adults are apically rounded. At present we are unable to explain the labral difference, as there are no works that model the developmental transformation from immature to imago in ants; such studies are much needed (for further detail, see: Boudinot et al., 2021b).

Figures

Figure 1. Overview of the Kachin amber piece and its syninclusions.A, the pupa of †G. gracilis (CASENT01741231). B, the adult of †G. gracilis (CASENT0741232). C, the holotype of †G. sternorhabda sp. nov. (CASENT0741233). D, the paratype of †G. sternorhabda sp. nov. (CASENT0741234). E, the entire amber piece (AMNH SY-23).

Figure 2. Volume renders of the pupa and two of the adult specimens. The black arrows indicate the subpetiolar process, while the white arrows indicate the prora. A–C, lateral view. D–F, dorsal view. G–I, ventral view. J–L, facial view. A, D, G, J. the pupa of †G. gracilis. B, E, H, K, the adult of †G. gracilis. C, F, I, L, the holotype of †G. sternorhabda sp. nov.. Abbreviations: AIII–VII, third through seventh abdominal segments; AIIIas, anterior surface of third abdominal segment; AIIIps, posterior surface of third abdominal segment; ce, compound eye; cl, clypeus; fc, frontal carina; lbr, labrum; md, mandible; msn, mesonotum; mspl, lower mesopectal region; mspu, upper mesopectal region; mtn, metanotum; oc, ocellus; pd, pedicel; pnt, pronotum; ppd, propodeum; pst, prosternum; pt, petiole; sc, scape.

Figure 3. Summary of the evidence for eusocial evolution in stem groups. A, overview of the phylogenetic relationships of the total clade Formicidae, with key biological traits mapped. F+, winged females; f-, wingless females; D, developmental simplification of the mesosoma; and B*, brood care. Solid squares, trait confirmed as present; empty squares, trait confirmed as absent; half-filled squares, trait confirmed as variable; question marks, state uncertain; black square with asterisk, new evidence provided in the present study. B, exemplars of females with the full and complex complement of flight sclerites, namely the mesoscutum (green), mesoscutellum (blue), and metanotum (magenta). C, exemplars of wingless †Zigrasimeciinae demonstrating independent convergence on the extremely simplified mesosomal form of various crown Formicidae, illustrated in this case by Discothyrea (Proceratiinae). D, exemplars of theAntennoclypeata, showing a similar degree of sclerite reduction between †Brownimecia and crown Formicidae. Notes: The topology in 1A is summarized from Johnson et al. (2013), Barden & Grimaldi (2016)and Boudinot et al.(2020a). Images for rows 1B, C were downloaded from AntWeb(2021); taxon names, imagers and unique specimen identifiers are listed from left to right, top to bottom are as follows: †Zigrasimecia tonsora Barden & Grimaldi, 2013 (P. Barden, ANTWEB1008098); †Dhagnathos autokrator Perrichot et al., 2020 (V.Perrichot, FANTWEB00022); †Linguamyrmex rhinocerus Miao & Wang, 2019 (V. Perrichot, FANTWEB00016); †Protozigrasimecia chauli Cao et al., 2020c (H. Cao, FANTWEB00051); †Zigrasimecia ufv-01 (J. Chaul, ANTWEB10141055); Discothyrea bobi Chaul, 2020 (J. Chaul, UFV-LABECOL-000032); †Brachyponera croceicornis (Emery, 1900) (F. Esteves, CASENT0916594); Brachyponera croceicornis (Emery, 1900) (A. Nobile, CASENT0172432); †Brownimecia clavata Grimaldi et al., 1997 (V. Perrichot, AMNH-NJ667).

Figure 6. Detailsof thepronota andmetapleural glandsof †Gerontoformica.A,B,fluorescent lightmicroscopy;C–G,standard photomicroscopy. A, B, †G. sternorhabda sp. nov. paratype (UFV-LABECOL-009656). C, †G. pilosa (ANTWEB1038931). D, †G. sternorhabda sp. nov. non-type (JWJ-BU21). E, F, †G. gracilis holotype (JZC-Bu324A). G, †G. near or conspecific with gracilis (ANTWEB1032649). Abbreviations: msnttc, transverse carina of mesonotum; mtplglb, metapleural gland bulla; mtplgldf, metapleural gland dorsal flange; mtplglvf, metapleural gland ventral flange; mtvlc, ventrolateral carina of metathorax; mtntsp, metanotal spiracle; mtnt, metanotum; pntl, pronotal lobe; pntfl, lateral pronotal flange; pntfm, medial pronotal flange; ppdsf, anterior flange of propodeal spiracle; ppl, propleuron; pt, petiole.

Figure 7. Maxillary and labial palps of †G.gracilis and †G.sternorhabda sp. nov.. Small black stars indicate each palpomere on the right-hand side of the body.A, B, †G.gracilis adult, CASENT0741232, in anterior dorsolateral oblique view (A) and anterior view (B).C, D, †G.gracilis pupa, CASENT0741231, in anterior view (C) and anterior dorsolateral view (D).E, F, †G.sternorhabda sp. nov. holotype, CASENT0741233, and paratype, CASENT0741234, in anteroventral oblique view. Abbreviations: pl, labial palp; plp, process of the proximal labial palpomere; pm, maxillary palp; pm?, possible maxillary palpomere.

Figure 8. Photomicrographs of †G. gracilis showing setation and certain key features. Specimen CASENT0741232. A, body in ventrolateral anterior oblique view. B, body in dorsolateral posterior oblique view. C, detail of head and prothorax in ventrolateral anterior oblique view. D, detail of mid and hind legs in ventrolateral anterior oblique view. Abbreviations: AII–VII, abdominal segments II–VII; AVsp, spiracle of abdominal segment V; ar, arolium; ca, calcar; cav, velum of calcar; ce, compound eye; fc, frontal carina; mc, cranial condyle of mandible; md, mandible; mspfm, prefemur of mesothoracic leg; msptc, tooth of mesothoracic leg pretarsal claw; mstbspa, anterior tibial spur of mesothoracic leg; mstbspp, posterior tibial spur of mesothoracic leg; mtpfm, prefemur of metathoracic leg; mtplglvf, metapleural gland ventral flange; pd, pedicel; pdcs, prodisticoxal suture; pl, labial palp; plo, plantar lobe; pm, maxillary palp; pnt, pronotum; ppd, propodeum; ppdsp, propodeal spiracle; ppl, propleuron; pr, prora; ptsp, spiracle of the petiole; sc, scape.

Figure 9. Exceptional soft tissue preservation. The adult specimen of †G. gracilis displays exceptional preservation of soft tissues, including identifiable neuropils (A), countable glomeruli of the antennal lobe (A’), the digestive tract, glands, and muscle (B), down to the scale of individual muscular cross-striations (B’).

Figure 10. Features hidden by appendages, including artefacts caused by close proximity of limbs. †Gerontoformica gracilis: A, B, D, adult, CASENT0741232; C, pupa (CASENT0741231). A, C, mesosoma in lateral view with the legs distal to the coxae digitally removed, with the exception of the fore leg of (C), which is not cropped from the render. B, D, head in facial view with the scapes digitally rendered (B) and removed (D). Abbreviations: mspa, mesopectal artefact; sca, scapal artefact.

Figure 11. Couplet 1: mesonotum with (1-1) or without (1’-1) transverse ridge; abdominal segment IV with (1-2) or without (1’-2) cinctus; prora large (1-3) or small (1’-3). (1-1) †G. ufv-05, ANTWEB103848 (J. Chaul, AntWeb), mesosoma in profile view. (1’-1, 1’-3) †G. indet., JWJ-Bu19 (V. Perrichot, AntWeb), mesosoma in profile view. (1-2) †G. sternorhabda sp. nov. paratype, UFV-LABECOL-009656, metasoma in ventrolateral view. (1’-2) †G. gracilis, CASENT0741232, metasoma in lateral view. (1-3) †G. pilosa holotype, JZC-Bu225 (P. Barden, AntWeb), anterior metasoma in profile view.