Ants comprise one lineage of the triumvirate of eusocial insects and experienced their early diversification within the Cretaceous []. Their ecological success is generally attributed to their remarkable social behavior. Not all ants cooperate in social hunting, however, and some of the most effective predatory ants are solitary hunters with powerful trap jaws []. Recent evolutionary studies predict that the early branching lineages of extant ants formed small colonies of ground-dwelling, solitary specialist predators [], while some Cretaceous fossils suggest group recruitment and socially advanced behavior among stem-group ants []. We describe a trap-jaw ant from 99 million-year-old Burmese amber with head structures that presumably functioned as a highly specialized trap for large-bodied prey. These are a cephalic horn resulting from an extreme modification of the clypeus hitherto unseen among living and extinct ants and scythe-like mandibles that extend high above the head, both demonstrating the presence of exaggerated morphogenesis early among stem-group ants. The new ant belongs to the Haidomyrmecini, possibly the earliest ant lineage [], and together these trap-jaw ants suggest that at least some of the earliest Formicidae were solitary specialist predators. With their peculiar adaptations, haidomyrmecines had a refined ecology shortly following the advent of ants.

Abbreviations are as follows: amd, apical portion of mandibles; bmd, basal portion of mandibles; btmd, basal tooth of mandible; ce, compound eye; cls, clypeal setae; es, epistomal sulcus; ho, horn; mp, maxillary palps; sc, scape; sl, setose lobe; th, trigger hair; to, torulus. See also Figures S1 and S2 and Table S1

Diagnosis. Differs from all other extinct and living ants by the presence, in workers, of a long cephalic horn arising from between the antennal insertions and curved forward and by very long, scythe-like mandibles, their tips reaching above head near to the horn’s apex. The horn is spatulate apically, and its undersurface is densely setose, with a semi-circular brush of peg-like spicules along edges. Two pairs of long trigger hairs are each flanking the apical portion of mandibles. The combination of distinct ocelli and subpetiolar process also serves to distinguish the genus from other haidomyrmecines.

The vast majority of Cretaceous ants belong to stem-group Formicidae and comprise workers and reproductives of largely generalized morphologies [], and it is difficult to draw clear conclusions about their ecology, although recent discoveries from Cretaceous Burmese amber suggest relatively advanced social levels []. Remarkable exceptions to this pattern of generalized morphologies are ants with bizarre mouthparts such as Zigrasimecia, Camelomecia, and five species composing the Haidomyrmecini in which both female castes (workers and reproductives; males are unknown) have modified heads and blade-like mandibles that uniquely move in a vertical rather than horizontal plane []. Haidomyrmecines have puzzled evolutionary biologists as to their specific ecology, the mandibles apparently acting as traps triggered by sensory hairs in a way distinct from that of modern trap-jaw ants []. Nonetheless, even within haidomyrmecines, there has been relatively little morphological disparity, and their ecology as solitary or social hunters, and as dietary specialists or generalists, remains obscure. Here, we report four individual fossils of a new haidomyrmecine ant species with extraordinary head structures that presumably function as a highly specialized trap for large-bodied prey. The specimens were found in four different pieces of amber from the Hukawng Valley in northern Myanmar, dated radiometrically at 99 mega-annum [].

Discussion

10 Larabee F.J.

Suarez A.V. The evolution and functional morphology of trap-jaw ants (Hymenoptera: Formicidae). 21 Baroni Urbani C. Anochetus corayi n. sp., the first fossil Odontomachiti ant (Amber Collection Stuttgart: Hymenoptera, Formicidae. II: Odontomachiti). 22 de Andrade M.L. Fossil Odontomachini ants from the Dominican Republic (Amber Collection Stuttgart: Hymenoptera, Formicidae. VII: Odontomachini). 23 Wappler T.

Dlussky G.M.

Engel M.S.

Prokop J.

Knor S. A new trap-jaw ant species of the genus Odontomachus (Hymenoptera: Formicidae: Ponerinae) from the Early Miocene (Burdigalian) of the Czech Republic. 24 Johnson B.R.

Borowiec M.L.

Chiu J.C.

Lee E.K.

Atallah J.

Ward P.S. Phylogenomics resolves evolutionary relationships among ants, bees, and wasps. 9 Barden P.

Grimaldi D.A. Adaptive radiation in socially advanced stem-group ants from the Cretaceous. 14 Barden P.

Grimaldi D. A new genus of highly specialized ants in Cretaceous Burmese amber (Hymenoptera: Formicidae). 15 Perrichot V. A new species of the Cretaceous ant Zigrasimecia based on the worker caste reveals placement of the genus in the Sphecomyrminae (Hymenoptera: Formicidae). Figure 2 The Ant Tree of Life and Parallelism among Trap-Jaw Ants Show full caption 5 Moreau C.S.

Bell C.D. Testing the museum versus cradle tropical biological diversity hypothesis: phylogeny, diversification, and ancestral biogeographic range evolution of the ants. 9 Barden P.

Grimaldi D.A. Adaptive radiation in socially advanced stem-group ants from the Cretaceous. Trap jaws have evolved independently at least four times in ants, occurring in 11 genera from four subfamilies (indicated in gray on topology; circled numbers refer to earliest trap-jaw fossils known: 1, Haidomyrmodes mammuthus; 2, various Odontomachus and Anochetus species; 3, Acanthognathus poinari). Thick lines denote the temporal range known for each subfamily. Relationships and divergence times among lineages are based on previous molecular and morphological hypotheses []. Ceratomyrmex has distinctive features of the haidomyrmecines such as the concave face and the scythe-like mandibles moving in a vertical plane, their apical portion flanked by two pairs of long trigger hairs inserted on the clypeus. The most striking feature of Ceratomyrmex is its unique cranio-mandibular system—the horn and trigger hairs evidently operate as a sensory complex to judge the distance of a target before eliciting closure of the oversized mandibles, presumably to subdue, puncture, and crush prey or opponents, and alternatively for contact with nestmates without eliciting a strike. Although differently constructed and in no way representing a common evolutionary origin, such trap jaws and their associated trigger hairs are known elsewhere among foragers of three extant ant subfamilies [] ( Figure 2 ), and such mandibular specializations across those lineages are known in the Cenozoic []. It is not surprising that predatory behavior should be present among stem-group ants, particularly as related aculeate families are virtually all predatory to some degree or other []. The other non-haidomyrmecine stem-group ants are likely to have been mostly generalist predators, except maybe Zigrasimecia and Camelomecia []. It is remarkable that among the haidomyrmecines there was an early origin of specialized, trap jaws and that this should be taken to such an exaggerated extreme in Ceratomyrmex. The previously dubbed “clypeal setose lobe” presumably functioned as a stabilizing structure when pressure was applied by the mandibles that braced the prey against the face, offering friction to minimize movement that might cause the victim to be dropped.

25 Boucot A.J.

Poinar Jr., G.O. Fossil Behavior Compendium. Spine-like cuticular expansions are frequent in ants, present in genera of various subfamilies, but are not linked to hunting strategies. These expansions can form short paired spines on the head (e.g., Acromyrmex), paired lateral spines on the pronotum or propodeum (e.g., Polyrhachis), or more rarely a single median spine on the propodeum or petiole (e.g., Acanthoponera). A mediocephalic horn acting as a sensory appendage is a novel organ hitherto never seen among living and fossil ants. This projection is longer than the head and projects high above and forward, with dense long setae on its undersurface and facing the elongate mandibles that reach nearly to its spatulate apex. Together these structures define, along with the surface of the face, a broad cavity in which large prey might be held. Such structures would also permit, with a more gentle touch, the movement of larvae and pupae within the nest. Such behaviors are well known among extant ant lineages and have even been observed in Cenozoic amber inclusions of extant genera [].

13 Engel M.S.

Grimaldi D.A. Primitive new ants in Cretaceous amber from Myanmar, New Jersey, and Canada (Hymenoptera, Formicidae). 16 Dlussky G.M. Ants (Hymenoptera: Formicidae) from Burmese amber. 18 Barden P.

Grimaldi D.A. Rediscovery of the bizarre Cretaceous ant Haidomyrmex Dlussky (Hymenoptera: Formicidae), with two new species. 19 McKellar R.C.

Glasier J.

Engel M.S. A new trap-jawed ant (Hymenoptera: Formicidae: Haidomyrmecini) from Canadian Late Cretaceous amber. 26 Bolton B. Identification Guide to the Ant Genera of the World. 26 Bolton B. Identification Guide to the Ant Genera of the World. Figure 3 Homologies in the Clypeo-Mandibular Complex of Selected Stem-Group Ants Show full caption (A–D) The clypeus varies from transverse (A and B) to longitudinal (C and D), its anterior margin (a-cpm) from convex (A) to concave (B–D). The arrangement of clypeal spicules varies from one row along a-cpm (A and B) to a brushy lobe along posterior clypeal margin (C) or apically on a protruding horn (D). The mandibles vary from short, not elbowed (A) to short elbowed (B) or elongate elbowed (C and D) and, when closed, with no gap between apical portion and a-cpm (A), or with large (B and C) to huge (D) gap. Genera omitted: Sphecomyrma, similar to Gerontoformica except clypeal spicules absent; Haidomyrmodes and Haidoterminus, similar to Haidomyrmex. See also Figure S3 The setose lobe unique to haidomyrmecines, situated far from the anterior margin of head and flanking the antennal insertions in Haidomyrmex, Haidomyrmodes, and Haidoterminus, was considered previously as a modification of the clypeus []. This unique conformation was questionable since, in all other ants, the anterior clypeal margin is always contiguous with the oral cavity []. The epistomal sulcus, which marks the lateral and posterior clypeal outlines, has not been clear in haidomyrmecines studied so far, but the setose lobe appeared to be separated from the anterior edge of head and following the oral cavity, suggesting that it is not the clypeus. Specimens of Ceratomyrmex as well as new Haidomyrmex specimens from Burmese amber have the face sufficiently preserved to ascertain the course of the epistomal sulcus ( Figures 1 B and S3 A–S3C). The clypeus appears as a pair of lateral sclerites on each side of an elevated median portion extending longitudinally from above the oral cavity to the ventral base of the prominent, pyramidal frontal triangle (a structure immediately posterior to the clypeus, inserted between antennal sockets, but generally not prominent nor obvious []). The elevated median portion of the clypeus consists, in Haidomyrmex, of a mushroom-shaped shelf anteriorly with a narrow triangular stem and posteriorly with a hemispheric brushy lobe, while in Ceratomyrmex, it consists of a single longitudinal carina posteriorly projecting into the horn, with the brushy lobe moved apically on the horn ( Figures 3 C and 3D ). It is unclear whether the frontal lobe is fused with the dorsal base of the horn or is just not as prominent as in other haidomyrmecines. The trigger hairs are present in a place homologous to that of other haidomyrmecines, slightly below the antennal sockets on the elevated median clypeal portion, and thereby supporting the homology of the entire horn of Ceratomyrmex with the setose pad of other Haidomyrmecini. While the trigger hairs are assuredly sensory structures that would make contact with a prey prior to closure of the mandibles, or with a nestmate (without a strike), the clypeal pad likely served a stabilizing function, although it certainly also had a sensory purpose. Its shorter form in other haidomyrmecines would have excluded its ability to receive any tactile information from prey prior to ensnarement. It could have provided information on pressure when prey was appressed against the head. In Ceratomyrmex, the typical function of the clypeal pad must have been further elaborated, as the setae are more elongate and the structure itself extends well in front of the ant, suggesting specialization on some large-bodied prey for which a greater grasp was required.

10 Larabee F.J.

Suarez A.V. The evolution and functional morphology of trap-jaw ants (Hymenoptera: Formicidae). 27 Larabee F.J.

Suarez A.V. Mandible-powered escape jumps in trap-jaw ants increase survival rates during predator-prey encounters. Trap-jaw ants are typically highly predatory and dietary generalists, although some species specialize on particular arthropods, and a few even harvest seeds []. The extreme morphogenesis observed in Ceratomyrmex implies a unique specialization for predation among this early ant lineage, prior to anything similar among the Formicidae. Indeed, the arrangement of the mouthparts and clypeal structures would have made it challenging for Ceratomyrmex to effectively capture small arthropod prey as they would have had a greater chance of escape before the mandibles closed against the face (and thereby presumably with the horn not being capable of playing a role in such entrapment) or would have had an easier time slipping laterally within the large space created by the horn, face, and mandibles. By contrast, the ant could approach larger prey with the mandibles opened, positioned to project beneath a potential quarry. Once the extended trigger hairs would be tripped, the mandibles would rise rapidly, pinning the sufferer against the horn and face. The setae from the brushy lobe would offer friction and potentially information as to the placement and movement of the victim. Moreover, it could be surmised that these structures were exclusive for manipulating nest materials or food other than prey. If this were the case, it would be impossible to explain the presence of trigger hairs, which are known exclusively in carnivorous, trap-jaw lineages. Alternatively, the trigger hairs were long enough to be tripped when the mandibles were closed; thus, Ceratomyrmex could also have snapped its mandibles open to stun prey, to fling attackers away, or to launch themselves away from a potential threat, similarly to what is observed in some modern trap-jaw ants []. An exclusive defense function is excluded, however, because the horn and setose lobe would then be useless.