What was the fate of the first evolutionary radiation of the ants? The Sphecomyrminae evidently vanished by the end of the Mesozoic. The myrmeciines retreated to Australia and New Caledonia, and the aneuretines retreated to Sri Lanka. But the myrmicines, formicines, and dolichoderines, together with the ponerines (the dominant poneromorph subfamily), not only flourished, but spread worldwide as ecologically pre-eminent insect groups. The history of the Ponerinae is of special interest in this story. Evidently monophyletic and comprising three tribes and 25 genera (4), the ponerines are as variable overall in anatomical characteristics and patterns of colony organization as any of the other subfamilies. Yet, despite being with the Formicinae and Myrmeciinae members of the oldest documented living phylogenetic assemblage and despite having achieved such prolific diversification and geographic breadth, they remain oddly primitive in their general social organization (27).
- Queens and workers of ponerine species are much closer in size than are the castes in the “higher” ant subfamilies Myrmicinae, Dolichoderinae, and Formicinae and army ant subfamilies.
- Most ponerine queens have relatively low fertility, seldom producing more than five eggs each day.
- Corresponding to the low degree of queen fecundity, colony sizes of ponerines are small.
- Young ponerine queens of many, perhaps most, species start new colonies independently but not claustrally. That is, they leave their natal nest, mate, and construct a nest of their own or find a preformed cavity. But then, like some wasps and other poneromorph ants, they forage outside the nest to obtain at least part of the food with which they rear the first brood of workers.
- With a few, sometimes striking exceptions (28, 29), workers of ponerine species forage alone and do not use odor trails or other pheromone signals to recruit nestmates to food sources they encounter.
- True oral trophallaxis, the exchange of regurgitated food among adults and between workers and larvae, is wide-spread in the higher subfamilies Myrmicinae, Dolichoderinae, and Formicinae. It is evidently much less so in the Ponerinae and, to date, has been observed only in the closely related genus Ponera and Hypoponera (30), with liquid otherwise transferred from drops held between the mandibles (31).
This, then, is the ponerine paradox: globally successful yet socially primitive. The puzzle might be partially resolved if the more advanced ant subfamilies can be shown to be derived from a ponerine stock or, put in the more exact language of cladistics, the paradox is partly soluble if the ponerines prove to be polyphyletic (of multiple origins). But even if such proves to be the case (contrary to the opinion of systematists who consider the ponerines overall monophyletic), there likely remain diverse modern subgroups that are surely monophyletic, such as the very large and global tribe Ponerini. So the paradox would not be truly resolved by taxonomic splitting.
The full and definitive solution to the ponerine paradox and other mysteries of ant evolution requires more information from paleontology and ecology than now exists. In the interim, and in the hope of stimulating research in the critical areas, we offer the following combined phylogenetic and ecological “dynastic-succession” hypothesis (under the “Dynastic-Succession Hypothesis” heading below), consistent with existing knowledge (commentary added above and below heading).
Possibly toward the end of Cretaceous times, but more likely during Paleocene and Early Eocene times, after the end-of-Mesozoic extinction spasm of many plant and animal groups, the ponerines underwent most of the adaptive radiation in taxonomic tribes and adaptive types that persist to the present time.
The fossil record of this interval, spanning some 30 million years, is still poorly represented for ants, preventing an exact placement of the ponerine radiation in geological history.
During this primary expansion, the ponerines became entrenched worldwide as arthropod predators, especially in warm-temperate and tropical mesic forests. They also evolved to favor ground and leaf-litter sites. In effect, they pre-empted this array of opportunities, partially blocking the sites from the later, otherwise more successful radiations of the advanced subfamilies Dolichoderinae and Formicinae. Of the “big four” in present-day diversity and geographic reach, only the Myrmicinae rivaled the Ponerinae in invasion of the forest-floor predator niches. Either the myrmicine radiation coincided with the peak of the ponerine expansion or followed close behind it.
The diets of by far the most known ponerines consist primarily or exclusively of fresh insect and other arthropod prey, supplemented by the scavenging of arthropods newly killed by other causes. Many ponerine species are, moreover, specialized predators (22, 27).
Ants foraging as solitary huntresses have small colonies, a necessity imposed by the relative paucity of their food, and the more so when they specialize on particular kinds of prey. Predation as a way of life and small colony size, in turn, render other social traits simple and hence “primitive.” Foraging tends to be solitary, recruitment and alarm simple, and worker subcastes few to none; workers are prepared to reproduce on their own in the absence of the queen, and brood care tends to be relatively unorganized.
The ponerines and other poneromorphs do well as predators and also as occupants of nest sites on forest floors in warm regions around the world (32). The favored sites are small spaces in the many dimensions of the litter, including the interiors of rotting logs and stumps, tree limbs and twigs lying on the ground, clusters of dead leaves, masses of bryophytes, and the root systems of living trees, shrubs, and herbaceous plants.
The ponerines hold their own in this complex and nutrient-rich environment. In samples recently analyzed from forested localities around the world (32), poneromorphs (mostly ponerines) composed 22.2% of the species and 12.4% of the specimens, compared with 10.6% of the species and 12.9% of the specimens for the formicines and a relatively paltry 1.1% of the species and 0.5% of the specimens for the dolichoderines. But these three subfamilies of the “big four” were dwarfed by the myrmicines, which made up 65.2% of the species and 73.7% of the specimens. Clearly, the myrmicines, many of which (such as members of the tribes Dacetini and Basicerotini) are specialized predators like the ponerines, are the rulers of the world's forest litter.
The soil and ground litter of the world's angiosperm forests, and especially tropical forests, comprise the habitat with the highest density and species diversity of ants. Because all of the subfamilies of ants since their origins in the mid-Cretaceous have living representatives, save the Sphecomyrminae and Formiciinae (the latter were giant ants, not to be confused with Formicinae), and most of the genera originating since the late Eocene also have them, it is reasonable to suppose that the tropical forest soil and ground litter has always played the same role. This habitat is reasonably interpreted to be the headquarters of ant evolution, from which major ant groups have spread into other habitats or, in a great many cases, failed to do so.
The picture changes radically for the ponerines and most other poneromorphs, for example, in habitats away from the tropical and warm-temperate forests. They are notably scarce in cool-temperate forests, deserts, and arid grasslands. (In contrast, one other poneromorph subfamily, the Ectatomminae, has done well in these peripheral habitats, especially in Australia.)
The picture changes in equal degree across a few vertical meters in the forests and thence on up into the forest canopy. In the Amazonian and Bornean forests, for example, subfamily dominance is nearly flipped upside down. There, the formicines and dolichoderines have risen sharply in numbers relative to the myrmicines, while the ponerines have dropped to very low levels (33, 34).
The great majority of the canopy ant species appear to be specialized for arboreal life, as opposed to being invaders from ground nests. Oddly, the arboreal ants, as a whole, are so abundant and possess such a large part of the animal biomass as to be inviable if they lived exclusively as predators and scavengers. Although tropical arboreal ants are, in general, highly efficient in these roles (35), there are not enough herbivorous insects available as immediate sources of protein to support them. This additional paradox now appears solved: It has been learned that in the Amazon forest, at least a large fraction of the ant populations of the canopy are not primarily predators but “cryptic herbivores,” subsisting on the liquid exudates of hemipterous sap-feeding insects, including scale insects and treehoppers (36, 37). They further tend many of these insects as a kind of cattle, protecting them from parasites and predators. Extrafloral nectaries are yet another significant plant-based source of nutrition.
Around the world, in all major habitats, a large fraction of the species of dolichoderines and formicines have invested their biology heavily in symbioses with aphids, mealybugs, and other homopterous insects. Myrmicines have done so to lesser degree, and ponerines almost never. Although quantitative data are lacking, these disparities are commonly observed in natural history studies, and it seems clear that the dolichoderines and formicines have benefited in the growth of their biomass and diversity through coevolution with symbiotic homopterans. These observations lead to the final part of the dynastic-succession hypothesis.