Martialis heureka Rabeling & Verhaagh HNS , sp. nov.
Worker description (holotype and only known specimen). Measurements: HW 0.65 mm, HL 0.62 mm, SL 0.46 mm, FL 1.03 mm, ML 0.90 mm, WL 1.02 mm, PW 0.40 mm, PEW 0.19 mm, PEL 0.27 mm, PPW 0.34 mm, PPL 0.30 mm, HFL 0.60 mm, HTL 0.57 mm, CI 105, MI 145, SI 72, DI 45 (See Table S1 for definitions and abbreviations of morphometrics). Including the characters of the subfamily and genus description given above: small (HW 0.65, WL 1.02), pale yellow, and blind, integument in dried condition partly translucent. Very long, slender, forcepslike mandibles (ML 0.90, MI 145) inserted on outer anterior margin ofhead capsule, projecting straight forward to =5/7 of its length, then curving slightly mesally. Inner margin bearing a tiny sudmedian tooth at =2/5 of its length, measured from the base and a group of 3 subapical teeth at =5/7 of its length: a median larger tooth and a somewhat smaller tooth to each side of it. The subapical teeth and the sharply pointed mandibular tip frame an oval space. Mandibles crossed in dried condition (Fig. 1), not crossing in live individual (Fig. 2) or while stored in 80% EtOH. Head capsule bulbous in lateral view, narrowing toward posterior margin. Clypeus reduced, narrow strip between lateral head margin and wider between antennal sockets, covered with at least 20 setae that project forward, beyond the margin of antennal sockets, resembling a brush. Antennal scape relatively short (SI 72, DI 45), 1st and 2nd funicular segment 3/4 and V4 longer than 3rd funicular segment. Funiculus more than twice as long as scape. Mesosoma long and slender. Promesonotal suture present, pronotum and mesonotum presumably capable of movement relative to each other. Pronotum forming a slender cervix. Front legs enlarged: procoxae twice as long and wide as meso- and metacoxae; profemura and tibiae also enlarged. Petiole subsessile with a short anterior peduncle; petiolar node rounded, smooth, with a short sloping posterior face; no teeth or projection ventrally. Metasoma (abdominal segment IV-VIII visible) laterally compressed, drop shaped in lateral view. Head, pronotum, and legs densely covered with erect to suberect hairs and sparsely with longer erect setae; mandibular pubescence dense, consisting of short suberect hairs. Inner margin with two rows of at least 18 long straight setae, which are arranged pair wise. Propodeum without any hairs; petiole with few suberect setae on dorsal surface of node and abdominal segment III-VIII with irregularly spaced long erect setae. Dense appressed pubescence absent from entire body. Only few body parts bear distinct sculpturing: neck, mesonotum, propodeum, and ventral surface of petiole punctate; lateral surface of propodeum faintly striate.
Holotype and Locality. Brazil : Amazonas , Manaus. Headquarters of Empresa Brasileira de Pesquisa Agropecuaria (EMBRAPA)- Amazonia Ocidental , located at kilometer 28 of highway AM 010; 2°53'S , 59°59'W ; elev. 40-50 m; 09 May 2003 ; col. C. Rabeling ; ex leaf litter at dusk, primary tropical lowland rainforest. The holotype is deposited in Museu de Zoologia da Universidade de Sao Paulo, Brazil ( MZSP ) .
Etymology. The genus name refers to the unknown combination of aberrant morphological characters, which led Stefan P. Cover and Edward O. Wilson to the conclusion that this ant has to be from the planet Mars; hence, the genus name Martialis HNS (gr.: ''of Mars'' or ''belonging to Mars''). The species epithet heureka (gr.: I found it!) epitomizes the troubled story of the species' rediscovery. Five years after two workers were discovered by M. Verhaagh in a soil sample and subsequently lost, a single worker, the present holotype, was recollected in a nearby patch of primary rainforest.
Discussion. We assume that the present specimen of M. heureka HNS is a worker, because it lacks ocelli, the enlarged mesosoma and the extra sclerites associated with wings (Figs. 1 and 2). In addition, the specimen was collected in the leaf litter suggesting foraging activity usually performed by the worker caste. However, queens with worker-like morphology have been reported from several poneroids and socially parasitic Formicinae and Myrmicinae (26 -29). Because we did not perform a dissection of the single specimen no statement can be made about palpal segmentation or internal anatomy.
Inferred Biology. On the basis of the specimen's external morphology, we are able to infer some aspects of the species' biology. The pale integument and the absence of eyes suggest that M. heureka HNS lives hypogaeicallyor in covered low-light environments, like leaf litter or rotting wood. The fact that the first two M. heureka HNS individuals were collected in soil core samples during the day, and the present specimen in leaf litter at dusk, supports this hypothesis. Possibly, M. heureka HNS surfaces during the night to forage. The unusually enlarged procoxae and long front legs could potentially be an adaptation to prey capture. Presumably, they are used less for digging activities, because the legs are relatively thin and lack the characteristic erect setae of actively digging species. We speculate that M. heureka HNS might take advantage of preexisting underground cavities, like hollow rotten roots (Fig. 2). The forceps-like mandible type is not seen in any other ant species. These long, filigree instruments could be used to drag soft prey items out of cavities. Annelids, termites, insect larvae, and other soft-bodied arthropods are possible prey. We do not expect M. heureka HNS to prey on heavily sclerotized invertebrates.
Phylogenetic Study. To infer the phylogenetic position of M. heureka HNS and to evaluate competing phylogenetic hypotheses, we sequenced 4.2 kb of Martialis HNS heureka's nuclear ribosomal and single-copy nuclear DNA. DNA sequence data were added to a previously published molecular data set of 151 ant species from 20 subfamilies and 11 aculeate outgroup taxa (20), except for four single-copy nuclear genes, which we could not amplify from the limited amount of DNA extract. The phylogeny was inferred using maximum likelihood (ML, 30) and Bayesian inference (BI, 31). Both approaches place Martialis HNS as sister to the remaining extant ants and support the monophyly of all ants, including Martialis HNS (Fig. 3). Martialis HNS did not associate with any extant subfamily in the molecular phylogeny, supporting the designation of the Martialinae as a distinct subfamily on morphological grounds. The basal position of Martialis HNS had a Bayesian posterior probability (BPP) of 0.912, a maximum likelihood bootstrap proportion (ML BP) of 0.76 (Fig. 3), and was strongly supported by Bayes factors (BF, 32-34) over the next most strongly supported rooting (Leptanillinae as basal to all extant ants; 2ln(BF) = -16.4; Fig. 4). However, the more conservative Shimodaira-Hasegawa (SH, 35, 36) test did not reject the alternative rootings (Fig. 4). Even though the BPP and ML BP were only moderately high, the basal positions of Martialis HNS and the Leptanillinae were robust to taxon sampling (Figs. S1 and S2). When Martialis HNS was removed from analyses, the leptanillines were recovered as sister to all extant ants. The converse was true when the leptanillines were removed. Because the basal position of neither Martialis HNS nor the leptanillines changed in the absence of the other, we suggest that their basal position is not because of a particular taxon-sampling scheme.
The basal position of Martialis is not likely caused by longbranch attraction (LBA), as was previously suggested of the leptanillines (20), because Martialis has a substantially shorter branch than all outgroup taxa and the Leptanillinae (Fig. 3). Additionally, the ribosomal DNA sequences in this study (87% of our data set) are the most slowly evolving of the genes used by Brady et al. (20) (58% of their data set) and are least likely to contribute to LBA artifacts (37). Taxon sampling was also increased by one important lineage over previous studies, breaking the long branch that subtended the extant ants in previous studies (20, 21). However, the reconstruction of the molecular ant phylogeny still faces at least two sources of uncertainty that could introduce analytical artifacts. First, even though Martialis HNS breaks the long branch leading to the remaining extant ants, the branch connecting the ingroup to the aculeate outgroup taxa remains long (Fig. 3). Second, the basal ant lineages seem to have originated in a relatively short period (20,21), potentially making the unambiguous resolution of their relationships quite difficult and sensitive to methodological error. Increased gene and taxon sampling for both ants and outgroup aculeates should reduce the potential for statistical artifacts in future analyses.
Fig. 3. Maximum likelihood (ML) tree with Bayesian posterior probabilities (BPP) and ML bootstrap proportions (ML BP) support values. Tree is rooted on the branch leading to the outgroup, Pristocera. The formicoid clade has been collapsed to increase resolution of relationships among basal ant groups ( Martialis HNS , Leptanillinae, and poneroids). Bipartitions with strong Bayesian support are indicated by blue triangles (BPP = 1.0), green circles (0.95 <BPP <1.0) or orange rectangles (0.9 <BPP <0.95).
Our phylogeny supports paraphyly of the poneroids (Fig. 3). The Ponerinae were strongly supported as sister to the formicoids by Bayesian analysis (BPP = 1), although less strongly by ML bootstrap analysis (ML BP = 68). Relationships among the remaining poneroid subfamilies were more ambiguous. The best estimate from both ML and Bayesian analyses (Fig. 3) has an Amblyoponinae/Agroecomyrmecinae clade basal to all other poneroids, followed by a Paraponerinae/Proceratiinae clade, although support is weak (BPP = 58, ML BP <50). Paraphyly of the poneroids was recovered, even if the outgroups, Martialis HNS , the leptanillines, both the outgroups and Martialis HNS , or both the outgroups and the leptanillines were removed from the analysis (Figs. S1 and S2).
Fig . 4. Alternative rootings evaluated with Bayes factors (BF) and the Shimodaira-Hasegawa(SH) test. Constraint trees used to evaluate alternative rootings are depicted on the left. Rootings 1-3 correspond to the first rooting considered by Brady etal. (20), but with alternative arrangements of Martialis HNS and Leptanillinae.Rootings4-7 correspond to Brady etal.'s rootings2-5. For each alternative rooting, the corresponding value of 2ln(BF) is given for the comparison of that rooting againstthe maximum posterior probability (MPP) rooting 1. Values lower than -10 can be interpreted as strong evidence against the alternative. P values resulting from the comparison of alternative rootingsto the maximum likelihood (ML) rooting 1 using the SH test are also given. Rootings significantly worse than the ML rooting would have P values <0.05.
Our phylogenetic analyses, combined with the inferred biology of M. heureka HNS , suggest that the most basal extant ant lineages are cryptic, hypogaeic foragers, rather than wasp-like, epigaeic foragers(Fig. 3). This finding is congruent with recent molecular studies (20-23), which previously suggested the Leptanillinae, another subfamily of subterranean predators, to be sister lineage to all extant ants. This result has puzzled ant systematists for two reasons. First, Wilson et al.'s (16, 17) classic study of the Mesozoic amber ant Sphecomyrma HNS postulated that the ancestral ant was a large-eyed, wasp-like, ground forager, creating a strong expectation that the most basal extant ant lineages would also be epigaeic foragers, presumably similar to Sphecomyrma HNS . Second, the Leptanillinae share common morphological (10, 38) and behavioral (39, 40) characteristics with the Amblyoponinae, implying the monophyly of this group (20). In contrast, our results and recent molecular systematic studies (20 -23) suggest that blind, subterranean, specialized predators, like Martialis HNS , the Leptanillinae, and some poneroids, evolved early during ant diversification. We hypothesize, that once these hypogaeic predators adapted to their specialized subterranean environment, their morphology and biology changed little over evolutionary time because their hypogaeic habitat has likely been ecologically stable and provided a refuge from competition with other, more recently evolved, ants. It is important to note that no definitive statement about the morphology and life history of the ancestral, Mesozoic ant can be derived from our current knowledge about the surviving basalmost ant lineages, because the relative probabilities of evolutionary transitions between epigaeic and hypogaeic habits are uncertain. On the basis of the combined evidence of morphological, phylogenetic, and Mesozoic fossil data, the possibility remains that the ancestral ant was a largeeyed, wasp-like, epigaeic forager (16-19), rather than a blind, specialized, hypogaeic predator.
The Mesozoic fossil Sphecomyrma freyi HNS has been interpreted as a representative of the stem-group ants and ant ground-plan characteristics have been derived from its morphology, suggesting that the most recent common ancestor (MRCA) of ants could be similar to tiphioid wasps (16-18). By considering both the topology of our inferred phylogeny (Fig. 3), and the timing of ant diversification presented in previous studies (20, 21), the Sphecomyrminae could alternatively be placed within the subfamilies grouped in the formicoid clade or as stem-group members of the formicoid subfamilies rather than the Formicidae as a whole (16-19). However, the morphology-inferred sister group relationship of Sphecomyrma HNS to all extant ants (14) and the absence of hypogaeic ant fossils in Cretaceous deposits (11, 24, 41-50) do not support this hypothesis.
Conclusion. Martialis heureka HNS exhibits a mosaic of plesiotypic ant characters and derived morphological adaptations to its hypogaeic predaceous lifestyle. The discovery of Martialis HNS and our phylogenetic analyses support the hypothesis that several of the most basal extant ant lineages are hypogaeic foragers, suggesting that hypogaeic foraging evolved at least thrice independently during the early evolution of ants or that the ancestral ant was a hypogaeic forager. These evolutionary scenarios are congruent with the dynastic succession hypothesis for ant evolution (5, 20, 21), proposing a ground-associated ant ancestor, derived from a wasp-like, aculeate predator that radiated into specialized soil, leaf litter, and arboreal habitats potentially coinciding with the diversification of the angiosperms. Martialis HNS and other soildwelling basal ants might therefore be relicts of early ant diversification, which survived in an environmentally stable refuge habitat, permitting them to retain plesiotypic characteristics because of reduced selective pressures. The exact nature of the ancestral ant remains uncertain, given that the propensity for repeated evolution of a hypogaeic lifestyle may be higher than for reevolution of an epigaeic lifestyle. Interestingly, M. heureka HNS is a unique Neotropical representative of an extant, basal ant lineage. This discovery hints at a wealth of species, possibly of great evolutionary importance, still hidden in the soils of the remaining rainforests. Nocturnal leaf litter sampling and subterranean traps would be promising additions to future biodiversity surveys.
Subfamily Martialinae Rabeling & Verhaagh, subfam. nov.
Martialis heureka Rabeling & Verhaagh HNS , gen. et sp. nov.
Martialinae Rabeling & Verhaagh, subfam. nov.
Worker diagnosis: small, blind, pale, presumably subterranean ants with the following combination of characters. Putative apomorphic conditions are marked by an asterisk. (1) Prementum partlyvisible with closed mouthparts, not entirelyconcealed behind the broad labrum and stipites; (2*) clypeus highly reduced; (3*) eyes absent; (4) frontal lobes absent; (5*) antennal sockets fully exposed and distant from each other, positioned at anterior margin of clypeus and projecting anteriorly beyond it; (6*) toruli raised vertically, forming cups to hold condylar bulbs; (7) antennae 12 segmented; (8) promesonotal suture present and flexible; (9) propodeal lobes absent; (10) metapleural gland orifice slit shaped, dorsal orifice margin projecting slightly forward, but not overhanging or concealing opening; (11*) metacoxal cavity closed, with a complete cuticular annulus surrounding the cavity; (12) metasternal process absent; (13*) petiole tergosternally fused, without a trace of a suture between tergite and sternite; (14*) abdominal segment III broadly attached to segment IV but distinctly smaller than the latter, tergosternally fused; (15) helcial tergite well developed, posterior part with a girdling constriction; (16) abdominal segment IV not tergosternally fused, posttergite broadly overlapping abdominal segment V; (17) stridulitrum on presclerite of abdominal segment IV absent; (18) spiracles of abdominal segments I-IV exposed, of V-VII concealed by preceding postsclerites; (19) pygidium (tergite of abdominal segment VII) well developed, simple, neither armed with teeth or setae nor heavily sclerotized nor otherwise modified; (20) sting present; (21) metatibial gland absent; (22) tarsal claws simple, without preapical teeth.
Author contributions: C.R., J.M.B., and M.V. designed research, performed research, analyzed data, and wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. EU913472-EU913474).
§To whom correspondence should be addressed. E-mail: firstname.lastname@example.org.
This article contains supporting information online at www.pnas.org/cgi/content/full/ 0806187105/DCSupplemental.
© 2008 by The National Academy of Sciences of the USA
Fig . 2. Worker of Martialis heureka HNS foraging in a subterranean tunnel. This drawing depicts M. heureka HNS in its assumed natural habitat as inferred from its external morphology. Please see the Inferred 6iology section for a more detailed discussion of the species' biology. (Scale bar: 1 mm.) Color pencil drawing by Barrett A. Klein.
Queen, male, and larva are unknown.
Martialis heureka is a species of ant discovered in 2000 from the Amazon rainforest near Manaus, Brazil. It was described as a new species and placed as the sole member of a new subfamily, Martialinae. The generic name means "from Mars" and was given due to its unusual morphology, and the species epithet heureka indicates the surprising discovery. It belongs to the oldest known distinct lineage to have diverged from the ancestors of all other ants.
Like all members of the family Formicidae, these ants have distinctive elbowed antennae, prominent metapleural glands, and distinctive petioles. The ants, though, lack compound eyes, are pale in colour, and lead a subterranean life, preying on small litter organisms. The workers have unusual, elongated mandibles, distinctly basal in their features.
Based on the morphology, the authors suggested the ants lead an underground life, possibly foraging on the surface during the night. The first two specimens were found in soil core samples,while another was found in leaf litter. They probably make use of pre-existing underground cavities,as their legs do not show adaptations for digging.
Two specimens were first discovered by Manfred Verhaagh of the Staatliches Museum für Naturkunde in Karlsruhe, Germany, in 2000, but they were damaged, and a new specimen was collected in 2003 by Christian Rabeling, a graduate student of the University of Texas at Austin.
The aberrant features of this ant led Stefan P. Cover and Edward O. Wilson to comment that it was an ant that had to be from Mars. The genus name, then, refers to the planet Mars, alluding to the strange characteristics that seem to come from nowhere; the species epithet is from Ancient Greek ηὕρηκα "I found it", echoing Archimedes' famous exclamation, meant to epitomize the troubles involved in the rediscovery of the species after the first specimen discovered in a soil sample was lost.
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