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.
Abstract. Ants in the Neotropical genus Sericomyrmex Mayr cultivate fungi for food. Both ants and fungi are obligate, coevolved symbionts. The taxonomy of Sericomyrmex is problematic because the morphology of the worker caste is generally homogeneous across all of the species within the genus, species limits are vague, and the relationships between them are unknown. We used ultraconserved elements (UCEs) as genome-scale markers to reconstruct evolutionary history and to infer species boundaries in Sericomyrmex. We recovered an average of ∼990 UCE loci for 88 Sericomyrmex samples from across the geographical range of the genus as well as for five outgroup taxa. Using maximum likelihood and species-tree approaches, we recovered nearly identical topologies across datasets with 50-95% matrix completeness. We identify nine species-level lineages in Sericomyrmex, including two new species. This is less than the previously described 19 species, even accounting for two species for which we had no UCE samples, which brings the total number of Sericomyrmex species to 11. Divergence-dating analyses recovered 4.3 Ma as the crown-group age estimates for Sericomyrmex, indicating a recent, rapid radiation. We also sequenced mitochondrial cytochrome oxidase subunit I (COI) for 125 specimens. Resolution and support for clades in our COI phylogeny are weak, indicating that COI is not an appropriate species-delimitation tool. However, taxa within species consistently cluster together, suggesting that COI is useful as a species identification ('DNA barcoding') tool. We also sequenced internal transcribed spacer (ITS) and large subunit (LSU) for 32 Sericomyrmex fungal cultivars. The fungal phylogeny confirms that Sericomyrmex fungi are generalized higher-attine cultivars, interspersed with Trachymyrmex-associated fungal species, indicating cultivar sharing and horizontal transfer between these two genera. Our results indicate that UCEs offer immense potential for delimiting and resolving relationships of problematic, recently diverged species.
Although calcareous anatomical structures have evolved in diverse animal groups, such structures have been unknown in insects. Here, we report the discovery of high-magnesium calcite [CaMg(CO3)2] armor overlaying the exoskeletons of major workers of the leaf-cutter ant Acromyrmex echinatior. Live-rearing and in vitro synthesis experiments indicate that the biomineral layer accumulates rapidly as ant workers mature, that the layer is continuously distributed, covering nearly the entire integument, and that the ant epicuticle catalyzes biomineral nucleation and growth. In situ nanoindentation demonstrates that the biomineral layer significantly hardens the exoskeleton. Increased survival of ant workers with biomineralized exoskeletons during aggressive encounters with other ants and reduced infection by entomopathogenic fungi demonstrate the protective role of the biomineral layer. The discovery of biogenic high-magnesium calcite in the relatively well-studied leaf-cutting ants suggests that calcareous biominerals enriched in magnesium may be more common in metazoans than previously recognized.
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.
Fungus-farming ("attine") ants are model systems for studies of symbiosis, coevolution, and advanced eusociality. A New World clade of nearly 300 species in 15 genera, all attine ants cultivate fungal symbionts for food. In order to better understand the evolution of ant agriculture, we sequenced, assembled, and analyzed transcriptomes of four different attine ant species in two genera: three species in the higher-attine genus Sericomyrmex and a single lower-attine ant species, Apterostigma megacephala, representing the first genomic data for either genus. These data were combined with published genomes of nine other ant species and the honey bee Apis mellifera for phylogenomic and divergence-dating analyses. The resulting phylogeny confirms relationships inferred in previous studies of fungus-farming ants. Divergence-dating analyses recovered slightly older dates than most prior analyses, estimating that attine ants originated 53.6–66.7 million of years ago, and recovered a very long branch subtending a very recent, rapid radiation of the genus Sericomyrmex. This result is further confirmed by a separate analysis of the three Sericomyrmex species, which reveals that 92.71% of orthologs have 99% - 100% pairwise-identical nucleotide sequences. We searched the transcriptomes for genes of interest, most importantly argininosuccinate synthase and argininosuccinate lyase, which are functional in other ants but which are known to have been lost in seven previously studied attine ant species. Loss of the ability to produce the amino acid arginine has been hypothesized to contribute to the obligate dependence of attine ants upon their cultivated fungi, but the point in fungus-farming ant evolution at which these losses occurred has remained unknown. We did not find these genes in any of the sequenced transcriptomes. Although expected for Sericomyrmex species, the absence of arginine anabolic genes in the lower-attine ant Apterostigma megacephala strongly suggests that the loss coincided with the origin of attine ants.
This article went through editorial changes (Tables 1 and 2 as well as references) after publication online and before publication in print. Following a trend of inovations in the scientific journal editorial management, instead of publishing an erratum, the current version (named Version 1) was kept online, along with a second one (named Version 2). Locating, collecting, and maintaining colonies of fungus-farming ants (Hymenoptera: Formicidae: Myrmicinae: Attini) Introduction The fungus-farming ants (Myrmicinae: Attini: Atta species group; herein referred to as "attine" ants, sensu Ward et al. (2015) are a monophyletic group, exclusively New World and primarily Neotropical in distribution, consisting of >250 described species as well as many more awaiting discovery and description (Brandão & Mayhé-Nunes, 2001;
Xerolitor, a new, monotypic genus of fungus‐growing ants, is described to accommodate the phylogenetically isolated, relict species Mycetosoritis explicatus Kempf. We also diagnose the male and the larva of Xerolitor explicatus (Kempf) comb.n. and report ecological observations for the species, including nest architecture and foraging behaviour. Xerolitor explicatus comb.n. inhabits the dry habitats of the Brazilian Cerrado and the Bolivian and Paraguayan Gran Chaco. Bayesian multilocus phylogenetic analyses indicate that X. explicatus comb.n. is, contrary to some prior hypotheses, a member of the ‘higher’ fungus‐growing ants and the sister taxon of the genus Sericomyrmex Mayr. Results from phylogenetic analyses of the fungal cultivar grown by X. explicatus comb.n. in Paraguay, as well as the presence of gongylidia, indicate that the fungal mutualist is a member of the clade of higher fungal cultivar species and that it is probably the same species cultivated by some Trachymyrmex Forel and Sericomyrmex species.
The genus Sericomyrmex Mayr (Formicidae: Myrmicinae: Attini) is a Neotropical group of fungus-farming ants known for its problematic taxonomy, caused by low morphological variability across the species, vague and old species descriptions, and an outdated and incomplete key published in 1916. Recent molecular studies revealed that Sericomyrmex is the product of a rapid recent radiation, with a divergence date of 4.3 million years ago. Here we present a comprehensive taxonomic revision of the genus Sericomyrmex based on morphology and a recently published molecular phylogeny. We discuss and illustrate morphological characters for Sericomyrmex workers, males, queens, and larvae. We report 18 standard morphological measurements and 5 indices for 529 workers, 50 queens, and 39 males, which we employ in morphometric analyses. The revised genus Sericomyrmex comprises eleven species, including three new species, here described as S. maravalhas sp. n., S. radioheadi sp. n., and S. saramama sp. n. We also redescribe S. amabilis Wheeler, S. bondari Borgmeier, S. lutzi Wheeler, S. mayri Forel, S. opacus Mayr, S. parvulus Forel, S. saussurei Emery, and S. scrobifer Forel. The number of recognized species (11) is lower than the previously recognized 19 species and 3 subspecies. The following species and subspecies are synonymized: under S. opacus [=S. aztecus Forel syn. n., S. zacapanus Wheeler syn. n., and S. diego Forel syn. n.]; under S. bondari [=S. beniensis Weber syn. n.]; under S. mayri [=S. luederwaldti Santschi syn. n., S. moreirai Santschi syn. n., S. harekulli Weber syn. n., S. harekulli arawakensis Weber syn. n., S. urichi Forel syn. n.]; under S. saussurei [=S. burchelli Forel syn. n., S. impexus Wheeler syn. n., S. urichi maracas Weber syn. n.]; and under S. parvulus [=S. myersi Weber syn. n.]. We provide a key to Sericomyrmex species for the worker caste and information on the geographic distributions of all species.
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