PERSPECTIVE The rise of the ants: A phylogenetic and ecological explanation Edward O. Wilson*† and Bert Ho¨ lldobler‡§ *Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138-2902; ‡School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501; and §Theodor-Boveri-Institut fu¨r Biowissenschaften (Biozentrum) der Universita¨t, Am Hubland, D-97074 Wu¨rzburg, Germany Contributed by Edward O. Wilson, March 18, 2005 In the past two decades, studies of anatomy, behavior, and, most recently, DNA sequences have clarified the phylogeny of the ants at the subfamily and generic levels. In addition, a rich new harvest of Cretaceous and Paleogene fossils has helped to date the major evolutionary radiations. We collate this information and then add data from the natural history of the modern fauna to sketch a his- tory of major ecological adaptations at the subfamily level. The key events appear to have been, first, a mid-Cretaceous initial radia- tion in forest ground litter and soil coincident with the rise of the angiosperms (flowering plants), then a Paleogene advance to eco- logical dominance in concert with that of the angiosperms in tropical forests, and, finally, an expansion of some of the lineages, aided by changes in diet away from dependence on predation, upward into the canopy, and outward into more xeric environments. ecology ͉ evolution ͉ phylogeny ͉ sociobiology umanity lives in a world recently divided (4), comprising the myrmine and more derivative traits. The largely filled by prokaryotes, abundant and diverse Ponerinae and Burmese amber (10), containing spheco- fungi, flowering plants, nem- five other less prominent subfamilies. myrmines and a possible myrmeciine, atode worms, spiders, mites, The workers of Sphecomyrma, the may be of comparable or even some- Hand six ecological keystone insect best known sphecomyrmine genus, were what older provenance. groups: termites, hemipteran ‘‘true’’ a mosaic of ant and wasp traits (5, 6). In still other very early deposits have bugs, phytophagan beetles, cyclorraphan Specimens have been found in deposits been found additional products of the flies, glossatan moths, and hymenopter- of Late Cretaceous amber (fossilized initial ant radiation, which appear to be ans, the last comprising bees, wasps— resin) in Asia, Siberia, and North Amer- members or precursors of the bulldog and ants (1). Ants are especially notable ica, hence across much of the northern ant subfamily Myrmeciinae, including among the insects for their ecological supercontinent of Laurasia (7, 8). the living ‘‘dawn ant’’ Nothomyrmecia dominance as predators, scavengers, and Unlike the ants of later, Paleogene macrops. The subfamily is today limited indirect herbivores. Although the deposits, the sphecomyrmines are very to Australia, with one very rare species Ϸ11,000 species of the ant family (For- rare. Among the many thousands of of Myrmecia on New Caledonia. A pos- micidae) make up Ͻ2% of the known Cretaceous insect specimens examined sible but still uncertain myrmeciine or global insect fauna, they compose at from New Jersey, Canada, and Burma, myrmeciine precursor, Cariridris bipeti- least one-third of its biomass (2). In the only seven specimens have enough fea- olata, has been described from a single, Brazilian Amazon, as judged by one sur- tures preserved to be called definitively poorly preserved specimen in the San- vey (3), the biomass of ants is approxi- sphecomyrmine workers. Of the biology tana Formation of Brazil, Ϸ110 million mately four times greater than that of of these ancient ants it can be said only years old. What seem to us to be other all of the land vertebrates (mammals, that they lived in mesic forests with rich myrmeciines are 10 rock fossils from the birds, reptiles, and amphibians) floras and insect faunas. The exact tim- Upper Cretaceous Orapa deposits of combined. ing and causes of their extinction in the Botswana (Ϸ90 million years B.P.) (12). The combination of advanced colonial final 10 or 20 million years of that era Several later myrmeciines of Paleogene life and worldwide environmental influ- remain unknown (9, 10). age, Ameghinoia and Polanskiella of Ar- ence gives special significance to the Early in the history of the sphecom- gentina, Archimyrmex of the U.S. Green evolutionary history of the ants. Recent yrmines, a wider radiation beyond the River Formation, and two species of phylogenetic analyses, when combined stem genus Sphecomyrma occurred. In Prionomyrmex recorded from the Baltic with data from a rich new harvest of addition to clearly derivative spheco- amber, bear witness to the spread of the Cretaceous and Paleogene fossils and myrmine genera were a sphecomyrmine- subfamily around the world, followed by the natural history of the modern fauna, ponerine intermediate (8), an apparent its retreat to Australia. It is reasonable permit a defensible reconstruction of true poneromorph, a member of the ad- to suppose that the Myrmeciinae di- the broad-scale ecological features of vanced subfamily Formicinae (9), and a verged from the sphecomyrmine stem ant evolution. possible member of the subfamily Aneu- and spread extensively by Late Creta- retinae, considered to be precursors of the ceous or Eocene times (13, 14). The Earliest Ants modern subfamily Dolichoderinae (10). By Paleocene times, as evidenced in Ants evidently arose during the Creta- What appear to be the oldest certifi- 10 specimens of ants from the presumed ceous period at somewhat more than able ant fossils include Gerontoformica Paleocene amber of Sakhalin, doli- 100 million years ago. Their earliest cretacica, from the Early Cenomanian to choderines and aneuretines (the latter known fossils fall into two groups. The Uppermost Abian (Lower Cretaceous) with one contemporary species, Aneure- first is the very primitive Mesozoic sub- amber of France, dated to Ϸ100 million family Sphecomyrminae. The second years B.P. (11). Because of imperfect group consists of primitive members of preservation, it cannot be placed with †To whom correspondence should be addressed. E-mail: the extant subfamily Formicinae and the reference to fossil or existing subfamilies [email protected]. poneromorph group of subfamilies, as but evidently contains a mix of spheco- © 2005 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0502264102 PNAS ͉ May 24, 2005 ͉ vol. 102 ͉ no. 21 ͉ 7411–7414 Downloaded by guest on September 29, 2021 tus simoni, surviving in Sri Lanka) had made their appearance alongside of poneromorphs, myrmeciines, and for- micines (15). By the Early to Middle Eocene, as revealed by the recently described Fushun amber fauna from northeastern China that is Ϸ50 million years or some- what younger in age, the diversification of the major groups of ants was in full play (16). Among some 20 identifiable specimens of workers and queens is a variety of primitive ponerines and myr- micines as well as primitive members of the ‘‘formicoid’’ complex, comprising formicines and an assortment of what are either primitive dolichoderines, an- euretines, or both. Most also bear traits shared with their presumed spheco- myrmine or sphecomyrmine-like ances- tors, including short mandibles with small numbers of teeth, circular or ovoid head shapes, and relatively unmodified middle body segments. Several sedimen- tary compression fossils of Early Eocene provenance recently discovered in Brit- ish Columbia also represent relatively primitive poneromorphs (B. Archibald, personal communication). Emergence of the Modern Fauna The next glimpse into the history of the ants has come from a set of three speci- mens found in a middle Eocene amber Fig. 1. A schematic of the evolution of ants (Formicidae) at the subfamily level. Minor subfamilies are deposit at Malvern, Arkansas, that omitted. The four most diverse, abundant, and geographically widespread living subfamilies are bold- represents three of the dominant sub- faced. The ‘‘dorylomorphs’’ are driver and army ants (Dorylinae) and an array of other, smaller subfamilies related to them. The schematic is based on our interpretation of the consensus of recent phylogenetic families in the present-day fauna: reconstructions (8, 9, 23–26). The Armaniidae were a Cretaceous sister group of the Formicidae that were Myrmicinae, Dolichoderinae, and believed not to be social; i.e., they had no anatomically distinct worker class (7). Formicinae (17). That the modern radiation had not only begun by Eocene times but was Origin and Phylogeny of the Mesozoic. The myrmeciines re- full-blown is disclosed by the Baltic am- The phylogeny of ants has been the sub- treated to Australia and New Caledonia, ber fossils, which are Middle Eocene in ject of several steadily improving recon- and the aneuretines retreated to Sri age. In examining 10,988 specimens as structions during the past half-century, Lanka. But the myrmicines, formicines, part of their pioneering ant fossil stud- starting with morphological data of and dolichoderines, together with the ies, G. Mayr (18) and W. M. Wheeler living faunas (9, 14, 21–23), then ad- ponerines (the dominant poneromorph (19) distinguished no fewer than 92 gen- vancing with additional morphological subfamily), not only flourished, but era. Ants were among the dominant in- information supplemented by fossil evi- spread worldwide as ecologically pre- sects, and the species as a whole had a dence, as reviewed here, and, finally, by eminent insect groups. The history of distinctly modern aspect, despite its the addition