João P. M. Araújo

Phylogenetic-based nomenclatural proposals for Ophiocordycipitaceae (Hypocreales) with new combinations in Tolypocladium.

Ophiocordycipitaceae is a diverse family comprising ecologically, economically, medicinally, and culturally important fungi. The family was recognized due to the polyphyly of the genus Cordyceps and the broad diversity of the mostly arthropod-pathogenic lineages of Hypocreales. The other two cordyceps-like families, Cordycipitaceae and Clavicipitaceae, will be revised taxonomically elsewhere. Historically, many species were placed in Cordyceps, but other genera have been described in this family as well, including several based on anamorphic features. Currently there are 24 generic names in use across both asexual and sexual life stages for species of Ophiocordycipitaceae. To reflect changes in Art. 59 in the International Code of Nomenclature for algae, fungi, and plants (ICN), we propose to protect and to suppress names within Ophiocordycipitaceae, and to present taxonomic revisions in the genus Tolypocladium, based on rigorous and extensively sampled molecular phylogenetic analyses. When approaching this task, we considered the principles of priority, monophyly, minimizing taxonomic revisions, and the practical utility of these fungi within the wider biological research community.

Diversity of Entomopathogenic Fungi: Which Groups Conquered the Insect Body?

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.

Diversity of Entomopathogenic Fungi

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.

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

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 to 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.

Evidence for convergent evolution of host parasitic manipulation in response to environmental conditions

Environmental conditions exert strong selection on animal behavior. We tested the hypothesis that the altered behavior of hosts due to parasitic manipulation is also subject to selection imposed by changes in environmental conditions over time. Our model system is ants manipulated by parasitic fungi to bite onto vegetation. We analyzed the correlation between forest type (tropical vs. temperate) and the substrate where the host bites (biting substrate: leaf vs. twigs), the time required for the fungi to reach reproductive maturity, and the phylogenetic relationship among specimens from tropical and temperate forests from different parts of the globe. We show that fungal development in temperate forests is longer than the period of time leaves are present and the ants are manipulated to bite twigs. When biting twigs, 90% of the dead ants we examined had their legs wrapped around twigs, which appears to provide better attachment to the plant. Ancestral state character reconstruction suggests that leaf biting is the ancestral trait and that twig biting is a convergent trait in temperate regions of the globe. These three lines of evidence suggest that changes in environmental conditions have shaped the manipulative behavior of the host by its parasite.

Multiple new species of Ophiocordyceps on ants

In tropical forests, one of the most common relationships between parasites and insects is that between the fungus Ophiocordyceps (Ophiocordycipitaceae, Hypocreales, Ascomycota) and ants, especially within the tribe Camponotini. These fungi have the ability to penetrate the exoskeleton of the ant and to manipulate the behavior of the host, making it leave the nest and ascend understorey shrubs, to die biting onto the vegetation: hence, the term zombie-ant fungi to describe this behavioral changes on the host. It is posited that this behavioral change aids spore dispersal and thus increases the chances of infection. 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 three new and host-specific species of the genus Ophiocordyceps on Camponotus ants from the central Amazonian region of Brazil which can readily be separated using classic taxonomic criteria, in particular ascospore morphology. In addition, we also employed molecular techniques to show for the first time the phylogenetic relationships between these taxa and closely related species within the Ophiocordyceps unilateralis complex, as well as with other members of the family Ophiocordycipitaceae.

Record of Ophiocordyceps unilateralis sensu lato, the zombie-ant fungus, parasitizing Camponotus in an urban fragment of Atlantic Rainforest in southeastern Brazil

Ophiocordyceps is a fungal pathogen of ants of the tribe Camponotini. It is called zombie fungus, since it changes the host behavior, causing them to die in an exposed position, typically clinging onto and biting into the adaxial surface of shrub leaves. This study aimed to describe the occurrence of parasitic associations between Ophiocordyceps and ants of the genus Camponotus in an urban fragment of Atlantic Rainforest in southeastern Brazil and to measure the rate of hyperparasitism in Ophiocordyceps by other fungi in the same location. We found 57 individuals of four species of ants and three species of fungus. The age categories of fungi were equally distributed, and rate of hyperparasitism was 17.5% (n = 10). The sampled area was recognized as an important site of Ophiocordyceps occurrence.

Complex behavioral manipulation drives mismatch between host and parasite diversity

Parasites and hosts are intimately associated such that changes in the diversity of one partner are thought to lead to changes in the other. We investigated this linked diversity hypothesis in a specialized ant-Ophiocordyceps system in three forests across 750 km in Central Amazonia. All species belonging to the fungal genus Ophiocordyceps associated with ants have evolved some degree of behavioral control to increase their own transmission, but the leaf-biting behavior is the most complex form of host manipulation. Such a system requires control of the mandibular muscles and a distinct shift in behavior, from climbing vegetation to walking on leaves to rasping leaf veins in the seconds before death. The need to induce complex behavior may limit host availability and represent a constraint on parasite diversity. The consequence for community structure is that complex behavioral manipulation leads to a mismatch between ant hosts and the diversity of their fungal parasites.

Unravelling the diversity behind Ophiocordyceps unilateralis complex: Three new species of Zombie-Ant fungus from Brazilian Amazon

In tropical forests, one of the most common 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 new and host-specific species of the genus Ophiocordyceps on Camponotus ants from the central Amazonian region of Brazil, which can readily be separated using morphological traits, in particular, ascospore form and function. In addition, we use sequence data to infer phylogenetic relationships between these taxa and closely related species within the Ophiocordyceps unilateralis complex, as well as with other members of the family Ophiocordycipitaceae.