Scott E. Solomon

Paleodistributions and Comparative Molecular Phylogeography of Leafcutter Ants (Atta spp.) Provide New Insight into the Origins of Amazonian Diversity

The evolutionary basis for high species diversity in tropical regions of the world remains unresolved. Much research has focused on the biogeography of speciation in the Amazon Basin, which harbors the greatest diversity of terrestrial life. The leading hypotheses on allopatric diversification of Amazonian taxa are the Pleistocene refugia, marine incursion, and riverine barrier hypotheses. Recent advances in the fields of phylogeography and species-distribution modeling permit a modern re-evaluation of these hypotheses. Our approach combines comparative, molecular phylogeographic analyses using mitochondrial DNA sequence data with paleodistribution modeling of species ranges at the last glacial maximum (LGM) to test these hypotheses for three co-distributed species of leafcutter ants (Atta spp.). The cumulative results of all tests reject every prediction of the riverine barrier hypothesis, but are unable to reject several predictions of the Pleistocene refugia and marine incursion hypotheses. Coalescent dating analyses suggest that population structure formed recently (Pleistocene-Pliocene), but are unable to reject the possibility that Miocene events may be responsible for structuring populations in two of the three species examined. The available data therefore suggest that either marine incursions in the Miocene or climate changes during the Pleistocene—or both—have shaped the population structure of the three species examined. Our results also reconceptualize the traditional Pleistocene refugia hypothesis, and offer a novel framework for future research into the area.

Evolution of cold-tolerant fungal symbionts permits winter fungiculture by leafcutter ants at the northern frontier of a tropical ant-fungus symbiosis.

The obligate mutualism between leafcutter ants and their Attamyces fungi originated 8 to 12 million years ago in the tropics, but extends today also into temperate regions in South and North America. The northernmost leafcutter ant Atta texana sustains fungiculture during winter temperatures that would harm the cold-sensitive Attamyces cultivars of tropical leafcutter ants. Cold-tolerance of Attamyces cultivars increases with winter harshness along a south-to-north temperature gradient across the range of A. texana, indicating selection for cold-tolerant Attamyces variants along the temperature cline. Ecological niche modeling corroborates winter temperature as a key range-limiting factor impeding northward expansion of A. texana. The northernmost A. texana populations are able to sustain fungiculture throughout winter because of their cold-adapted fungi and because of seasonal, vertical garden relocation (maintaining gardens deep in the ground in winter to protect them from extreme cold, then moving gardens to warmer, shallow depths in spring). Although the origin of leafcutter fungiculture was an evolutionary breakthrough that revolutionized the food niche of tropical fungus-growing ants, the original adaptations of this host-microbe symbiosis to tropical temperatures and the dependence on cold-sensitive fungal symbionts eventually constrained expansion into temperate habitats. Evolution of cold-tolerant fungi within the symbiosis relaxed constraints on winter fungiculture at the northern frontier of the leafcutter ant distribution, thereby expanding the ecological niche of an obligate host–microbe symbiosis.

Phylogeny of leafcutter ants in the genus Atta Fabricius (Formicidae: Attini) based on mitochondrial and nuclear DNA sequences

Leafcutting ants of the genus Atta are the most conspicuous members of the tribe Attini, the fungus-growing ants. Atta species have long attracted the attention of naturalists, and have since become a common model system for the study of complex insect societies as well as for the study of coevolutionary dynamics due to their numerous interactions with fungi and other microbes. Nevertheless, systematics and taxonomy of the 15 species in the genus Atta have proven challenging, due in part to the extreme levels of worker polymorphism these species display, leading to disagreements about the validity of as many as five different subgenera and calling into question the monophyly of the genus. Here, we use DNA sequence information from fragments of three mitochondrial genes (COI, tRNA leucine and COII) and one nuclear gene (EF1-alphaF1), totaling 1070 base pairs, to reconstruct the phylogenetic relationships of Atta species using maximum parsimony, maximum likelihood and Bayesian inference techniques. Our results provide support for monophyly of the genus Atta, and suggest that the genus is divided into four monophyletic groups, which correspond to four of the five previously erected Atta subgenera: Atta sensu stricto and Archeatta, each with species composition identical to earlier proposals; Neoatta and Epiatta, with major differences in species composition from earlier proposals. The current geographic ranges of these species suggest that the historical separation of South America from Central and North America has played a role in speciation within this genus.

Nuclear mitochondrial-like sequences in ants: evidence from Atta cephalotes (Formicidae: Attini)

Nuclear mitochondrial‐like sequences (numts) are copies of mitochondrial DNA that have migrated to the genomic DNA. We present the first characterization of numts in ants, these numts being homologues to a mitochondrial DNA fragment containing loci the 3′ portion of the cytochrome oxidase I gene, an intergenic spacer, the tRNA leucine gene and the 5′ portion of the cytochrome oxidase II gene. All 67 specimens of Atta cephalotes (Hymenoptera: Formicidae: Attini) investigated had these homologues, which are within two monophyletic groups that we called numt1 and numt2. Numt1 and numt2 sequences are less variable than mitochondrial sequences and released from the severe purifying selection constraining the evolution of mitochondrial genes. Their formation probably involved bottlenecks related to two distinct transfer events of ancient and fast evolving mitochondrial DNA fragments to comparative slowly evolving nuclear DNA regions.

Frontier mutualism: coevolutionary patterns at the northern range limit of the leaf-cutter ant–fungus symbiosis

Tropical leaf-cutter ants cultivate the fungus Attamyces bromatificus in a many-to-one, diffuse coevolutionary relationship where ant and fungal partners re-associate frequently over time. To evaluate whether ant–Attamyces coevolution is more specific (tighter) in peripheral populations, we characterized the host-specificities of Attamyces genotypes at their northern, subtropical range limits (southern USA, Mexico and Cuba). Population-genetic patterns of northern Attamyces reveal features that have so far not been observed in the diffusely coevolving, tropical ant–Attamyces associations. These unique features include (i) cases of one-to-one ant–Attamyces specialization that tighten coevolution at the northern frontier; (ii) distributions of genetically identical Attamyces clones over large areas (up to 81 000 km2, approx. the area of Ireland, Austria or Panama); (iii) admixture rates between Attamyces lineages that appear lower in northern than in tropical populations; and (iv) long-distance gene flow of Attamyces across a dispersal barrier for leaf-cutter ants (ocean between mainland North America and Cuba). The latter suggests that Attamyces fungi may occasionally disperse independently of the ants, contrary to the traditional assumption that Attamyces fungi depend entirely on leaf-cutter queens for dispersal. Peripheral populations in Argentina or at mid-elevation sites in the Andes may reveal additional regional variants in ant–Attamyces coevolution. Studies of such populations are most likely to inform models of coextinctions of obligate mutualistic partners that are doubly stressed by habitat marginality and by environmental change.

Nesting biology of the fungus growing ants Mycetarotes Emery (Attini, Formicidae)

Summary.Fungus-growing ants of the genus Mycetarotes are among the least studied in the tribe Attini. This report documents nest architecture and worker population numbers for 19 nests of M. parallelus and 5 nests of M. acutus, including the first such report for M. acutus. This new information is integrated with the scant biological information reported on Mycetarotes to date. The resulting picture of Mycetarotes life history, as well as the relative ease with which large numbers of nests can be collected and observed in the field, suggest that Mycetarotes (particularly M. parallelus) is an ideal model system for the study of coevolution of lower-attine ants and their cultivated fungi.

Nesting biology and fungiculture of the fungus-growing ant, Mycetagroicus cerradensis: New light on the origin of higher-attine agriculture

Abstract The genus Mycetagroicus is perhaps the least known of all fungus-growing ant genera, having been first described in 2001 from museum specimens. A recent molecular phylogenetic analysis of the fungus-growing ants demonstrated that Mycetagroicus is the sister to all higher attine ants (Trachymyrmex, Sericomyrmex, Acromyrmex, Pseudoatta, and Atta), making it of extreme importance for understanding the transition between lower and higher attine agriculture. Four nests of Mycetagroicus cerradensis near Uberlândia, Minas Gerais, Brazil were excavated, and fungus chambers for one were located at a depth of 3.5 meters. Based on its lack of gongylidia (hyphal-tip swellings typical of higher attine cultivars), and a phylogenetic analysis of the ITS rDNA gene region, M. cerradensis cultivates a lower attine fungus in Clade 2 of lower attine (G3) fungi. This finding refines a previous estimate for the origin of higher attine agriculture, an event that can now be dated at approximately 21–25 mya in the ancestor of extant species of Trachymyrmex and Sericomyrmex.

New Light on the Systematics of Fungi Associated with Attine Ant Gardens and the Description of Escovopsis kreiselii sp. nov.

Since the formal description of fungi in the genus Escovopsis in 1990, only a few studies have focused on the systematics of this group. For more than two decades, only two Escovopsis species were described; however, in 2013, three additional Escovopsis species were formally described along with the genus Escovopsioides, both found exclusively in attine ant gardens. During a survey for Escovopsis species in gardens of the lower attine ant Mycetophylax morschi in Brazil, we found four strains belonging to the pink-colored Escovopsis clade. Careful examination of these strains revealed significant morphological differences when compared to previously described species of Escovopsis and Escovopsioides. Based on the type of conidiogenesis (sympodial), as well as morphology of conidiogenous cells (percurrent), non-vesiculated conidiophores, and DNA sequences, we describe the four new strains as a new species, Escovopsis kreiselii sp. nov. Phylogenetic analyses using three nuclear markers (Large subunit RNA; translation elongation factor 1-alpha; and internal transcribed spacer) from the new strains as well as available sequences in public databases confirmed that all known fungi infecting attine ant gardens comprise a monophyletic group within the Hypocreaceae family, with very diverse morphological characteristics. Specifically, Escovopsis kreiselii is likely associated with gardens of lower-attine ants and its pathogenicity remains uncertain.

THE ANT (HYMENOPTERA: FORMICIDAE) FAUNA OF COCOS ISLAND, COSTA RICA

Abstract Cocos Island, Costa Rica is a 24-square kilometer volcanic island in the tropical eastern Pacific Ocean, located approximately 480 kilometers from the mainland. Despite its biogeographic significance, much of the entomofauna have not been systematically surveyed. A detailed survey of the ant (Hymenoptera: Formicidae) fauna of this island was conducted over a three-week period. The results suggest that, despite the relatively minor presence of humans on Cocos, much of the ant fauna is dominated by non-native species. Furthermore, the current ant community is substantially different from that described by previous expeditions. One of the previously described endemics, Camponotus biolleyi Forel, was not found during the survey. A species known to be invasive, Wasmannia auropunctata Roger, was found in extremely high abundance near disturbed sites, but was not present in more pristine habitats. Furthermore, this population displays intraspecific aggression, which is uncommon among invasive ants, including other invasive populations of this species.

Shared Escovopsis parasites between leaf-cutting and non-leaf-cutting ants in the higher attine fungus-growing ant symbiosis

Fungus-gardening (attine) ants grow fungus for food in protected gardens, which contain beneficial, auxiliary microbes, but also microbes harmful to gardens. Among these potentially pathogenic microorganisms, the most consistently isolated are fungi in the genus Escovopsis, which are thought to co-evolve with ants and their cultivar in a tripartite model. To test clade-to-clade correspondence between Escovopsis and ants in the higher attine symbiosis (including leaf-cutting and non-leaf-cutting ants), we amassed a geographically comprehensive collection of Escovopsis from Mexico to southern Brazil, and reconstructed the corresponding Escovopsis phylogeny. Contrary to previous analyses reporting phylogenetic divergence between Escovopsis from leafcutters and Trachymyrmex ants (non-leafcutter), we found no evidence for such specialization; rather, gardens from leafcutters and non-leafcutters genera can sometimes be infected by closely related strains of Escovopsis, suggesting switches at higher phylogenetic levels than previously reported within the higher attine symbiosis. Analyses identified rare Escovopsis strains that might represent biogeographically restricted endemic species. Phylogenetic patterns correspond to morphological variation of vesicle type (hyphal structures supporting spore-bearing cells), separating Escovopsis with phylogenetically derived cylindrical vesicles from ancestral Escovopsis with globose vesicles. The new phylogenetic insights provide an improved basis for future taxonomic and ecological studies of Escovopsis.