Evaluating alternative hypotheses for the early evolution and diversification of ants

Abstract

Ants are the world's most diverse and ecologically dominant eusocial organisms. Resolving the phylogeny and timescale for major ant lineages is vital to understanding how they achieved this success. Morphological, molecular, and paleontological studies, however, have presented conflicting views on early ant evolution. To address these issues, we generated the largest ant molecular phylogenetic data set published to date, containing Ϸ6 kb of DNA sequence from 162 species representing all 20 ant subfamilies and 10 aculeate outgroup families. When these data were analyzed with and without outgroups, which are all distantly related to ants and hence long-branched, we obtained conflicting ingroup topologies for some early ant lineages. This result casts strong doubt on the existence of a poneroid clade as currently defined. We compare alternate attachments of the outgroups to the ingroup tree by using likelihood tests, and find that several alternative rootings cannot be rejected by the data. These alternatives imply fundamentally different scenarios for the early evolution of ant morphology and behavior. Our data strongly support several notable relationships within the more derived formicoid ants, including placement of the enigmatic subfamily Aenictogitoninae as sister to Dorylus army ants. We use the molecular data to estimate divergence times, employing a strategy distinct from previous work by incorporating the extensive fossil record of other aculeate Hymenoptera as well as that of ants. Our age estimates for the most recent common ancestor of extant ants range from Ϸ115 to 135 million years ago, indicating that a Jurassic origin is highly unlikely.divergence dating ͉ Formicidae ͉ long-branch attraction ͉ phylogeny A nts (Hymenoptera:Formicidae) are the world's most successful group of eusocial insects. They constitute 15-20% of the animal biomass in tropical rainforests (1, 2) and occupy keystone positions in many terrestrial environments (3). Ants are among the leading predators of invertebrates in most ecosystems and are also prominent herbivores in many neotropical communities. Various ant species participate in symbiotic relationships with Ͼ465 plant species in Ͼ52 families (4), with thousands of arthropod species (5, 6), and with as-yet-unknown numbers of fungi and microorganisms (7). Some ant lineages have evolved astonishing adaptive specializations [agriculture of fungi, seed harvesting, herding and milking of other insects, communal nest weaving, cooperative hunting in packs, social parasitism, and slave-making (6)] that have fueled the curiosities of scientists as well as the general public.Understanding the sequence of events contributing to the rise of ants to ecological dominance requires a robust phylogeny of their early evolution and a reliable timescale for their diversification. However, both the age of ants and the relationships among their earliest evolving lineages remain controversial. Ant fossils from the Cretaceous are relatively scarce (8, 9), although their abundance and diversity inc...

Comparative genomics of chemosensory protein genes reveals rapid evolution and positive selection in ant-specific duplicates

“…In order to evaluate whether different approaches give Figure 1 Ant species used in this study. The divergence estimates are in My and based on large-scale sequence data from Brady et al (2006) and Moreau et al (2006). CSP evolution in ants J Kulmuni et al similar results, we made a neighbour-joining tree of each alignment and confirmed that different alignment methods produced similar overall topology.…”

Natural selection drives the evolution of ant life cycles

“…The basal rooting of present-day Martialinae and Leptanillinae places the origin and early diversification of ants as far back as Early Cretaceous times. Molecular phylogenetic studies of these and other living species place the origin of almost all the living subfamilies in the early or middle Late Cretaceous or the Early Paleogene Periods (29)(30)(31). The history of the ants as a whole, however, appears not to extend as far back as the Jurassic Period (29)(30)(31).…”

“…The origin of eusociality in halictid bees occurred during the mid-Paleogene Period, 35 Mya (27,28). The ants appeared, evidently from a single aculeate wasp ancestor (29), during the Cretaceous Period, about 140 Mya (29)(30)(31). By the Paleogene Period and likely during the very Late Cretaceous, most or all of the contemporary 21 ant subfamilies had separated (29-31).…”

“…Some species might have existed in sparse populations, as exemplified today by modern Microstigmus wasps, or have lived in hidden niches, as do presentday scolytid beetles and gall-forming thrips. As yet, however, no trace has been detected of an anatomically distinct worker caste, the hallmark of obligatory eusociality (26)(27)(28)(29)(30)(31)(32)(33).…”

Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants

“…Throughout the course of their 115-168 million year history (7,8), these diverse and ecologically dominant insects have repeatedly evolved symbiotic relationships with sap-feeding insects (9), plants (10), and microbes (11, 12, 13), including nitrogen-recycling and upgrading Blochmannia species harbored by ants from the Camponotini (carpenter ants) (14, 15). With only a few exceptions outside of this group (16)(17)(18)(19)(20) and the tribe Attini (13), we know little about the identities and significance of bacteria across Ͼ12,000 described ant species.…”