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Zombie-ant fungi across continents: 15 new species and new combinations within Ophiocordyceps . I. Myrmecophilous hirsutelloid species

Authors:
João PM Araújo at University of Copenhagen
João PM Araújo
Harry C. Evans
Harry C. Evans
Harry C. Evans
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Ryan M Kepler at United States Department of Agriculture
Ryan M Kepler
David P Hughes at Pennsylvania State University
David P Hughes
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Abstract and Figures

Ophiocordyceps species infecting ants – the so-called zombie-ant fungi – comprise one of the most intriguing and fascinating relationships between microbes and animals. They are widespread within tropical forests worldwide, with relatively few reports from temperate ecosystems. These pathogens possess the ability to manipulate host behaviour in order to increase their own fitness. Depending on the fungal species involved the infected ants are manipulated either to leave the nest or ascend understorey shrubs, to die biting onto vegetation, or descend from the canopy to die at the base of trees. Experimental evidence has demonstrated that the behavioural change aids spore dispersal and thus increases the chances of infection, because of the existing behavioural immunity expressed inside ant colonies that limits fungal development and transmission. Despite their undoubted importance for ecosystem functioning, these fungal pathogens are still poorly documented, especially regarding their diversity, ecology and evolutionary relationships. Here, we describe 15 new species of Ophiocordyceps with hirsutella-like asexual morphs that exclusively infect ants. These, form a monophyletic group that we identified in this study as myrmecophilous hirsutelloid species. We also propose new combinations for species previously described as varieties and provide for the first time important morphological and ecological information. The species proposed herein were collected in Brazil, Colombia, USA, Australia and Japan. All species could readily be separated using classic taxonomic criteria, in particular ascospore and asexual morphology.
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... However, in the Central Brazilian Amazon, species belonging to three complexes were recorded: O. unilateralis sensu lato, O. kniphofioides sensu lato, and O. australis sensu lato (Cardoso Neto et al. 2019). Each group, per se, has specific extended phenotypes to achieve reproductive success and continue infecting healthy ants (Andersen et al. 2009;Araújo et al. 2018;Evans andSamson 1982, 1984). ...
... We grouped and distinguished the ants into three complexes-O. unilateralis s.l., O. kniphofioides s.l., and O. australis s.l., according to the literature description of infections recorded and fruiting body fungal morphology (Evans andSamson 1982, 1984;Araújo et al. 2015Araújo et al. , 2018Araújo and Hughes 2017). The unilateralis complex infects exclusively Camponotini ants that bite substrate, producing brown fruiting bodies attached laterally to emerged stroma. ...
... For instance, some extended phenotypes, such as the biting behavior, are unanimous within some species (all O. unilateralis s.l. complex), yet not by others (Andersen et al. 2009Araújo et al. 2018 Climbing and biting before death, the remarkable and final acts in the life of a zombie ant infected by O. unilateralis s.l. were well investigated in several studies (Andersen et al. 2009, Andriolli et al. 2019, de Bekker et al. 2015, de Bekker et al. 2017, de Bekker and Das 2022, Chung et al. 2017. Our findings suggest that most of the dead ants infected by O. unilateralis s.l. were in leaves on understory bushes, mostly in palm trees. ...
With the dead under the mat: the zombie ant extended phenotype under a new perspective
Article
Full-text available
  • Jun 2024
  • NATURWISSENSCHAFTEN
Some parasitic fungi can increase fitness by modifying the behavior of their hosts. These behaviors are known as extended phenotypes because they favor parasitic gene propagation. Here, we studied three lineages of Ophiocordyceps, a fungus that infects ants, altering their conduct before death. According to fungal strategy, ants may die in leaf litter, with entwined legs in branches, under the moss mat, or biting plant tissue. It is critical for parasites that the corpses stay at these places because Ophiocordyceps exhibit iteroparity, possibly releasing spores in multiple life cycles. Thus, we assumed substrate cadaver permanence as a fungi reproductive proxy and corpse height as a proxy of cadaver removal. We hypothesize that biting vegetation and dying in higher places may increase the permanence of ant corpses while avoiding possible corpse predation on the forest floor. We monitored over a year more than 4000 zombie ants in approximately 15 km² of undisturbed tropical forest in central Amazonia. Our results show a longer permanence of corpses with increasing ground height, suggesting that the parasites may have better chances of releasing spores and infecting new hosts at these places. We found that the zombie ants that last longer on the substrate die under the moss mat in tree trunks, not necessarily biting vegetation. The biting behavior appears to be the most derived and complex mechanism among Ophiocordyceps syndromes. Our results put these findings under a new perspective, proposing that seemingly less complex behavioral changes are ecologically equivalent and adaptative for other parasite lineages.
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... The primer pair 2218R and 983F was used to amplify the translation elongation factor 1α (TEF) (Rehner and Buckley, 2005). The largest and second largest subunits of RNA polymerase II (RPB1 and RPB2) were amplified by primer pairs RPB1 and RPB1Cr_oph and fRPB2-7cR and fRPB2-5F, respectively (Liu et al., 1999;Castlebury et al., 2004;Araújo et al., 2018). The polymerase chain reaction (PCR) matrix was carried out in 25 μL final volume, consisting of 17.25 of μl sterile water, 2 μL of dNTP (2.5 mmoL/L), 2.5 μL of PCR 10 × Buffer (2 mmoL/L Mg 2+ ) (Transgen Biotech, Beijing, China), 1 μL of forwarding primers (10 μmol/L), 0.25 μL of Taq DNA polymerase (Transgen Biotech, Beijing, China), 1 μL of reverse primers (10 1 μmol/L), and 1 μL of DNA template (500 ng/μL). ...
... Many phylogenetic classifications of the O. unilateralis complex had been undertaken, and these groups had been continuously supplemented and improved on the basis of molecular phylogeny, morphology and ecology (Evans et al., 2011b;Kobmoo et al., 2012Kobmoo et al., , 2015Araújo et al., 2018;Wei et al., 2020). As the same time, the use of multi-gene combined datasets for species classification had been widely adopted. ...
... Alleviation of hypercholesterolemia and atherosclerosis was demonstrated in a mouse model of hyperlipidemia. The putative BGC associated with the catalytic synthesis of pyripyropene A compound (GenBank: was commonly distributed in tropical rainforests, and many studies track its behavior on a one-year basis, with a long growth cycle (Araújo et al., 2018;Cardoso et al., 2019), For O. unilateralis sensu lato species distributed in tropical rainforests, the production of pyranonigrin E, a compound that cleaned up superoxide free radicals in their bodies in time, might be the reason for their longer growth time. ...
Genomic comparative analysis of Ophiocordyceps unilateralis sensu lato
Article
Full-text available
  • Apr 2024
Ophiocordyceps unilateralis sensu lato is a common pathogenic fungus of ants. A new species, O. fusiformispora, was described based on morphology and phylogenetic evidence from five genes (SSU, LSU, TEF1α, RPB1, and RPB2). The whole genomes of O. fusiformispora, O. contiispora, O. subtiliphialida, O. satoi, O. flabellata, O. acroasca, and O. camponoti-leonardi were sequenced and annotated and compared with whole genome sequences of other species in O. unilateralis sensu lato. The basic genome-wide characteristics of the 12 species showed that the related species had similar GC content and genome size. AntiSMASH and local BLAST analyses revealed that the number and types of putative SM BGCs, NPPS, PKS, and hybrid PKS-NRPS domains for the 12 species differed significantly among different species in the same genus. The putative BGC of five compounds, namely, NG-391, lucilactaene, higginsianin B, pyripyropene A, and pyranonigrin E were excavated. NG-391 and lucilactaene were 7-desmethyl analogs of fusarin C. Furthermore, the 12 genomes had common domains, such as KS-AT-DH-MT-ER-KR-ACP and SAT-KS-AT-PT-ACP-ACP-Te. The ML and BI trees of SAT-KS-AT-PT-ACP-ACP-Te were highly consistent with the multigene phylogenetic tree in the 12 species. This study provided a method to obtain the living culture of O. unilateralis sensu lato species and its asexual formed on the basis of living culture, which was of great value for further study of O. unilateralis sensu lato species in the future, and also laid a foundation for further analysis of secondary metabolites of O. unilateralis sensu lato.
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... In contrast to Beauveria, Ophiocordyceps species are highly specialized entomopathogens that generally infect only one insect species (4)(5)(6). The 'zombie-making' fungi of the species complex Ophiocordyceps unilateralis sensu lato infect ants from the Camponotini tribe. ...
... Following this summiting behavior, the fungus converts to a multicellular, mycelial growth, which eventually gives rise to a fruiting body that sprouts from the cadaver (11,12). This fruiting body carries the spores that are released to infect new ants (4)(5)(6). These manipulated behaviors are a crucial aspect of the Ophiocordyceps life cycle that aid in circumventing social immunity behaviors of healthy nest mates (13) and place the ant in a microclimate that promotes fungal growth and spore dispersal (10,14). ...
What does your gut tell you? Influences of a zombie-making and generalist fungal entomopathogen on carpenter ant micro- and mycobiota
Preprint
Full-text available
  • May 2024
Microbiome composition impacts many host aspects including health, nutrition, reproduction, and behavior. This warrants the recent uptick in insect microbiota research across species and ecosystems. Commensurate with this, the bacterial microbiome of the ant Camponotus floridanus has been well characterized across body regions and maturation levels. However, potential effects of entomopathogens on the gut microbiome, and the fungal communities therein, are yet to be assessed. Investigation of the microbiome during infection could provide insight into entomopathogenic infection and manipulation strategies and inform effective biopesticide strategies. Additionally, the mycobiome remains often overlooked despite playing a vital role in gut ecology with potential implications for health and infection outcomes. To improve our limited understanding of fungal infections in insects, and ants in particular, we characterized the effects of two entomopathogens with different infection strategies on the gut micro- and mycobiota of C. floridanus over time; Ophiocordyceps camponoti-floridani and Beauveria bassiana. Specialist, zombie-making O. camponoti-floridani fungi hijack the behavior of C. floridanus ants over three weeks, causing them to find an elevated position, and fix themselves in place with their mandibles. This summiting behavior is adaptive to Ophiocordyceps as the ant transports the fungus to conditions that favor fruiting body development, spore production, dispersal, and transmission. In contrast, the generalist entomopathogen B. bassiana infects and kills the ant within a few days, without the induction of obvious fungus-adaptive behaviors. By comparing healthy ants with Beauveria- and Ophiocordyceps-infected ants we aimed to 1) describe the dynamics of the micro- and mycobiome of C. floridanus during infection, and 2) determine if the effects on gut microbiota are distinctive between fungi that have different infection strategies. While Beauveria did not measurably affect the ant host micro-and mycobiome, Ophiocordyceps did, especially for the mycobiome. Moreover, ants that were sampled during Ophiocordyceps-adaptive summiting behavior had a significantly different micro- and mycobiome composition compared to healthy controls and those sampled before and after manipulation took place. This suggests that the host microbiome might have a role to play in the manipulation strategy of Ophiocordyceps.
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... According to the current status of Cordyceps s. l. taxonomy, it belongs to four families: Clavicipitaceae, Cordycipitaceae, Ophiocordycipitaceae and Polycephalomycetaceae (Sung et al. 2007a;Xiao et al. 2023). Among them, the genus Ophiocordyceps Petch (Ophiocordycipitaceae) has received significant attention for its unique interactions with hosts and medical values (Zou et al. 2017;Araújo et al. 2018;Luangsa-ard et al. 2018;Khonsanit et al. 2019;Wang et al. 2021a;Zou et al. 2022;Tang et al. 2023a). ...
... Names.asp) (Sung et al. 2007a;Sanjuan et al. 2015;Spatafora et al. 2015;Araújo et al. 2018;Evans et al. 2018;Luangsa-ard et al. 2018;Wijayawardene et al. 2018;Khonsanit et al. 2019;Mongkolsamrit et al. 2023;Tang et al. 2023a, b). ...
Molecular phylogeny and morphology reveal two new entomopathogenic species of Ophiocordyceps (Ophiocordycipitaceae, Hypocreales) parasitic on termites from China
Article
Full-text available
  • Mar 2024
Two new termite-pathogenic species, Ophiocordyceps globiperitheciata and O. longistipes , are described from Yunnan Province, China. Six-locus (ITS, nrSSU, nrLSU, tef-1α , rpb1 and rpb2 ) phylogenetic analyses in combination with morphological observations were employed to characterize these two species. Phylogenetically, O. globiperitheciata is most closely related to Hirsutella cryptosclerotium and O. communis , whereas O. longistipes shares a sister relationship with O. fusiformis . However, O. globiperitheciata differs from H. cryptosclerotium by parasitizing Blattodea and producing clavate, unbifurcated stromata. Ophiocordyceps globiperitheciata is distinguished from O. communis by multiple stromata, shorter asci and ascospores. Ophiocordyceps longistipes differs from O. fusiformis in producing larger stromata, perithecia, asci and ascospores, as well as smaller citriform or oval conidia. Morphological descriptions of the two new species and a dichotomous key to the 19 termite-pathogenic Ophiocordyceps species are presented.
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... The taxa used for phylogenetic analyses were selected, based on BLAST search results and related references Quandt et al. 2014;Sanjuan et al. 2015;Araújo et al. 2018;Luangsa-Ard et al. 2018 (Nylander 2004) as implemented in MrMTgui v.1.0. (Nuin 2007) was used to determine the best-fit evolution model for Bayesian Inference analyses under the Akaike Information Criterion (AIC). ...
... clavate 130.0-250 × 5-6, filiform, septate Chen et al. (2011) Ophiocordyceps paludosa larvae of Lepidoptera 55-130 × 0.5-1.0, slender filiform, greyish-brown 800-855 × 375-410, superficial, greyish-brown to deep brown, flattened-ovoid 480-550 × 8-10, cylindrical 390-490 × 2.0-2.5, filiform, multi-septate, non-disarticulating Mains (1940) on more sufficient taxa sampling (Ban et al. 2009;Evans et al. 2011;Sanjuan et al. 2015;Simmons et al. 2015;Spatafora et al. 2015;Araújo et al. 2018;Khonsanit et al. 2019;Araújo et al. 2020;Mongkolsamrit et al. 2021;Yang et al. 2021;Araújo et al. 2022;Mongkolsamrit et al. 2022;Tang et al. 2022;Mongkolsamrit et al. 2023;Tang et al. 2023a, b). However, Cordyceps musicaudata has not been revised because there are no specimens available for study of its morphological and molecular data. ...
Two new species and one new combination of Ophiocordyceps (Hypocreales, Ophiocordycipitaceae) in Guizhou
Article
Full-text available
  • Feb 2024
Ophiocordyceps is the largest genus in Ophiocordycipitaceae and has a broad distribution with high diversity in subtropical and tropical regions. In this study, two new species, pathogenic on lepidopteran larvae are introduced, based on morphological observation and molecular phylogeny. Ophiocordyceps fenggangensis sp. nov. is characterised by having fibrous, stalked stroma with a sterile tip, immersed perithecia, cylindrical asci and filiform ascospores disarticulating into secondary spores. Ophiocordyceps liangii sp. nov. has the characteristics of fibrous, brown, stipitate, filiform stroma, superficial perithecia, cylindrical asci and cylindrical-filiform, non-disarticulating ascospores. A new combination Ophiocordyceps musicaudata (syn. Cordyceps musicaudata ) is established employing molecular analysis and morphological characteristics. Ophiocordyceps musicaudata is characterised by wiry, stipitate, solitary, paired to multiple stromata, yellowish, branched fertile part, brown stipe, immersed perithecia, cylindrical asci and cylindrical-filiform, non-disarticulating ascospores.
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... For ITS and LSU, the cycle started with an initial denaturation of doublestranded DNA molecules at 95 • C for 5 min; followed by 35 cycles of denaturation at 95 • C for 1 min, annealing at 58 • C for 45 s, and extension at 72 • C for 2 min; with a final extension at 72 • C for 5 min. The TEF-1α fragment was amplified using a PCR cycle adapted from Araújo et al. (2018). The cycle conditions were as follows: initial denaturation at 95 • C for 2 min; 10 cycles of denaturation at 95 • C for 30 s, annealing at 64 • C for 50 s, and extension at 72 • C for 1 min; followed by 35 cycles of denaturation at 95 • C for 30 s, annealing at 54 • C for 50 s, and extension at 72 • C for 1 min; and a final extension at 72 • C for 5 min. ...
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... DNA templates were obtained from cultures using the CTAB method, following that described in Liu et al. (2001). The polymerase chain reaction (PCR) was used to amplify genetic markers using the following primer pairs: ITS4/ITS5 for ITS (internal transcribed spacer gene region) (White et al. 1990), NS1/NS4 for SSU (small subunit ribosomal RNA gene region) (White et al. 1990), LR0R/ LR5 for LSU (large subunit rRNA gene region) (Hopple 1994) 2218R/983F for TEF-1α (translation elongation factor 1-alpha gene region) (Rehner and Buckley 2005), CRPB1/RPB1Croph for RPB1 (RNA polymerase II largest subunit gene region) (Castlebury et al. 2004;Araújo et al. 2018), fRPB2-7cR/fRPB2-5F for RPB2 (RNA polymerase II second largest subunit) (Liu et al. 1999). A total of 25 µl PCR matrix contained PCR 2.5 µl Buffer (Transgen Biotech, Beijing, China), 17.25 µl sterile water, 4 µl dNTP, 1 µl each forward and reverse primer, 0.25 µl Taq DNA polymerase (Transgen Biotech, Beijing, China) and 1 µl DNA template. ...
Morphology and phylogeny of four new species within Polycephalomycetaceae (Hypocreales) parasitising Ophiocordyceps species
Article
Full-text available
  • May 2024
Species of the family Polycephalomycetaceae grow on insects or entomopathogenic fungi and are distributed from tropical to subtropical regions. This study proposed four new species of hyperparasitic fungi from China based on six molecular markers (ITS, SSU, LSU, TEF-1α, RPB1 and RPB2) phylogenetic analyses and morphological characteristics. The four new species, i.e. Pleurocordyceps litangensis, Polycephalomyces jinghongensis, Po. multiperitheciatae and Po. myrmecophilus, were described and illustrated. Pl. litangensis, exhibiting a hyperparasitic lifestyle on Ophiocordyceps sinensis, differed from Pleurocordyceps other species in producing subulate β-phialides and ovoid or elliptic α-conidia. Po. jinghongensis was distinct from Polycephalomyces other species, being parasitic on Ophiocordyceps sp., as producing oval or long oval-shaped α-conidia and columns of β-conidia. Po. multiperitheciatae differed from Polycephalomyces other species as having synnemata with fertile head, linear β-conidia and parasitic on Ophiocordyceps multiperitheciata. Po. myrmecophilus was distinct from Polycephalomyces other species, being parasitic on the fungus Ophiocordyceps acroasca, as producing round or ovoid α-conidia and elliptical β-conidia without synnemata from the colonies. These four species were clearly distinguished from other species in the family Polycephalomycetaceae by phylogenetic and morphological characteristics. The morphological features were discussed and compared to relevant species in the present paper.
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... Total DNA was extracted using the CTAB method described by [15]. Polymerase chain reaction (PCR) was used to amplify genetic markers using the following primer pairs: LR0R/LR5 for small subunit nuclear ribosomal DNA (LSU) [16,17], EF1α-EF/EF1α-ER for translation elongation factor 1-α (TEF1-α) [18], RPB1-5 ′ F/RPB1-5 ′ R for partial RNA polymerase II largest subunit gene region (RPB1), RPB2-5 ′ F/RPB2-5 ′ R for partial RNA polymerase II second largest subunit gene region (RPB2) [19,20]. The PCR assay was completed with a final volume of 25 µL. ...
Molecular Phylogenetic and Comparative Genomic Analysis of Pleurocordyceps fusiformispora sp. nov. and Perennicordyceps elaphomyceticola in the Family Polycephalomycetaceae
Article
Full-text available
  • Apr 2024
  • J. Fungi
Several Pleurocordyceps species have been reported as hyperparasitic fungi. A new species, Pleurocordyceps fusiformispora, and a known species, Perennicordyceps elaphomyceticola, are described here based on morphology and phylogenetic evidence from six genes (ITS, SSU, LSU, TET1-α, RPB1, and RPB2). Pl. fusiformispora differed from the other Pleurocordyceps species by producing flaky colonies, ovoid or elliptic α-conidia, and fusiform or long fusiform β-conidia. Both full genomes of Pe. elaphomyceticola and Pl. fusiformispora were sequenced, annotated, and compared. The antiSMASH and local BLAST analyses revealed significant differences in the number and types of putative secondary metabolite biosynthetic gene clusters, i.e., NPPS, PKS, and hybrid PKS–NRPS domains, between the two species. In addition, the putative BGCs of six compounds, namely ε-poly lysine, 4-epi-15-epi-brefeldin A, Monorden D/monocillin IV/monocillin VII/pochonin M/monocillin V/monocillin II, Tolypyridone, Piperazine, and Triticone DABFC, were excavated in the present study. This study motivates the use of heterologous expression and gene knockout methods to discover novel biologically active SMs from Polycephalomycetaceae.
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... The variation in morphology exhibited by specimens of this genus, as well as the challenges in their full identification, suggests the presence of species complexes within this fungal type. Such complexes can solely be differentiated by means of molecular phylogenetic analysis, as is the case in the Ophiocordyceps genus [28]. Remarkably, the genus richness values of Ophiocordyceps and Cordyceps s.s. in this case appear to exceed those of some highly diverse tropical regions, such as the Amazon Basin from Ecuador, where up to 15 morphospecies of Ophiocordyceps and 15 species of Cordyceps s. l. were identified in deciduous woods from Mexico [27,29]. ...
Patterns of Diversity, Structure and Local Ecology of Arthropod-Pathogenic Fungi in the Amazonian Forest of Cusco and Madre de Dios Regions, Southern Peru
Article
Full-text available
  • Oct 2023
  • Diversity
Citation: Huamantupa-Chuquimaco, I.; Holgado Rojas, M.E.; Quispe Ordoñez, M.A.; García Roca, M.; Medina, A.C.; Ancco, W.Q.; Poccohuanca-Aguilar, R.O.; Córdova, Z.M.C.; Meza Calvo, J.G.; Sanjuan Giraldo, T.I. Patterns of Diversity, Structure and Local Ecology of Arthropod-Pathogenic Fungi in the Amazonian Forest of Cusco and Madre de Dios Regions, Southern Peru. Diversity 2023, 15, 1122. Abstract: The ecological role and potential management of arthropod-pathogenic fungi (APF) in neotropical forests are of great importance, but they are still little studied. The present study achieves a first estimation of diversity patterns, structure and local ecology of APF in the Amazonian forests of the Cusco and Madre de Dios regions in southern Peru. We sampled 39 localities in five basins, examining 277 specimens, four families and 20 genera with 82 species (40% morphospecies). The most diverse families were Cordycipitaceae with 51 species and Ophiocordicipitaceae (22). Cusco obtained a greater diversity: four families, 18 genera and 58 morphospecies, with the Urubamba and Amarumayu basins having greater diversity (31 and 20 species); for the Madre de Dios basin, there was 28 species. In both regions, the richness values were corroborated by Fisher's Alpha and Chao-1 indexes, the latter identifies Amarumayu and Araza with maximum values. The NMDS analysis showed a good pattern of separation of the two APF communities, although an important group was shared. Elevation was identified as the environmental variable with the strongest influence on diversity and structure. The dominance analysis identified Ophiocordyceps australis and Paraisaria amazonica as hyperdominant, due to their density and distribution. The local ecological patterns in Pongo de Qoñec show that the richness of entomopathogens is largely favored by low understory light, associated with pristine or little-impacted habitats. We conclude that this first approximation of the knowledge of the high diversity of APF in southern Peru is still insufficient, but it demonstrates the importance of their conservation and represents enormous potential for sustainable management.
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Molecular phylogenetics of the Ophiocordyceps sinensis-species complex lineage (Ascomycota, Hypocreales), with the discovery of new species and predictions of species distribution
Article
Full-text available
  • Feb 2024
Ophiocordyceps sinensis is a famous traditional Chinese medicine adapted to the alpine environment of the Qinghai-Tibet Plateau and adjacent regions. Clarification of the species diversity of Ophiocordyceps sinensis and its relatives could expand the traditional medicinal resources and provide insights into the speciation and adaptation. The study is prompted by the discovery of a new species, O. megala, described here from a biodiversity hotspot in the Hengduan Mountains, China. Combined morphological, ecological, and phylogenetic evidence supports its distinctiveness from O. sinensis, O. xuefengensis, and O. macroacicularis. Additionally, based on the phylogenetic construction of Ophiocordyceps, a special clade was focused phylogenetically on the more closely related O. sinensis complex, which was defined as the O. sinensis- species complex lineage. A total of 10 species were currently confirmed in this lineage. We made a comprehensive comparison of the sexual/asexual morphological structures among this species complex, distinguishing their common and distinctive features. Furthermore, using the method of species distribution modelling, we studied the species ocurrences in relation to climatic, edaphic, and altitudinal variables for the eight species in the O. sinensis-species complex, and determined that their potential distribution could extend from the southeastern Qinghai-Tibet Plateau to the Xuefeng Mountains without isolating barrier. Thus, the biodiversity corridor hypothesis was proposed around the O. sinensis-species complex. Our study highlights the phylogeny, species diversity, and suitable distribution of the O. sinensis-species complex lineage, which should have a positive implication for the resource discovery and adaptive evolution of this unique and valuable group. Supplementary Information The online version contains supplementary material available at 10.1186/s43008-023-00131-8.
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Epitypification and re-description of the zombie-ant fungus, Ophiocordyceps unilateralis (Ophiocordycipitaceae)
Article
Full-text available
  • Jun 2018
The type of Ophiocordyceps unilateralis (Ophiocordycipitaceae, Hypocreales, Ascomycota) is based on an immature specimen collected on an ant in Brazil. The host was identified initially as a leaf-cutting ant (Atta cephalotes, Attini, Myrmicinae). However, a critical examination of the original illustration reveals that the host is the golden carpenter ant, Camponotus sericeiventris (Camponotini, Formicinae). Because the holotype is no longer extant and the original diagnosis lacks critical taxonomic information - specifically, on ascus and ascospore morphology - a new type from Minas Gerais State of south-east Brazil is designated herein. A re-description of the fungus is provided and a new phylogenetic tree of the O. unilateralis clade is presented. It is predicted that many more species of zombie-ant fungi remain to be delimited within the O. unilateralis complex worldwide, on ants of the tribe Camponotini.
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Unravelling the Diversity behind the Ophiocordyceps unilateralis (Ophiocordycipitaceae) complex: Three new species of zombie-ant fungi from the Brazilian Amazon
Data
Full-text available
  • Jul 2015
In tropical forests, one of the most commonly encountered relationships between parasites and insects is that between the fungus Ophiocordyceps (Ophiocordycipitaceae, Hypocreales, Ascomycota) and ants, especially within the tribe Camponotini. Here, we describe three newly discovered host-specific species, Ophiocordyceps camponoti-atricipis, O. camponotibispinosi and O. camponoti-indiani, on Camponotus ants from the central Amazonian region of Brazil, which can readily be separated using morphological traits, in particular the shape and behavior of the ascospores. DNA sequence data support inclusion of these species within the Ophiocordyceps unilateralis complex.
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Ancient Tripartite Coevolution in the Attine Ant-Microbe Symbiosis
Article
Full-text available
  • Feb 2003
  • SCIENCE
The symbiosis between fungus-growing ants and the fungi they cultivate for food has been shaped by 50 million years of coevolution. Phylogenetic analyses indicate that this long coevolutionary history includes a third symbiont lineage: specialized microfungal parasites of the ants' fungus gardens. At ancient levels, the phylogenies of the three symbionts are perfectly congruent, revealing that the ant-microbe symbiosis is the product of tripartite coevolution between the farming ants, their cultivars, and the garden parasites. At recent phylogenetic levels, coevolution has been punctuated by occasional host-switching by the parasite, thus intensifying continuous coadaptation between symbionts in a tripartite arms race.
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The Life of a Dead Ant: The Expression of an Adaptive Extended Phenotype
Article
  • Sep 2009
Specialized parasites are expected to express complex adaptations to their hosts. Manipulation of host behavior is such an adaptation. We studied the fungus Ophiocordyceps unilateralis, a locally specialized parasite of arboreal Camponotus leonardi ants. Ant‐infecting Ophiocordyceps are known to make hosts bite onto vegetation before killing them. We show that this represents a fine‐tuned fungal adaptation: an extended phenotype. Dead ants were found under leaves, attached by their mandibles, on the northern side of saplings ∼25 cm above the soil, where temperature and humidity conditions were optimal for fungal growth. Experimental relocation confirmed that parasite fitness was lower outside this manipulative zone. Host resources were rapidly colonized and further secured by extensive internal structuring. Nutritional composition analysis indicated that such structuring allows the parasite to produce a large fruiting body for spore production. Our findings suggest that the osmotrophic lifestyle of fungi may have facilitated novel exploitation strategies.
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From So Simple a Beginning
Article
  • Feb 2016
  • Adv Genet
Parasites can manipulate the behavior of their hosts in ways that increase either their direct fitness or transmission to new hosts. The Kingdom Fungi have evolved a diverse array of strategies to manipulate arthropod behavior resulting in some of the most complex and impressive examples of behavioral manipulation by parasites. Here we provide an overview of these different interactions and discuss them from an evolutionary perspective. We discuss parasite manipulation within the context of Niko Tinbergen's four questions (function, phylogeny, causation, and ontogeny) before detailing the proximate mechanisms by which fungi control arthropod behavior and the evolutionary pathways to such adaptations. We focus on some systems for which we have recently acquired new knowledge (such as the zombie ant fungus, Ophiocordyceps unilateralis s.l.), but a major goal is also to highlight how many interesting examples remain to be discovered and investigated. With this in mind, we also discuss likely examples of manipulated spiders that are largely unexplored ("zombie spiders"). Armed with advanced tools in evolutionary biology (from serial block face SEM to RNAseq) we can discover how the fungi, a group of microbes capable of coordinated activity, have evolved the ability to direct animal behavior. In short, we have the ability to understand how the organism without the brain controls the one with the brain. We hope such a goal, coupled with the knowledge that many diverse examples of control exist, will inspire other organismal biologists to study the complex adaptations that have arisen from "so simple a beginning."
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Diversity of Entomopathogenic Fungi: Which Groups Conquered the Insect Body?
Chapter
  • Mar 2016
  • Adv Genet
The entomopathogenic fungi are organisms that evolved to exploit insects. They comprise a wide range of morphologically, phylogenetically, and ecologically diverse fungal species. Entomopathogenic fungi can be found distributed among five of the eight fungal phyla. Entomopathogens are also present among the ecologically similar but phylogenetically distinct Oomycota or water molds, which belong to a different kingdom, the Stramenopila. As a group of parasites, the entomopathogenic fungi and water molds infect a wide range of insect hosts, from aquatic larvae to adult insects from high canopies in tropical forests or even deserts. Their hosts are spread among 20 of the 31 orders of insects, in all developmental stages: eggs, larvae, pupae, nymphs, and adults. Such assortment of niches has resulted in these parasites evolving a considerable morphological diversity, resulting in enormous biodiversity, the majority of which remains unknown. Here we undertake a comprehensive survey of records of these entomopathogens in order to compare and contrast both their morphologies and their ecological traits. Our findings highlight a wide range of adaptations that evolved following the evolutionary transition by the fungi and water molds to infect the most diverse and widespread animals on Earth, the insects.
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Five new species of entomopathogenic fungi from the Amazon and evolution of neotropical Ophiocordyceps
Article
  • Jun 2015
The neotropical biogeographic zone is a ‘hot spot’ of global biodiversity, especially for insects. Fungal pathogens of insects appear to track this diversity. However, the integration of this unique component of fungal diversity into molecular phylogenetic analyses remains sparse. The entomopathogenic fungal genus Ophiocordyceps is species rich in this region with the first descriptions dating to the early nineteenth century. In this study, material from various ecosystems throughout Colombia and Ecuador was examined. Molecular phylogenetic analyses of five nuclear loci including SSU, LSU, TEF, RPB1 and RPB2 were conducted alongside a morphological evaluation. Thirty-five specimens were examined representing fifteen different species of Ophiocordyceps, and five new species, O. blattarioides, O. tiputini, O. araracuarensis, O. fulgoromorphila and O. evansii, were described. An accurate identification of the host allowed us to conclude that host identity and host habitat are positively correlated with phylogenetic species of Ophiocordyceps and are probably strong drivers for speciation of neotropical entomopathogenic fungi.
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