RESUMEN
Fungus-farming ants cultivate multiple lineages of fungi for food, but, because fungal cultivar relationships are largely unresolved, the history of fungus-ant coevolution remains poorly known. We designed probes targeting >2000 gene regions to generate a dated evolutionary tree for 475 fungi and combined it with a similarly generated tree for 276 ants. We found that fungus-ant agriculture originated ~66 million years ago when the end-of-Cretaceous asteroid impact temporarily interrupted photosynthesis, causing global mass extinctions but favoring the proliferation of fungi. Subsequently, ~27 million years ago, one ancestral fungal cultivar population became domesticated, i.e., obligately mutualistic, when seasonally dry habitats expanded in South America, likely isolating the cultivar population from its free-living, wet forest-dwelling conspecifics. By revealing these and other major transitions in fungus-ant coevolution, our results clarify the historical processes that shaped a model system for nonhuman agriculture.
Asunto(s)
Hormigas , Coevolución Biológica , Hongos , Simbiosis , Animales , Agricultura , Hormigas/microbiología , Hormigas/genética , Domesticación , Hongos/genética , Hongos/clasificación , Fotosíntesis , Filogenia , América del SurRESUMEN
Leafcutter ants propagate co-evolving fungi for food. The nearly 50 species of leafcutter ants (Atta, Acromyrmex) range from Argentina to the United States, with the greatest species diversity in southern South America. We elucidate the biogeography of fungi cultivated by leafcutter ants using DNA sequence and microsatellite-marker analyses of 474 cultivars collected across the leafcutter range. Fungal cultivars belong to two clades (Clade-A and Clade-B). The dominant and widespread Clade-A cultivars form three genotype clusters, with their relative prevalence corresponding to southern South America, northern South America, Central and North America. Admixture between Clade-A populations supports genetic exchange within a single species, Leucocoprinus gongylophorus. Some leafcutter species that cut grass as fungicultural substrate are specialized to cultivate Clade-B fungi, whereas leafcutters preferring dicot plants appear specialized on Clade-A fungi. Cultivar sharing between sympatric leafcutter species occurs frequently such that cultivars of Atta are not distinct from those of Acromyrmex. Leafcutters specialized on Clade-B fungi occur only in South America. Diversity of Clade-A fungi is greatest in South America, but minimal in Central and North America. Maximum cultivar diversity in South America is predicted by the Kusnezov-Fowler hypothesis that leafcutter ants originated in subtropical South America and only dicot-specialized leafcutter ants migrated out of South America, but the cultivar diversity becomes also compatible with a recently proposed hypothesis of a Central American origin by postulating that leafcutter ants acquired novel cultivars many times from other nonleafcutter fungus-growing ants during their migrations from Central America across South America. We evaluate these biogeographic hypotheses in the light of estimated dates for the origins of leafcutter ants and their cultivars.
Asunto(s)
Agaricales/genética , Hormigas/microbiología , Coevolución Biológica , Animales , Hormigas/clasificación , América Central , Marcadores Genéticos , Genética de Población , Genotipo , Repeticiones de Microsatélite , América del Norte , Filogenia , Filogeografía , América del Sur , SimbiosisRESUMEN
We report the rediscovery of the exceedingly rarely collected and enigmatic fungus-farming ant species Mycetosoritis asper. Since the description of the type specimen in 1887, only four additional specimens are known to have been added to the world's insect collections. Its biology is entirely unknown and its phylogenetic position within the fungus-farming ants has remained puzzling due to its aberrant morphology. In 2014 we excavated and collected twenty-one colonies of M. asper in the Floresta Nacional de Chapecó in Santa Catarina, Brazil. We describe here for the first time the male and larva of the species and complement the previous descriptions of both the queen and the worker. We describe, also for the first time, M. asper biology, nest architecture, and colony demographics, and identify its fungal cultivar. Molecular phylogenetic analyses indicate that both M. asper and M. clorindae are members of the genus Cyphomyrmex, which we show to be paraphyletic as currently defined. More precisely, M. asper is a member of the Cyphomyrmex strigatus group, which we also show to be paraphyletic with respect to the genus Mycetophylax. Based on these results, and in the interest of taxonomic stability, we transfer the species M. asper, M. clorindae, and all members of the C. strigatus group to the genus Mycetophylax, the oldest available name for this clade. Based on ITS sequence data, Mycetophylax asper practices lower agriculture, cultivating a fungal species that belongs to lower-attine fungal Clade 2, subclade F.
Asunto(s)
Hormigas/clasificación , Conducta Animal/fisiología , Hongos , Filogenia , Animales , BrasilRESUMEN
The evolution of ant agriculture, as practised by the fungus-farming 'attine' ants, is thought to have arisen in the wet rainforests of South America about 55-65 Ma. Most subsequent attine agricultural evolution, including the domestication event that produced the ancestor of higher attine cultivars, is likewise hypothesized to have occurred in South American rainforests. The 'out-of-the-rainforest' hypothesis, while generally accepted, has never been tested in a phylogenetic context. It also presents a problem for explaining how fungal domestication might have occurred, given that isolation from free-living populations is required. Here, we use phylogenomic data from ultra-conserved element (UCE) loci to reconstruct the evolutionary history of fungus-farming ants, reduce topological uncertainty, and identify the closest non-fungus-growing ant relative. Using the phylogeny we infer the history of attine agricultural systems, habitat preference and biogeography. Our results show that the out-of-the-rainforest hypothesis is correct with regard to the origin of attine ant agriculture; however, contrary to expectation, we find that the transition from lower to higher agriculture is very likely to have occurred in a seasonally dry habitat, inhospitable to the growth of free-living populations of attine fungal cultivars. We suggest that dry habitats favoured the isolation of attine cultivars over the evolutionary time spans necessary for domestication to occur.
Asunto(s)
Hormigas/fisiología , Evolución Biológica , Ecosistema , Hongos/fisiología , Simbiosis , Animales , Hormigas/genética , Domesticación , Proteínas de Insectos/genética , Filogenia , Bosque Lluvioso , Análisis de Secuencia de ADN , América del SurRESUMEN
The genus Simopelta consists of 21 described species restricted to Central America and South America. The present study describes a new cryptobiotic species, Simopelta anomma sp. nov.. The new species is blind, possesses a 3-segmented antennal club, and has the midtibia with several stout setae, a combination of characters unique within the genus. Moreover, some traits of this species require broadening the definition of the genus. The discovery of S. anomma sp. nov. suggests that many undiscovered species, some of which may be important for understanding ant evolution, remain hidden below ground in Neotropical rainforests.
Asunto(s)
Hormigas/clasificación , Distribución Animal , Estructuras Animales/anatomía & histología , Estructuras Animales/crecimiento & desarrollo , Animales , Hormigas/anatomía & histología , Hormigas/crecimiento & desarrollo , Evolución Biológica , Tamaño Corporal , Brasil , Costa Rica , Tamaño de los Órganos , Bosque LluviosoRESUMEN
Fungus-farming (attine) ant agriculture is made up of five known agricultural systems characterized by remarkable symbiont fidelity in which five phylogenetic groups of ants faithfully cultivate five phylogenetic groups of fungi. Here we describe the first case of a lower-attine ant cultivating a higher-attine fungus based on our discovery of a Brazilian population of the relictual fungus-farming ant Apterostigma megacephala, known previously from four stray specimens from Peru and Colombia. We find that A. megacephala is the sole surviving representative of an ancient lineage that diverged â¼39 million years ago, very early in the â¼55-million-year evolution of fungus-farming ants. Contrary to all previously known patterns of ant-fungus symbiont fidelity, A. megacephala cultivates Leucoagaricus gongylophorus, a highly domesticated fungal cultivar that originated only 2-8 million years ago in the gardens of the highly derived and recently evolved (â¼12 million years ago) leaf-cutting ants. Because no other lower fungus-farming ant is known to cultivate any of the higher-attine fungi, let alone the leaf-cutter fungus, A. megacephala may provide important clues about the biological mechanisms constraining the otherwise seemingly obligate ant-fungus associations that characterize attine ant agriculture.
Asunto(s)
Hormigas/fisiología , Basidiomycota/fisiología , Animales , Hormigas/genética , Secuencia de Bases , Basidiomycota/genética , Evolución Biológica , Brasil , Funciones de Verosimilitud , Datos de Secuencia Molecular , Filogenia , SimbiosisRESUMEN
Cyatta abscondita, a new genus and species of fungus-farming ant from Brazil, is described based on morphological study of more than 20 workers, two dealate gynes, one male, and two larvae. Ecological field data are summarized, including natural history, nest architecture, and foraging behavior. Phylogenetic analyses of DNA sequence data from four nuclear genes indicate that Cyatta abscondita is the distant sister taxon of the genus Kalathomyrmex, and that together they comprise the sister group of the remaining neoattine ants, an informal clade that includes the conspicuous and well-known leaf-cutter ants. Morphologically, Cyatta abscondita shares very few obvious character states with Kalathomyrmex. It does, however, possess a number of striking morphological features unique within the fungus-farming tribe Attini. It also shares morphological character states with taxa that span the ancestral node of the Attini. The morphology, behavior, and other biological characters of Cyatta abscondita are potentially informative about plesiomorphic character states within the fungus-farming ants and about the early evolution of ant agriculture.
Asunto(s)
Hormigas/clasificación , Animales , Hormigas/anatomía & histología , Hormigas/genética , Evolución Biológica , Brasil , Femenino , Genes de Insecto , Geografía , Masculino , Datos de Secuencia Molecular , Comportamiento de Nidificación , FilogeniaRESUMEN
Workers of the ant Carebarella bicolor collected in Panama were found to have two major poison-frog alkaloids, cis- and trans-fused decahydroquinolines (DHQs) of the 269AB type, four minor 269AB isomers, two minor 269B isomers, and three isomers of DHQ 271D. For the first time in an ant, however, the DHQs were accompanied by six histrionicotoxins (HTXs), viz., 283A, 285A, 285B, 285C, 287A, and 287D. This co-occurrence of the HTX and DHQ alkaloids is the usual pattern seen in dendrobatid frogs. This finding contrasts with our earlier study, where workers of a Brazilian ant, Solenopsis (Diplorhoptrum) sp., were found to have a very similar DHQ complex but failed to show HTXs. Several new DHQ alkaloids of MW 271 (named in the frog as 271G) are reported from the above ants that have both m/z 202 and 204 as major fragment ions, unlike the spectrum seen for the poison-frog alkaloid 271D, which has only an m/z 204 base peak. Found also for the first time in skin extracts from the comparison frog Oophaga granulifera of Costa Rica is a trace DHQ of MW 273. It is coded as 273F in the frog; a different isomer is found in the ant.
Asunto(s)
Alcaloides/aislamiento & purificación , Alcaloides/farmacología , Venenos de Anfibios/aislamiento & purificación , Venenos de Anfibios/farmacología , Hormigas/química , Anuros/metabolismo , Venenos , Quinolinas/aislamiento & purificación , Quinolinas/farmacología , Alcaloides/química , Venenos de Anfibios/química , Animales , Brasil , Costa Rica , Estructura Molecular , Panamá , Quinolinas/química , Piel/efectos de los fármacos , EstereoisomerismoRESUMEN
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.