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Red/Blue plots of the sampling plots. a. Schematic maps of the five 10610 m sampling plots. Trees are shown in dark brown and paths in light brown. Black dots indicate cell densities of dead O. unilateralis infected ants (each dot is a single ant). Colour codes represent the vegetation cover of the cells, ranging from 0 (lightest green) to 5 (darkest green). b. Red/blue plot showing source cells in red and sink cells in blue in 2006. c. Red/blue plot showing source cells in red and sink cells in blue in 2007. doi:10.1371/journal.pone.0004835.g003
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Parasites are likely to play an important role in structuring host populations. Many adaptively manipulate host behaviour, so that the extended phenotypes of these parasites and their distributions in space and time are potentially important ecological variables. The fungus Ophiocordyceps unilateralis, which is pan-tropical in distribution, causes...
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... density) and source (high density) areas. However, the percentage of source area differed considerably between the plots. Plot 5 and plot 3 had the largest source areas (27% and 19%, respectively) followed by plot 1 and plot 2 (10% and 9%, respectively). Plot 4 had a source area of only 4%. A red/blue plot [22] depicting sources and sinks (Fig. 3b) identified a single large source area radiating from one corner in plot 5. Plot 3 contained one large and one small source area while the rest of the plots had several smaller sources scattered around the ...
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... total recount of all cells in September 2007 revealed some dramatic changes in mean density and distribution in the plots (Fig. 3 b, c). In plots 3 and 4, the mean densities had more than doubled from 2.8 ants/m 2 in 2006 to 6.6 ants/m 2 and 5.8 ants/ m 2 , respectively, in 2007 (Wilcoxon signed-rank test, Plot 3: Z = 26.81, p,0.01; Plot 4: Z = 26.22, p,0.01). Density frequen- cy distributions were also much less skewed and had a considerable broader range than in ...
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... diameters in plot 5 had been reduced from 6 to 3-4 m. These trends were confirmed by the SADIE analyses, showing increased and statistically significant values of I a in all plots except plot 5, as well as greatly increased sizes of clusters (Table 1, Fig. 3c). In plot correlation could be found between the spatial structure in 2006 and 2007 (Fig. ...
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... In the case of Ophiocordyceps, ants latch and bite onto their final summit perches until death, which is thought to promote development of the fungal fruiting body and dispersal of the spores therein [9][10][11][12][13] . Moreover, preceding this fatal change in behavior, infected ants also deviate from foraging trails and increase locomotor activity, reduce nestmate communication, and convulse [12][13][14][15][16][17] . ...
... As such, the exact effects of these neurotransmitters can differ by species and social or physiological context. However, parallels exist with Ophiocordyceps-infected ants that exhibit changes in behavior that include increased walking, deviation from foraging trails, reduced nestmate communication, and the final manipulated bite [12][13][14][15][16] . ...
... In some manipulated ant samples, we detected elevated acetylcholine concentrations, which may correspond to reduced acetylcholinesterase gene expression previously observed. Speculatively, transient high acetylcholine levels could contribute to the altered behavior and muscular activity observed in manipulated hosts at fine timescales 12,[15][16][17]20,26,93,94,106 . ...
Camponotus floridanus ants show altered behaviors followed by a fatal summiting phenotype when infected with manipulating Ophiocordyceps camponoti-floridani fungi. Host summiting as a strategy to increase transmission is also observed with parasite taxa beyond fungi, including aquatic and terrestrial helminths and baculoviruses. The drastic phenotypic changes can sometimes reflect significant molecular changes in gene expression and metabolite concentrations measured in manipulated hosts. Nevertheless, the underlying mechanisms still need to be fully characterized. To investigate the small molecules producing summiting behavior, we infected C. floridanus ants with O. camponoti-floridani and sampled their heads for LC–MS/MS when we observed the characteristic summiting phenotype. We link this metabolomic data with our previous genomic and transcriptomic data to propose mechanisms that underlie manipulated summiting behavior in “zombie ants.” This “multiomic” evidence points toward the dysregulation of neurotransmitter levels and neuronal signaling. We propose that these processes are altered during infection and manipulation based on (1) differential expression of neurotransmitter synthesis and receptor genes, (2) altered abundance of metabolites and neurotransmitters (or their precursors) with known behavioral effects in ants and other insects, and (3) possible suppression of a connected immunity pathway. We additionally report signals for metabolic activity during manipulation related to primary metabolism, detoxification, and anti-stress protectants. Taken together, these findings suggest that host manipulation is likely a multi-faceted phenomenon, with key processes changing at multiple levels of molecular organization.
... Many organisms infect animals and compel them to perform specific, often bizarre, behaviors that serve to promote their own fitness at the expense of their host. For example, 'zombie ant' fungi of genus Ophiocordyceps compel their host carpenter ants to aberrantly leave the nest, wander away from established foraging trails, scale nearby stems or twigs, and, in their dying moments, clamp onto vegetation to ultimately perish in elevated positions Pontoppidan et al., 2009). Days later, a fungal stalk emerges from the dead ant's pronotum, well poised to rain spores on the ants that forage below (Evans and Samson, 1984). ...
For at least two centuries, scientists have been enthralled by the “zombie” behaviors induced by mind-controlling parasites. Despite this interest, the mechanistic bases of these uncanny processes have remained mostly a mystery. Here, we leverage the Entomophthora muscae-Drosophila melanogaster “zombie fly” system to reveal the mechanistic underpinnings of summit disease, a manipulated behavior evoked by many fungal parasites. Using a high-throughput approach to measure summiting, we discovered that summiting behavior is characterized by a burst of locomotion and requires the host circadian and neurosecretory systems, specifically DN1p circadian neurons, pars intercerebralis to corpora allata projecting (PI-CA) neurons and corpora allata (CA), the latter being solely responsible for juvenile hormone (JH) synthesis and release. Using a machine learning classifier to identify summiting animals in real time, we observed that PI-CA neurons and CA appeared intact in summiting animals, despite invasion of adjacent regions of the “zombie fly” brain by E. muscae cells and extensive host tissue damage in the body cavity. The blood-brain barrier of flies late in their infection was significantly permeabilized, suggesting that factors in the hemolymph may have greater access to the central nervous system during summiting. Metabolomic analysis of hemolymph from summiting flies revealed differential abundance of several compounds compared to non-summiting flies. Transfusing the hemolymph of summiting flies into non-summiting recipients induced a burst of locomotion, demonstrating that factor(s) in the hemolymph likely cause summiting behavior. Altogether, our work reveals a neuro-mechanistic model for summiting wherein fungal cells perturb the fly’s hemolymph, activating a neurohormonal pathway linking clock neurons to juvenile hormone production in the CA, ultimately inducing locomotor activity in their host.
... Many organisms infect animals and compel them to perform specific, often bizarre, behaviors that serve to promote their own fitness at the expense of their host. For example, 'zombie ant' fungi of genus Ophiocordyceps compel their host carpenter ants to aberrantly leave the nest, wander away from established foraging trails, scale nearby stems or twigs, and, in their dying moments, clamp onto vegetation to ultimately perish in elevated positions Pontoppidan et al., 2009). Days later, a fungal stalk emerges from the dead ant's pronotum, well poised to rain spores on the ants that forage below (Evans and Samson, 1984). ...
For at least two centuries, scientists have been enthralled by the “zombie” behaviors induced by mind-controlling parasites. Despite this interest, the mechanistic bases of these uncanny processes have remained mostly a mystery. Here, we leverage the Entomophthora muscae-Drosophila melanogaster “zombie fly” system to reveal the mechanistic underpinnings of summit disease, a manipulated behavior evoked by many fungal parasites. Using a high-throughput approach to measure summiting, we discovered that summiting behavior is characterized by a burst of locomotion and requires the host circadian and neurosecretory systems, specifically DN1p circadian neurons, pars intercerebralis to corpora allata projecting (PI-CA) neurons and corpora allata (CA), the latter being solely responsible for juvenile hormone (JH) synthesis and release. Using a machine learning classifier to identify summiting animals in real time, we observed that PI-CA neurons and CA appeared intact in summiting animals, despite invasion of adjacent regions of the “zombie fly” brain by E. muscae cells and extensive host tissue damage in the body cavity. The blood-brain barrier of flies late in their infection was significantly permeabilized, suggesting that factors in the hemolymph may have greater access to the central nervous system during summiting. Metabolomic analysis of hemolymph from summiting flies revealed differential abundance of several compounds compared to non-summiting flies. Transfusing the hemolymph of summiting flies into non-summiting recipients induced a burst of locomotion, demonstrating that factor(s) in the hemolymph likely cause summiting behavior. Altogether, our work reveals a neuro-mechanistic model for summiting wherein fungal cells perturb the fly’s hemolymph, activating a neurohormonal pathway linking clock neurons to juvenile hormone production in the CA, ultimately inducing locomotor activity in their host.
... Many organisms infect animals and compel them to perform specific, often bizarre, behaviors that serve to promote their own fitness at the expense of their host. For example, 'zombie ant' fungi of genus Ophiocordyceps compel their host carpenter ants to aberrantly leave the nest, wander away from established foraging trails, scale nearby stems or twigs, and, in their dying moments, clamp onto vegetation to ultimately perish in elevated positions Pontoppidan et al., 2009). Days later, a fungal stalk emerges from the dead ant's pronotum, well poised to rain spores on the ants that forage below (Evans and Samson, 1984). ...
For at least two centuries, scientists have been enthralled by the “zombie” behaviors induced by mind-controlling parasites. Despite this interest, the mechanistic bases of these uncanny processes have remained mostly a mystery. Here, we leverage the Entomophthora muscae-Drosophila melanogaster “zombie fly” system to reveal the mechanistic underpinnings of summit disease, a manipulated behavior evoked by many fungal parasites. Using a high-throughput approach to measure summiting, we discovered that summiting behavior is characterized by a burst of locomotion and requires the host circadian and neurosecretory systems, specifically DN1p circadian neurons, pars intercerebralis to corpora allata projecting (PI-CA) neurons and corpora allata (CA), the latter being solely responsible for juvenile hormone (JH) synthesis and release. Using a machine learning classifier to identify summiting animals in real time, we observed that PI-CA neurons and CA appeared intact in summiting animals, despite invasion of adjacent regions of the “zombie fly” brain by E. muscae cells and extensive host tissue damage in the body cavity. The blood-brain barrier of flies late in their infection was significantly permeabilized, suggesting that factors in the hemolymph may have greater access to the central nervous system during summiting. Metabolomic analysis of hemolymph from summiting flies revealed differential abundance of several compounds compared to non-summiting flies. Transfusing the hemolymph of summiting flies into non-summiting recipients induced a burst of locomotion, demonstrating that factor(s) in the hemolymph likely cause summiting behavior. Altogether, our work reveals a neuro-mechanistic model for summiting wherein fungal cells perturb the fly’s hemolymph, activating a neurohormonal pathway linking clock neurons to juvenile hormone production in the CA, ultimately inducing locomotor activity in their host.
... However, the mechanism of manipulating host behavior remained unknown (Herbison 2017;Will et al. 2020). Many studies have often used the term O. unilateralis sensu lato for the zombie-ant fungus, including the evolutionary relationship between fungi and hosts, the mechanism of manipulating host behavior, and genomes (Andersen et al. 2009;Hughes et al. 2009;Pontoppidan et al. 2009;Evans et al. 2011a). Regarding the evolutionary relationship between fungi and hosts, Evans et al. (2011b) found that different fungi parasitized different ants; their appearances were very similar but differed in morphological characters. ...
Some Ophiocordyceps species infecting ants are able to manipulate the host behavior. The hosts are manipulated in order to move to location that are advantageous for fungal spore transmission. Ophiocordyceps species that are able to manipulate the ant's behavior are called "zombie-ant fungi". They are widespread within tropical forests worldwide, with relatively few reports from subtropical monsoon evergreen broad-leaf forest. Zombie-ant fungi have been described and reported in different countries worldwide. However, there were a few reports from China. This study proposed six new species of zombie-ant fungi from China based on multi-gene (SSU, LSU, TEF , RPB1 and RPB2 ) phylogenetic analyses and morphological characteristics. Six novel species of Ophiocordyceps from China were identified as the Ophiocordyceps unilateralis core clade, forming a separate lineage with other species. Six novel species of Ophiocordyceps with hirsutella-like asexual morphs exclusively infecting ants were presented herein, namely, Ophiocordyceps acroasca , Ophiocordyceps bifertilis , Ophiocordyceps subtiliphialida , Ophiocordyceps basiasca , Ophiocordyceps nuozhaduensis and Ophiocordyceps contiispora . Descriptions and illustrations for six taxon were provided. Five of these species were collected from the subtropical monsoon evergreen broad-leaf forest, and one was collected from the rainforest and subtropical monsoon evergreen broad-leaf forest. This work proposes that the same host of Camponotus can be infected by multiple ant pathogenic fungi, while multiple ants of Polyrhachis can be infected by the same pathogenic fungi at the same time. This study contributes towards a better understanding of the evolutionary relationship between hosts and fungi, and provides novel insights into the morphology, distribution, parasitism, and ecology of Ophiocordyceps unilateralis sensu lato. We have provided a method for obtaining living cultures of Ophiocordyceps unilateralis complex species and their asexual morphs based on the living cultures, which is of significant value for further studies of Ophiocordyceps unilateralis complex species in the future.
... This strategy is usually employed by fungi that grow outside the host body after infection to reach a next suitable host [4], such as those inducing infected ants to die suspended while attached to vegetation [1,2,5]. These parasites generally induce host death in a specific place of the vegetation to increase their fitness, development, and transmission [1,6,7]. ...
Gibellula (Cordycipitaceae, Hypocreales) is frequently observed growing on spiders, but little is known about their host range. One of the greatest challenges in describing these interactions is identifying the host, since the fungus often rapidly consumes the parasitised spiders and destroys important diagnostic taxonomic traits. Additionally, the global diversity of Gibellula remains unclear, as does the natural history and phylogenetic relationships of most of the species. Herein, we performed an extensive investigation on the species of Gibellula, reconstructed the most complete molecular phylogeny of the genus in the context of Cordycipitaceae, and performed a systematic review in order to provide the foundations towards a better understanding of the genus. Therefore, we have performed an integrative study to investigate the life history of the genus and to disentangle the questionable number of valid species proposed over time. We provided novel molecular data for published species that had not been sequenced before, such as G. mirabilis and G. mainsii, and evaluated all the original and modern morphological descriptions. In addition, we presented its global known distribution and compiled all available molecular data. We suggested a set of terms and morphological traits that should be considered in future descriptions of the genus and that a total of 31 species should be considered as accepted.
... Manipulated ant cadavers generally cluster in 'graveyards' at higher densities than the surrounding habitat Andriolli et al., 2019;Pontoppidan et al., 2009). Moreover, cadaver distributions and abundances within graveyards can shift over time (Pontoppidan et al., 2009), likely reflecting changing environmental factors. ...
... Manipulated ant cadavers generally cluster in 'graveyards' at higher densities than the surrounding habitat Andriolli et al., 2019;Pontoppidan et al., 2009). Moreover, cadaver distributions and abundances within graveyards can shift over time (Pontoppidan et al., 2009), likely reflecting changing environmental factors. Ultimately, Ophiocordyceps must transmit to new hosts, requiring the formation of a spore-containing perithecium, or 'fruiting body'. ...
... Our aim was not to rigorously compare graveyard versus non-graveyard conditions, but rather to use these high-density areas as an efficient means of finding as many cadavers as possible for our study. Initial cadaver densities during plot establishment at our sites were nearly eight-fold less than previously reported for Ophiocordyceps graveyards in Southern Thailand (Pontoppidan et al., 2009), which likely reflects differences in the fungal and ant species studied (Ophiocordyceps camponoti-leonardi and Colobopsis leonardi), as well as habitat (tropical vs. subtropical). For each wilderness area, we established three graveyard plots of 9-by-9 m for a total of nine plots. ...
Ophiocordyceps fungi manipulate the behaviour of their ant hosts to produce a summit disease phenotype, thereby establishing infected ant cadavers onto vegetation at elevated positions suitable for fungal growth and transmission. Multiple environmental and ecological factors have been proposed to shape the timing, positioning and outcome of these manipulations.
We conducted a long‐term field study of Ophiocordyceps camponoti‐floridani infections of Camponotus floridanus ants—the Florida zombie ants. We propose and refine hypotheses on the factors that shape infection outcomes by tracking the occurrence of and fungal growth from hundreds of ant cadavers. We modelled and report these data in relation to weather, light, vegetation and attack by hyperparasites.
We investigated environmental factors that could affect the occurrence and location of newly manipulated ant cadavers. New cadaver occurrence was preferentially biased towards epiphytic Tillandsia bromeliads, canopy openness and summer weather conditions (an interactive effect of temperature, humidity and precipitation). Furthermore, we suggest that incident light at the individual cadaver level reflects microhabitat choice by manipulated ants or selective pressure on cadaver maintenance for conditions that improve fungal survival.
We also asked which environmental conditions affect fungal fitness. Continued fungal development of reproductive structures and putative transmission increased with moist weather conditions (interaction of humidity and precipitation) and canopy openness, while being reduced by hyperparasitic mycoparasite infections. Moreover, under the most open canopy conditions, we found an atypical Ophiocordyceps growth morphology that could represent a plastic response to conditions influenced by high light levels.
Taken together, we explore general trends and the effects of various ecological conditions on host and parasite disease outcomes in the Florida zombie ant system. These insights from the field can be used to inform experimental laboratory setups that directly test the effects of biotic and abiotic factors on fungus–ant interactions or aim to uncover underlying molecular mechanisms.
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... The vast majority of entomopathogenic fungal species must kill their hosts to transmit their infective units (spores), which makes them important agents of natural control of arthropod populations (Evans 2013;Redman et al. 2016;Samson et al. 2013). The most speciose groups of entomopathogenic fungi are the order Hypocreales (Ascomycota) and subphylum Entomophthoromycotina (Zoopagomycota) (Li et al. 2021), with species within both groups frequently killing several hosts in a relatively small area, causing epizootic events Pontoppidan et al. 2009;Samson et al. 2013). Hypocrealean fungi infecting arthropods include both generalist and specialist lineages Roy et al. 2006;Vega et al. 2009). ...
Fungal parasites that infect spiders can affect their survival and potentially their behaviour. The genus Gibellula (Ascomycota, Cordycipitaceae) infects arachnids, and due to difficulties in identifying hosts after fungal sporulation, its ecology and spider host diversity are poorly understood. Herein, we propose a new species of Gibellula from the Brazilian Atlantic Forest: Gibellula aurea, which parasitizes two spider families (Anyphaenidae and Corinnidae). Gibellula aurea exhibits characteristic golden-yellow hyphae that completely cover hosts and white conidiophores emerging along synnemata or directly from hosts. Molecular identification was performed by sequencing the small and large nuclear ribosomal subunits, translation elongation factor, and RNA polymerase II second largest subunit regions, and reconstructing multigene phylogenetic trees. Maximum Likelihood and Bayesian Inference phylogenies demonstrate that G. aurea forms a well-supported clade closer to G. flava, G. gamsii, G. leiopus, G. longispora, G. pigmentosinum, and G. pulchra. The phylogenetic reconstruction displayed herein represents the most comprehensive phylogeny for this genus to date. Spider hosts parasitized by G. aurea have been invariably found attached underneath leaves in vegetation, regardless of the identity of the infected hosts. The consistency of the death locations of G. aurea hosts indicates recurrent behaviour given the habitat heterogeneity of these host groups. Nevertheless, it is still unclear to what extent the place where hosts die can favour parasite fitness.
... For example, Will et al. (48) used comparative transcriptomics before, during, and after manipulation to uncover a network of candidate genes that were linked to host circadian rhythm, foraging behaviors, neuromodulation, and novel parasite compounds and toxins -all biological pathways thought to be important for the successful manipulation of ants by Ophiocordyceps fungi. In this well-documented system, infected ants climb up vegetation, clamp down on the underside of leaves with their mandibles, and die, where the fungus can produce a fruiting body and spread its spores by shedding them upon other ants (49). Undoubtedly, this type of integrative research can help uncover the candidate mechanisms involved in host manipulation events, but linking these mechanisms to functional and observable changes in host phenotype will require a completely different type of technology, one that harnesses the remarkable properties of a certain prokaryotic immune system. ...
Insects and parasites dominate the biosphere, in terms of known biodiversity and mode of life, respectively. Consequently, insects play a part in many host-parasite systems, either as parasite, host, or both. Moreover, a lot of these systems involve adaptive parasite-induced changes of host phenotype (typically behavior or morphology), which is commonly known as host manipulation. While many host manipulation systems have been described within the last few decades, the proximate mechanisms that underpin host phenotypic change are still largely unknown. Given the intimate co-evolutionary
history of host-parasite systems, teasing apart the intricate network of biochemical reactions involved in host manipulation requires the integration of various complementary technologies. In this perspective, we stress the importance of multidisciplinary research on host manipulation, such as high-throughput sequencing methods (genomics and transcriptomics) to search for candidate mechanisms that are activated during a manipulation event. Then, we argue that gene editing technologies, specifically the CRISPR-Cas9 system, are a powerful way to test for the functional roles of candidate mechanisms, in both the parasite and the host. Finally, given the sheer diversity of unique host-parasite systems discovered to date, there is indeed a tremendous potential to create novel non-traditional model systems that could greatly expand our capacity to test the fundamental aspects of behavior and behavioral regulation.
... Many organisms induce summit disease including the studied Pandora formicae. A similar extended phenotype is known in Ophiocordyceps fungal species that infect primarily tropical ants of the genus Camponotus (Andersen et al. 2009;Pontoppidan et al. 2009) and similar mechanisms can be found in the ant parasitizing Dicrocoelium uke worms. These analogous phenologies probably represent convergent evolutionary responses to evade social handling of infected hosts by ant workers, which would considerably decrease the pathogen's reproductive success unless the pathogen evolved mechanisms to drive newly infected hosts out of the reach of their nestmates (Cremer et al. 2007;Boomsma et al. 2014). ...
Social systems are attractive targets for parasites. Once infiltrated they could manipulate the host to contribute to their further dispersal. A wide array of parasites causes summit disease driving their host up on a grass blade from where propagules are then dispersed. In ants, previous observations suggested the existence of a social prophylactic strategy that could help reduce the pathogen’s dispersal success through early corpse disposal in the case of summit causing pathogenic Pandora fungus. We experimentally tested the efficiency of such prophylactic mechanisms in a large nest complex using fresh ant corpses and dummies fixed to grass blades. Indeed, ants discovered and disposed of corpses very efficiently, primarily of those close to the nest margin, while dummies were mostly neglected. We argue that this behavior is not necessarily specific, but rather part of a general set of behaviors that could be of use to fight other pathogens as well that cause summit disease.
