Ted R. Schultz

Evaluating alternative hypotheses for the early evolution and diversification of ants

Ants are the worlds 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 ≈6 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 ≈115 to 135 million years ago, indicating that a Jurassic origin is highly unlikely.

Major evolutionary transitions in ant agriculture

Agriculture is a specialized form of symbiosis that is known to have evolved in only four animal groups: humans, bark beetles, termites, and ants. Here, we reconstruct the major evolutionary transitions that produced the five distinct agricultural systems of the fungus-growing ants, the most well studied of the nonhuman agriculturalists. We do so with reference to the first fossil-calibrated, multiple-gene, molecular phylogeny that incorporates the full range of taxonomic diversity within the fungus-growing ant tribe Attini. Our analyses indicate that the original form of ant agriculture, the cultivation of a diverse subset of fungal species in the tribe Leucocoprineae, evolved ≈50 million years ago in the Neotropics, coincident with the early Eocene climatic optimum. During the past 30 million years, three known ant agricultural systems, each involving a phylogenetically distinct set of derived fungal cultivars, have separately arisen from the original agricultural system. One of these derived systems subsequently gave rise to the fifth known system of agriculture, in which a single fungal species is cultivated by leaf-cutter ants. Leaf-cutter ants evolved remarkably recently (≈8–12 million years ago) to become the dominant herbivores of the New World tropics. Our analyses identify relict, extant attine ant species that occupy phylogenetic positions that are transitional between the agricultural systems. Intensive study of those species holds particular promise for clarifying the sequential accretion of ecological and behavioral characters that produced each of the major ant agricultural systems.

Evolutionary history of the symbiosis between fungus-growing ants and their fungi

The evolutionary history of the symbiosis between fungus-growing ants (Attini) and their fungi was elucidated by comparing phylogenies of both symbionts. The fungal phylogeny based on cladistic analyses of nuclear 28S ribosomal DNA indicates that, in contrast with the monophyly of the ants, the attine fungi are polyphyletic. Most cultivated fungi belong to the basidiomycete family Lepiotaceae; however, one ant genus, Apterostigma, has acquired a distantly related basidiomycete lineage. Phylogenetic patterns suggest that some primitive attines may have repeatedly acquired lepiotaceous symbionts. In contrast, the most derived attines have clonally propagated the same fungal lineage for at least 23 million years.

THE ORIGIN OF THE ATTINE ANT-FUNGUS MUTUALISM

Cultivation of fungus for food originated about 45-65 million years ago in the ancestor of fungus-growing ants (Formicidae, tribe Attini), representing an evolutionary transition from the life of a hunter-gatherer of arthropod prey, nectar, and other plant juices, to the life of a farmer subsisting on cultivated fungi. Seven hypotheses have been suggested for the origin of attine fungiculture, each differing with respect to the substrate used by the ancestral attine ants for fungal cultivation. Phylogenetic information on the cultivated fungi, in conjunction with information on the nesting biology of extant attine ants and their presumed closest relatives, reveal that the attine ancestors probably did not encounter their cultivars-to-be in seed stores (von Ihering 1894), in rotting wood (Forel 1902), as mycorrhizae (Garling 1979), on arthropod corpses (von Ihering 1894) or ant faeces in nest middens (Wheeler 1907). Rather, the attine ant-fungus mutualism probably arose from adventitious interactions with fungi that grew on walls of nests built in leaf litter (Emery 1899), or from a system of fungal myrmecochory in which specialized fungi relied on ants for dispersal (Bailey 1920) and in which the ants fortuitously vectored these fungi from parent to offspring nests prior to a true fungicultural stage.

A phylogenetic analysis of the fungus-growing ants (Hymenoptera: Formicidae: Attini) based on morphological characters of the larvae

A phylogenetic hypothesis of the fungus‐growing ants (subfamily Myrmicinae, tribe Attini) is proposed, based on a cladistic analysis utilizing forty‐four morphological characters (109 states) of the prepupal worker larva. The fifty‐one attine species analysed include representatives of eleven of the twelve currently recognized attine genera, excluding only the monotypic workerless parasite Pseudoatta; the non‐attines include two outgroups (species of the basal myrmicine genera Myrmica and Pogonomyrmex), two myrmicine species presumed to be distantly related to the attines, and twelve species representing taxa that have been proposed by prior workers as possible sister groups of the Attini. There is strong character support for the monophyly of the Attini and for a sister‐group relationship of the Attini and the Neotropical Blepharidatta brasiliensis. The Attini are divided into two distinct lineages, an ‘apterostigmoid’ clade (containing Apterostigma and Mycocepurus) and an ‘attoid’ clade (containing all other attine genera except Myrmicocrypta). The attine genus Myrmicocrypta appears to be paraphyletic with respect to these two groups; the species M.buenzlii in particular retains many attine plesiomorphies.

The evolution of myrmicine ants: phylogeny and biogeography of a hyperdiverse ant clade (Hymenoptera: Formicidae)

This study investigates the evolutionary history of a hyperdiverse clade, the ant subfamily Myrmicinae (Hymenoptera: Formicidae), based on analyses of a data matrix comprising 251 species and 11 nuclear gene fragments. Under both maximum likelihood and Bayesian methods of inference, we recover a robust phylogeny that reveals six major clades of Myrmicinae, here treated as newly defined tribes and occurring as a pectinate series: Myrmicini, Pogonomyrmecini trib.n., Stenammini, Solenopsidini, Attini and Crematogastrini. Because we condense the former 25 myrmicine tribes into a new six‐tribe scheme, membership in some tribes is now notably different, especially regarding Attini. We demonstrate that the monotypic genus Ankylomyrma is neither in the Myrmicinae nor even a member of the more inclusive formicoid clade—rather it is a poneroid ant, sister to the genus Tatuidris (Agroecomyrmecinae). Several species‐rich myrmicine genera are shown to be nonmonophyletic, including Pogonomyrmex, Aphaenogaster, Messor, Monomorium, Pheidole, Temnothorax and Tetramorium. We propose a number of generic synonymies to partially alleviate these problems (senior synonym listed first): Pheidole = Anisopheidole syn.n. = Machomyrma syn.n.; Temnothorax = Chalepoxenus syn.n. = Myrmoxenus syn.n. = Protomognathus syn.n.; Tetramorium = Rhoptromyrmex syn.n. = Anergates syn.n. = Teleutomyrmex syn.n. The genus Veromessor stat.r. is resurrected for the New World species previously placed in Messor; Syllophopsis stat.r. is resurrected from synonymy under Monomorium to contain the species in the hildebrandti group; Trichomyrmex stat.r. is resurrected from synonymy under Monomorium to contain the species in the scabriceps‐ and destructor‐groups; and the monotypic genus Epelysidris stat.r. is reinstated for Monomorium brocha. Bayesian divergence dating indicates that the crown group Myrmicinae originated about 98.6 Ma (95% highest probability density 87.9–109.6 Ma) but the six major clades are considerably younger, with age estimates ranging from 52.3 to 71.1 Ma. Although these and other suprageneric taxa arose mostly in the middle Eocene or earlier, a number of prominent, species‐rich genera, such as Pheidole, Cephalotes, Strumigenys, Crematogaster and Tetramorium, have estimated crown group origins in the late Eocene or Oligocene. Most myrmicine species diversity resides in the two sister clades, Attini and Crematogastrini, which are estimated to have originated and diversified extensively in the Neotropics and Paleotropics, respectively. The newly circumscribed Myrmicini is Holarctic in distribution, and ancestral range estimation suggests a Nearctic origin. The Pogonomyrmecini and Solenopsidini are reconstructed as being Neotropical in origin, but they have subsequently colonized the Nearctic region (Pogonomyrmecini) and many parts of the Old World as well as the Nearctic region (Solenopsidini), respectively. The Stenammini have flourished primarily in the northern hemisphere, and are most likely of Nearctic origin, but selected lineages have dispersed to the northern Neotropics and the Paleotropics. Thus the evolutionary history of the Myrmicinae has played out on a global stage over the last 100 Ma, with no single region being the principal generator of species diversity.

The evolution of myrmicine ants: Phylogeny and biogeography of a hyperdiverse ant clade

This study investigates the evolutionary history of a hyperdiverse clade, the ant subfamily Myrmicinae (Hymenoptera: Formicidae), based on analyses of a data matrix comprising 251 species and 11 nuclear gene fragments. Under both maximum likelihood and Bayesian methods of inference, we recover a robust phylogeny that reveals six major clades of Myrmicinae, here treated as newly defined tribes and occurring as a pectinate series: Myrmicini, Pogonomyrmecini trib.n., Stenammini, Solenopsidini, Attini and Crematogastrini. Because we condense the former 25 myrmicine tribes into a new six‐tribe scheme, membership in some tribes is now notably different, especially regarding Attini. We demonstrate that the monotypic genus Ankylomyrma is neither in the Myrmicinae nor even a member of the more inclusive formicoid clade—rather it is a poneroid ant, sister to the genus Tatuidris (Agroecomyrmecinae). Several species‐rich myrmicine genera are shown to be nonmonophyletic, including Pogonomyrmex, Aphaenogaster, Messor, Monomorium, Pheidole, Temnothorax and Tetramorium. We propose a number of generic synonymies to partially alleviate these problems (senior synonym listed first): Pheidole = Anisopheidole syn.n. = Machomyrma syn.n.; Temnothorax = Chalepoxenus syn.n. = Myrmoxenus syn.n. = Protomognathus syn.n.; Tetramorium = Rhoptromyrmex syn.n. = Anergates syn.n. = Teleutomyrmex syn.n. The genus Veromessor stat.r. is resurrected for the New World species previously placed in Messor; Syllophopsis stat.r. is resurrected from synonymy under Monomorium to contain the species in the hildebrandti group; Trichomyrmex stat.r. is resurrected from synonymy under Monomorium to contain the species in the scabriceps‐ and destructor‐groups; and the monotypic genus Epelysidris stat.r. is reinstated for Monomorium brocha. Bayesian divergence dating indicates that the crown group Myrmicinae originated about 98.6 Ma (95% highest probability density 87.9–109.6 Ma) but the six major clades are considerably younger, with age estimates ranging from 52.3 to 71.1 Ma. Although these and other suprageneric taxa arose mostly in the middle Eocene or earlier, a number of prominent, species‐rich genera, such as Pheidole, Cephalotes, Strumigenys, Crematogaster and Tetramorium, have estimated crown group origins in the late Eocene or Oligocene. Most myrmicine species diversity resides in the two sister clades, Attini and Crematogastrini, which are estimated to have originated and diversified extensively in the Neotropics and Paleotropics, respectively. The newly circumscribed Myrmicini is Holarctic in distribution, and ancestral range estimation suggests a Nearctic origin. The Pogonomyrmecini and Solenopsidini are reconstructed as being Neotropical in origin, but they have subsequently colonized the Nearctic region (Pogonomyrmecini) and many parts of the Old World as well as the Nearctic region (Solenopsidini), respectively. The Stenammini have flourished primarily in the northern hemisphere, and are most likely of Nearctic origin, but selected lineages have dispersed to the northern Neotropics and the Paleotropics. Thus the evolutionary history of the Myrmicinae has played out on a global stage over the last 100 Ma, with no single region being the principal generator of species diversity.

Phylogeny of Anophelinae (Diptera: Culicidae) based on nuclear ribosomal and mitochondrial DNA sequences

Abstract Phylogenetic relationships among thirty‐two species of mosquitoes in subfamily Anophelinae are inferred from portions of the mitochondrial genes COI and COII, the nuclear 18S small subunit rRNA gene and the expansion D2 region of the nuclear large subunit 28S rRNA gene. Sequences were obtained from the genera Anopheles, Bironella and Chagasia. Representatives of all six subgenera of Anopheles were included: Anopheles, Cellia, Kerteszia, Lophopodomyia, Nyssorhynchus and Stethomyia. Using parsimony and maximum likelihood methods, various combinations of these DNA sequence data were analysed separately: 18S, 28S, combined 18S and 28S, combined COI and COII, and combined 18S, 28S, COI and COII (‘total evidence’). The combined rDNA data contain strong phylogenetic signal, moderately to strongly supporting most clades in MP and ML analyses; however, the mtDNA data (analysed as either nucleotide or amino acid sequences) contain little phylogenetic signal, except for relationships of very recently derived groups of species and, at the deepest level, for the monophyly of Anophelinae. The paraphyly of Anopheles relative to Bironella is confirmed by most analyses and statistical tests. Support for the monophyly of subgenera Anopheles, Cellia, Kerteszia and Nyssorhynchus is indicated by most analyses. Subgenus Lophopodomyia is reconstructed as the sister to Bironella, nested within a clade also containing Nyssorhynchus and Kerteszia. The most basal relationships within genus Anopheles are not well resolved by any of the data partitions, although the results of statistical analyses of the rDNA data (S‐H‐tests, likelihood ratio tests for monophyly and Bayesian MCMC analyses) suggest that the clade consisting of Bironella, Lophopodomyia, Nyssorhynchus and Kerteszia is the sister to the clade containing Cellia and Anopheles.

Identifying the transition between single and multiple mating of queens in fungus-growing ants.

Obligate mating of females (queens) with multiple males has evolved only rarely in social Hymenoptera (ants, social bees, social wasps) and for reasons that are fundamentally different from those underlying multiple mating in other animals. The monophyletic tribe of ‘attin’) fungus–growing ants is known to include evolutionarily derived genera with obligate multiple mating (the Acromyrmex and Atta leafcutter ants) as well as phylogenetically basal genera with exclusively single mating (e.g. Apterostigma, Cyphomyrmex, Myrmicocrypta). All attine genera share the unique characteristic of obligate dependence on symbiotic fungus gardens for food, but the sophistication of this symbiosis differs considerably across genera. The lower attine genera generally have small, short–lived colonies and relatively non–specialized fungal symbionts (capable of living independently of their ant hosts), whereas the four evolutionarily derived higher attine genera have highly specialized, long–term clonal symbionts. In this paper, we investigate whether the transition from single to multiple mating occurred relatively recently in the evolution of the attine ants, in conjunction with the novel herbivorous ‘leafcutte’ niche acquired by the common ancestor of Acromyrmex and Atta, or earlier, at the transition to rearing specialized long–term clonal fungi in the common ancestor of the larger group of higher attines that also includes the genera Trachymyrmex and Sericomyrmex. We use DNA microsatellite analysis to provide unambiguous evidence for a single, late and abrupt evolutionary transition from exclusively single to obligatory multiple mating. This transition is historically correlated with other evolutionary innovations, including the extensive use of fresh vegetation as substrate for the fungus garden, a massive increase in mature colony size and morphological differentiation of the worker caste.

Phylogeny of Anophelinae (Diptera Culicidae) Based on Morphological Characters

Abstract Phylogenetic relationships of mosquitoes in the subfamily Anophelinae are presented based on a cladistic analysis of 163 morphological characters from females, males, fourth-instar larvae, and pupae of 64 species. Species examined include one Chagasia Cruz, three Bironella Theobald, and 60 species representing all six subgenera of Anopheles Meigen. Uranotaenia lowii Theobald and Aedeomyia squamipennis (Lynch Arribalzaga) are used as outgroups. This analysis indicates that Anophelinae is monophyletic, that Chagasia is the earliest-diverged lineage within Anophelinae, and that the genus Anopheles, as currently defined, is paraphyletic because it excludes Bironella. Four nonhomoplastic synapomorphies support the monophyly of the clade composed of the genera Bironella and Anopheles. Three major lineages are recognized within this clade. The basal lineage (lineage 1) contains An. (Nyssorhynchus), An. (Kerteszia), and An. implexus (Theobald). This analysis supports the monophyly of the sister groups Nyssorhynchus Blanchard and Kerteszia Theobald, but finds the Albimanus, Argyritarsis, and Myzorhynchella sections of the subgenus Nyssorhynchus to be paraphyletic. The second lineage (lineage 2) contains species of the subgenus Cellia Theobald, which is monophyletic. Except for the Cellia series, however, all other series of the subgenus Cellia are paraphyletic. The third lineage (lineage 3) contains species of the subgenera Anopheles Meigen, Stethomyia Theobald, Lophopodomyia Antunes, and of the genus Bironella. Bironella and Stethomyia are monophyletic sister groups. The Lophoscelomyia and Arribalzagia series are monophyletic. The Arribalzagia and Cycloleppteron series are sister groups nested within the Myzorhynchus series. We conclude that there is no support for the generic recognition of Bironella, nor the subgeneric rank of Lophopodomyia and Stethomyia.