Metabolism And The Rise Of Fungus Cultivation By Ants

Most ant colonies are comprised of workers that cooperate to harvest resources and feed developing larvae. Around 50 million years ago (MYA), ants of the attine lineage adopted an alternative strategy, harvesting resources used as compost to produce fungal gardens. While fungus cultivation is considered a major breakthrough in ant evolution, the associated ecological consequences remain poorly understood. Here, we compare the energetics of attine colony-farms and ancestral hunter-gatherer colonies using metabolic scaling principles within a phylogenetic context. We find two major energetic transitions. First, the earliest lower-attine farmers transitioned to lower mass-specific metabolic rates while shifting significant fractions of biomass from ant tissue to fungus gardens. Second, a transition 20 MYA to specialized cultivars in the higher-attine clade was associated with increased colony metabolism (without changes in garden fungal content) and with metabolic scaling nearly identical to hypometry observed in hunter-gatherer ants, although only the hunter-gatherer slope was distinguishable from isometry. Based on these evolutionary transitions, we propose that shifting living-tissue storage from ants to fungal mutualists provided energetic storage advantages contributing to attine diversification and outline critical assumptions that, when tested, will help link metabolism, farming efficiency, and colony fitness.Integrative Biolog

Potential Distribution of Six North American Higher-Attine Fungus-Farming Ant (Hymenoptera: Formicidae) Species

Ants are among the most successful insects in Earth’s evolutionary history. However, there is a lack of knowledge regarding range-limiting factors that may influence their distribution. The goal of this study was to describe the environmental factors (climate and soil types) that likely impact the ranges of five out of the eight most abundant Trachymyrmex species and the most abundant Mycetomoellerius species in the United States. Important environmental factors may allow us to better understand each species’ evolutionary history. We generated habitat suitability maps using MaxEnt for each species and identified associated most important environmental variables. We quantified niche overlap between species and evaluated possible congruence in species distribution. In all but one model, climate variables were more important than soil variables. The distribution of M. turrifex (Wheeler, W.M., 1903) was predicted by temperature, specifically annual mean temperature (BIO1), T. arizonensis (Wheeler, W.M., 1907), T. carinatus, and T. smithi Buren, 1944 were predicted by precipitation seasonality (BIO15), T. septentrionalis (McCook, 1881) were predicted by precipitation of coldest quarter (BIO19), and T. desertorum (Wheeler, W.M., 1911) was predicted by annual flood frequency. Out of 15 possible pair-wise comparisons between each species’ distributions, only one was statistically indistinguishable (T. desertorum vs T. septentrionalis). All other species distribution comparisons show significant differences between species. These models support the hypothesis that climate is a limiting factor in each species distribution and that these species have adapted to temperatures and water availability differently

Data from: Sex at the margins: parthenogenesis vs. facultative and obligate sex in a Neotropical ant

Geographic parthenogenesis is a distribution pattern, in which parthenogenetic populations tend to live in marginal habitats, at higher latitudes and altitudes and island-like habitats compared with the sexual forms. The facultatively parthenogenetic ant Platythyrea punctata is thought to exhibit this general pattern throughout its wide range in Central America and the Caribbean Islands. Workers of P. punctata from the Caribbean produce diploid female offspring from unfertilized eggs by thelytokous parthenogenesis, and mated females and males are rare. In contrast, workers in one colony from Costa Rica were incapable of thelytoky; instead mated workers produced all female offspring. Because sample sizes were very low in former studies, we here use microsatellite markers and explicit tests of thelytoky to examine the population genetic structure of ancestral and derived populations of P. punctata throughout the Caribbean and Central America. Populations from the Caribbean islands were fully capable of parthenogenesis and population genetic signatures indicate that this is the predominant mode of reproduction, although males are occasionally produced. In contrast, the northernmost population on the mainland (Texas) showed signatures of sexual reproduction and individuals were incapable of reproduction by thelytoky. Contrary to expectations from a geographic parthenogenesis distribution pattern, most parts of the mainland populations were found to be facultatively thelytokous, with population genetic signatures of both sexual and parthenogenetic reproduction

Symbiosis, dysbiosis and the impact of horizontal exchange on bacterial microbiomes in higher fungus-gardening ants

Abstract Advances in our understanding of symbiotic stability have demonstrated that microorganisms are key to understanding the homeostasis of obligate symbioses. Fungus-gardening ants are excellent model systems for exploring how microorganisms may be involved in symbiotic homeostasis as the host and symbionts are macroscopic and can be easily experimentally manipulated. Their coevolutionary history has been well-studied; examinations of which have depicted broad clade-to-clade specificity between the ants and fungus. Few studies hitherto have addressed the roles of microbiomes in stabilizing these associations. Here, we quantified changes in microbiome structure as a result of experimentally induced horizontal exchange of symbionts. This was done by performing cross-fostering experiments forcing ants to grow novel fungi and comparing known temporally unstable (undergoing dysbiosis) and stable combinations. We found that fungus-gardening ants alter their unstable, novel garden microbiomes into configurations like those found in native gardens. Patterns of dysbiosis/symbiosis appear to be predictable in that two related species with similar specificity patterns also show similar patterns of microbial change, whereas a species with more relaxed specificity does not show such microbiome change or restructuring when growing different fungi. It appears that clade-to-clade specificity patterns are the outcomes of community-level interactions that promote stability or cause symbiotic collapse

Excavation of a <i>Trachymyrmex septentrionalis</i> in progress, showing other screen-bottom cages with planted colonies.

<p>Colonies were planted in the cages in April 2015 and excavated in November 2015, at which time nine of the ten colonies survived. Written consent to use the images of these individuals was obtained.</p

Summary of the weight of backfill deposited in each host layer, and its layer of origin.

<p>The area of the circles is proportional to the weight of sand, with the largest circle representing 286 g. Backfill originating within the same host layer as deposition was excluded from these calculations. Upward displacement greatly exceeded downward displacement, with greatest deposition tending to be in the next higher layer. "Native" was the sand weight of deposits that could not be accounted for as the diluent in the colored mixtures. Purple and yellow were combined because they occupied the same depth.</p

Displacement distance (cm) of the average backfilled grain of sand in relation to the depth at which it was deposited.

<p>The host color in which the grain was deposited is shown as the color of the symbols. Displacement was calculated from the mean depth of each host layer and the depth-source of each color of backfill. Most of the backfill was displaced upward, and displacement was greater for backfill originating from deeper host layers.</p

Data from: Metabolism and the rise of fungus cultivation by ants

Most ant colonies are comprised of workers that cooperate to harvest resources and feed developing larvae. Around 50 million years ago (MYA), ants of the attine lineage adopted an alternative strategy, harvesting resources used as compost to produce fungal gardens. While fungus cultivation is considered a major breakthrough in ant evolution, the associated ecological consequences remain poorly understood. Here, we compare the energetics of attine colony-farms and ancestral hunter-gatherer colonies using metabolic scaling principles within a phylogenetic context. We find two major energetic transitions. First, the earliest lower-attine farmers transitioned to lower mass-specific metabolic rates while shifting significant fractions of biomass from ant tissue to fungus gardens. Second, a transition 20 MYA to specialized cultivars in the higher-attine clade was associated with increased colony metabolism (without changes in garden fungal content) and with metabolic scaling nearly identical to hypometry observed in hunter-gatherer ants, although only the hunter-gatherer slope was distinguishable from isometry. Based on these evolutionary transitions, we propose that shifting living-tissue storage from ants to fungal mutualists provided energetic storage advantages contributing to attine diversification and outline critical assumptions that, when tested, will help link metabolism, farming efficiency, and colony fitness