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1. Welcome to the Atta world: A framework for understanding the effects of leaf‐cutter ants on ecosystem functions

   https://doi.org/10.1111/1365-2435.13319  

   Swanson, Amanda C. ; Schwendenmann, Luitgard ; Allen, Michael F. ; Aronson, Emma L. ; Artavia‐León, Allan ; Dierick, Diego ; Fernandez‐Bou, Angel S. ; Harmon, Thomas C. ; Murillo‐Cruz, Catalina ; Oberbauer, Steven F. ; et al ( March 2019 , Functional Ecology)

   Leaf‐cutter ants are a prominent feature in Neotropical ecosystems, but a comprehensive assessment of their effects on ecosystem functions is lacking. We reviewed the literature and used our own recent findings to identify knowledge gaps and develop a framework to quantify the effects of leaf‐cutter ants on ecosystem processes.

   Leaf‐cutter ants disturb the soil structure during nest excavation changing soil aeration and temperature. They mix relatively nutrient‐poor soil from deeper layers with the upper organic‐rich layers increasing the heterogeneity of carbon and nutrients within nest soils.

   Leaf‐cutter ants account for about 25% of all herbivory in Neotropical forest ecosystems, moving 10%–15% of leaves in their foraging range to their nests. Fungal symbionts transform the fresh, nutrient‐rich vegetative material to produce hyphal nodules to feed the ants. Organic material from roots and arbuscular mycorrhizal fungi enhances carbon and nutrient turnover in nest soils and creates biogeochemical hot spots. Breakdown of organic matter, microbial and ant respiration, and nest waste material decomposition result in increased CO₂, CH_4,and N₂O production, but the build‐up of gases and heat within the nest is mitigated by the tunnel network ventilation system. Nest ventilation dynamics are challenging to measure without bias, and improved sensor systems would likely solve this problem.

   Canopy gaps above leaf‐cutter ant nests change the light, wind and temperature regimes, which affects ecosystem processes. Nests differ in density and size depending on colony age, forest type and disturbance level and change over time resulting in spatial and temporal changes of ecosystem processes. These characteristics remain a challenge to evaluate rapidly and non‐destructively.

   Addressing the knowledge gaps identified in this synthesis will bring insights into physical and biological processes driving biogeochemical cycles at the nest and ecosystem scale and will improve our understanding of ecosystem biogeochemical heterogeneity and larger scale ecological phenomena.

   Aplain language summaryis available for this article.

    

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2. 28 minutes later: investigating the role of aflatrem-like compounds in Ophiocordyceps parasite manipulation of zombie ants

   https://doi.org/10.1016/j.anbehav.2023.06.011  

   Beckerson, William C. ; Krider, Courtney ; Mohammad, Umar A. ; de Bekker, Charissa ( September 2023 , Animal Behaviour)

   Coevolutionary relationships between parasites and their hosts can lead to the emergence of diverse phenotypes over time, as seen in Ophiocordyceps fungi that manipulate insect and arachnid behaviour to aid fungal spore transmission. The most conspicuous examples are found in ants of the Camponotini tribe, colloquially known as ‘zombie ants’. While the behaviours induced during infection are well described, their molecular underpinnings remain unknown. Recent genomics and transcriptomics ana- lyses of Ophiocordyceps camponoti-floridani have identified several highly upregulated biomolecules produced by the fungus during infection of Camponotus floridanus. Among them is an ergot alkaloid related to the mycotoxin aflatrem, known to cause ‘staggers syndrome’ in cows. Staggering, defined as unsteady movements side to side, is also observed in C. floridanus ants during late-stage infection. To test whether aflatrem-like compounds could be responsible, we injected healthy ants with aflatrem and recorded their behaviour for 30 min. Using both the automated object-tracking software MARGO and manual behavioural quantification, we found that aflatrem reduced ant activity and speed and increased staggering behaviours. To examine underlying transcriptomic changes, we performed RNA-seq on the heads of aflatrem-injected ants, keeping in step with previous transcriptomic work on Ophiocordyceps- manipulated ants. We identified 261 genes that were significantly dysregulated in the aflatrem-injected ants compared to sham-injected controls. When compared with RNA-seq data from Ophiocordyceps- manipulated ants, we found that both groups shared 113 differentially regulated genes. These included sensory neuron membrane protein genes, several odorant-binding protein genes and musculoskeletal genes such as titin and obscurin. Together, these results indicate that aflatrem-like compounds significantly affect neuromuscular and sensory function in C. floridanus. The conservation of staggers phenotype between C. floridanus and Bos taurus suggests that behaviour-manipulating strategies exhibited across the Tree of Life may be more similar in approach, if not widely different in application, than we realize. 

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3. Using machine learning to predict protein–protein interactions between a zombie ant fungus and its carpenter ant host

   https://doi.org/10.1038/s41598-023-40764-8  

   Will, Ian ; Beckerson, William C. ; de Bekker, Charissa ( December 2023 , Scientific Reports)

   Parasitic fungi produce proteins that modulate virulence, alter host physiology, and trigger host responses. These proteins, classified as a type of “effector,” often act via protein–protein interactions (PPIs). The fungal parasiteOphiocordyceps camponoti-floridani(zombie ant fungus) manipulatesCamponotus floridanus(carpenter ant) behavior to promote transmission. The most striking aspect of this behavioral change is a summit disease phenotype where infected hosts ascend and attach to an elevated position. Plausibly, interspecific PPIs drive aspects ofOphiocordycepsinfection and host manipulation. Machine learning PPI predictions offer high-throughput methods to produce mechanistic hypotheses on how this behavioral manipulation occurs. Using D-SCRIPT to predict host–parasite PPIs, we found ca. 6000 interactions involving 2083 host proteins and 129 parasite proteins, which are encoded by genes upregulated during manipulated behavior. We identified multiple overrepresentations of functional annotations among these proteins. The strongest signals in the host highlighted neuromodulatory G-protein coupled receptors and oxidation–reduction processes. We also detectedCamponotusstructural and gene-regulatory proteins. In the parasite, we found enrichment ofOphiocordycepsproteases and frequent involvement of novel small secreted proteins with unknown functions. From these results, we provide new hypotheses on potential parasite effectors and host targets underlying zombie ant behavioral manipulation.

    

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4. Cold adaptations along a range limit in an obligate symbiosis

   https://doi.org/10.1111/1365-2435.14120  

   Senula, Sarah F. ; Scavetta, Joseph T. ; Mueller, Ulrich G. ; Seal, Jon Nicholas ; Kellner, Katrin ( July 2022 , Functional Ecology)

   Symbionts can have profound effects on host fitness, adaptations and range distributions. Stress‐induced evolution is difficult to show in obligate symbioses; however, adaptive evolution within an obligate symbiosis can be investigated experimentally or by correlating trait variation with stress along an ecological cline (i.e. temperature‐stress gradient).

   We investigated the cold tolerance of the fungus‐growing antTrachymyrmex septentrionalisby performing cold tolerance assays comparing two populations collected from either the southernmost range of their distribution (Bastrop, Texas) or from a site that is approximately 600 km further north (Norman, Oklahoma). We first compared isolated fungal symbionts grown on artificial media to determine cold tolerance of fungus alone. Subsequently, we conducted cross‐fostering experiments between northern and southern host and symbionts to test for synergisms between the partners in generating adaptations of cold tolerance.

   Ants of the northern fungal populations were more cold adapted than southern fungal populations. Northern nests were deeper and northern colonies initially rejected fungi from the southern population. The cross‐fostering experiments demonstrated that only one partner must be cold tolerant to confer maximum cold tolerance to the ant–fungus symbiosis, because northern ants growing southern fungus under cold stress performed just as well as northern ants growing northern fungi.

   Our results suggest that cold stress has been an important selective factor during the migration of this ant–fungus symbiosis into northern latitudes during the last 10,000 years, and that cold tolerance likely is an energetically demanding trait that may be traded off with other aspects of the symbiosis' life history. The symbiosis also appears to have evolved several additional adaptations that increase survival in cold environments, such as building deeper nests that insulate the fungi from cold surface.

   Read the freePlain Language Summaryfor this article on the Journal blog.

    

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5. Masters of the manipulator: two new hypocrealean genera, Niveomyces ( Cordycipitaceae ) and Torrubiellomyces ( Ophiocordycipitaceae ), parasitic on the zombie ant fungus Ophiocordyceps camponoti-floridani

   https://doi.org/10.3767/persoonia.2022.49.05  

   Araújo, J.P.M. ; Lebert, B.M. ; Vermeulen, S. ; Brachmann, A. ; Ohm, R.A. ; Evans, H.C. ; Debekker, C. ( December 2022 , Persoonia - Molecular Phylogeny and Evolution of Fungi)

   During surveys in central Florida of the zombie-ant fungus Ophiocordyceps camponoti-floridani , which manipulates the behavior of the carpenter ant Camponotus floridanus , two distinct fungal morphotypes were discovered associated with and purportedly parasitic on O. camponoti-floridani . Based on a combination of unique morphology, ecology and phylogenetic placement, we discovered that these morphotypes comprise two novel lineages of fungi. Here, we propose two new genera, Niveomyces and Torrubiellomyces , each including a single species within the families Cordycipitaceae and Ophiocordycipitaceae , respectively. We generated de novo draft genomes for both new species and performed morphological and multi-loci phylogenetic analyses. The macro-morphology and incidence of both new species, Niveomyces coronatus and Torrubiellomyces zombiae , suggest that these fungi are mycoparasites since their growth is observed exclusively on O. camponoti-floridani mycelium, stalks and ascomata, causing evident degradation of their fungal hosts. This work provides a starting point for more studies into fungal interactions between mycopathogens and entomopathogens, which have the potential to contribute towards efforts to battle the global rise of plant and animal mycoses. 

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