Cordyceps unilateralis
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''Ophiocordyceps unilateralis'', commonly known as zombie-ant fungus, is an insect-pathogenic fungus, discovered by the British naturalist
Alfred Russel Wallace Alfred Russel Wallace (8 January 1823 – 7 November 1913) was a British naturalist, explorer, geographer, anthropologist, biologist and illustrator. He is best known for independently conceiving the theory of evolution through natural se ...
in 1859, and currently found predominantly in
tropical forest Tropical forests (a.k.a. jungle) are forested landscapes in tropical regions: ''i.e.'' land areas approximately bounded by the tropic of Cancer and Capricorn, but possibly affected by other factors such as prevailing winds. Some tropical fores ...
ecosystems. ''O. unilateralis'' infects ants of the tribe
Camponotini Camponotini is a tribe containing 2 extinct ant genera and 8 extant ant genera, including '' Camponotus'' (carpenter ants). Genera * ''Calomyrmex'' Emery, 1895 * '' Camponotus'' Mayr, 1861 * †''Chimaeromyrma'' Dlussky, 1988 * ''Colobopsis'' Ma ...
, with the full pathogenesis being characterized by alteration of the behavioral patterns of the infected ant. Infected hosts leave their canopy nests and foraging trails for the forest floor, an area with a temperature and humidity suitable for fungal growth; they then use their
mandible In anatomy, the mandible, lower jaw or jawbone is the largest, strongest and lowest bone in the human facial skeleton. It forms the lower jaw and holds the lower tooth, teeth in place. The mandible sits beneath the maxilla. It is the only movabl ...
s to attach themselves to a major vein on the underside of a leaf, where the host remains after its eventual death. The process leading to mortality takes 4–10 days, and includes a reproductive stage where fruiting bodies grow from the ant's head, rupturing to release the fungus's spores. ''O. unilateralis'' is, in turn, also susceptible to fungal infection itself, an occurrence that can limit its impact on ant populations, which has otherwise been known to devastate ant colonies. ''Ophiocordyceps unilateralis'' and related species are known to engage in an active secondary metabolism, among other reasons, for the production of substances active as antibacterial agents that protect the fungus-host ecosystem against further pathogenesis during fungal reproduction. Because of this secondary metabolism, an interest in the species has been taken by
natural product A natural product is a natural compound or substance produced by a living organism—that is, found in nature. In the broadest sense, natural products include any substance produced by life. Natural products can also be prepared by chemical syn ...
s chemists, with corresponding discovery of small molecule agents (e.g. of the polyketide family) of potential interest for use as human immunomodulatory, anti-infective, and anticancer agents.


Systematics

After years of research, the taxonomy of ''Ophiocordyceps unilateralis'' is becoming increasingly clear.


''Cordyceps'' vs ''Ophiocordyceps''

Throughout history there has been confusion about the distinction between the
genera Genus ( plural genera ) is a taxonomic rank used in the biological classification of living and fossil organisms as well as viruses. In the hierarchy of biological classification, genus comes above species and below family. In binomial nomenclat ...
''
Cordyceps ''Cordyceps'' is a genus of ascomycete fungi (sac fungi) that includes about 600 species. Most ''Cordyceps'' species are endoparasitoids, parasitic mainly on insects and other arthropods (they are thus entomopathogenic fungi); a few are parasiti ...
'' and ''
Ophiocordyceps ''Ophiocordyceps'' is a genus of fungi within the family Ophiocordycipitaceae. The widespread genus, first described scientifically by British mycologist Tom Petch in 1931, contains about 140 species that grow on insects. Anamorphic genera that c ...
''. There have been many debates about whether the zombie-ant fungus (and other fungi) belonged to one or to the other as ''Ophiocordyceps'' was only recently brought forward. The genus ''Cordyceps'' comprises over 400 species, historically classified in the family Clavicipitaceae within the order
Hypocreales The Hypocreales are an order of fungi within the class Sordariomycetes. In 2008, it was estimated that it contained some 237 genera, and 2647 species in seven families. Since then, a considerable number of further taxa have been identified, in ...
. The classification was based on different morphological characteristics such as filiform ascospores and cylindrical
asci ASCI or Asci may refer to: * Advertising Standards Council of India * Asci, the plural of ascus, in fungal anatomy * Accelerated Strategic Computing Initiative * American Society for Clinical Investigation * Argus Sour Crude Index * Association of ...
. When ''Cordyceps'' were first classified, there was no concrete evidence for the genus ''Ophiocordyceps''. However, in 2007, important new molecular data was tested, and enabled them to reorganize the family Clavicipitaceae. It was found that Clavicipitaceae was in fact three distinct
monophyletic In cladistics for a group of organisms, monophyly is the condition of being a clade—that is, a group of taxa composed only of a common ancestor (or more precisely an ancestral population) and all of its lineal descendants. Monophyletic gro ...
families: the Clavicipitaceae, the Cordycipitaceae and the Ophiocordycipitaceae. The new molecular phylogenetics studies contradicted the older classification and moved all ''Cordyceps'' species forming a sister group with '' Tolypocladium'', into Ophiocordycipitaceae. Fungi able to parasitize ants were also included in the transfer, such as ''Cordyceps unilateralis'' which was later renamed ''Ophiocordyceps unilateralis''. Following this study, multiple traits such as the production of darkly pigmented, hard to flexible
stromata The ''Stromata'' ( el, Στρώματα), a mistake for ''Stromateis'' (Στρωματεῖς, "Patchwork," i.e., ''Miscellanies''), attributed to Clement of Alexandria (c. 150 – c. 215), is the third of a trilogy of works regarding the Christ ...
were defined as characteristics of the family Ophiocordycipitaceae.


''Ophiocordyceps unilateralis sensu lato''

The fungus' scientific name is sometimes written as ''Ophiocordyceps unilateralis sensu lato'', which means 'in the broad sense', because the species actually represents a complex of many species within ''O. unilateralis''. Support for this term has become increasingly important. In 2011, it was hypothesized that the zombie-ant fungus could actually be described as a complex of species which are host-specific, meaning that one ''O. unilateralis'' species can only successfully infect and manipulate one host ant species. There is a possibility that this resulted in or re-inforced the
reproductive isolation The mechanisms of reproductive isolation are a collection of evolutionary mechanisms, behaviors and physiological processes critical for speciation. They prevent members of different species from producing offspring, or ensure that any offspring ...
of the fungi, leading to its
speciation Speciation is the evolutionary process by which populations evolve to become distinct species. The biologist Orator F. Cook coined the term in 1906 for cladogenesis, the splitting of lineages, as opposed to anagenesis, phyletic evolution within ...
. Following this, a study conducted in Brazil delimited using morphological comparison of the ascospores, germination process and asexual morphs, four different ''Ophiocordyceps'' species. Afterwards, three new species were described in the Brazilian Amazon, six in Thailand, and one in Japan. More recently in 2018, 15 new ''O. unilateralis'' species were described based on classic taxonomic criteria, and macro-morphological data with a deeper focus on ascospore and asexual morphology. The asexual morphologies made it possible to distinguish two different
clades A clade (), also known as a monophyletic group or natural group, is a group of organisms that are monophyletic – that is, composed of a common ancestor and all its lineal descendants – on a phylogenetic tree. Rather than the English term, t ...
mainly composed of species associated with ants which they termed "''O. unilateralis'' core clade" and "''O. kniphofioides'' subclade". Further analyses were conducted using a set of different traits. Morphological traits were used and included both macro-morphological characters (e.g. typical single stroma arising from the host's dorsal pronotum, the ascoma (perithecia) growing from the storm) and microscopic traits (e.g. the morphology of the ascospores in terms of size, shape,
septation In biology, a septum (Latin for ''something that encloses''; plural septa) is a wall, dividing a cavity or structure into smaller ones. A cavity or structure divided in this way may be referred to as septate. Examples Human anatomy * Interatri ...
and germination). Moreover, other traits such as the host and the location of the death grip were added to the analyses. The morphological study led to 15 new identified species, with 14 which were distributed in the core clade, and one in the subclade. Moreover, it was found that species in the ''O. kniphofioides'' subclade specialise on neotropical ants, whereas species in the core clade specialise on ''Camponotini'' species. Species within the ''O. unilateralis'' core clade as described in 2018: * ''O. albacongiuae'' * ''O. blakebarnesii'' * ''O. camponoti-atricipis'' * ''O. camponoti-balzani'' * ''O. camponoti-bispinosi'' * ''O. camponoti-chartificis'' * ''O. camponoti-femorati'' * ''O. camponoti-floridani'' * ''O. camponoti-hippocrepidis'' * ''O. camponoti-indiani'' * ''O. camponoti-leonardi'' * ''O. camponoti- melanotic'' * ''O. camponoti-nidulantis'' * ''O. camponoti-novogranadensis'' * ''O. camponoti-renggeri'' * ''O. camponoti-saundersi'' * ''O. halabalaensis'' * ''O. kimflemingiae'' * ''O. naomipierceae'' * ''O. ootakii'' * ''O. polyrhachis-furcata'' * ''O. pulvinata'' * ''O. rami'' * ''O. satoi'' Species within the ''O. kniphofioides'' subclade as described in 2018: * ''O. daceti'' * ''O. kniphofioides''


Morphology


Typical morphology

The zombie-ant fungus is easily identifiable when its reproductive structure becomes apparent on its dead host, usually a carpenter ant. At the end of its life cycle, ''O. unilateralis'' typically generates a single, wiry yet pliant, darkly pigmented stroma which arises from the dorsal pronotum region of the ant once it is dead. Moreover, perithecia, the spore-bearing sexual structure, can be observed on the stalk, just below its tip. This complex forms the fungus' fruiting body. Most species within the ''O. unilateralis s.l.'' species complex have both a sexual ( teleomorph) and an asexual morph (
anamorph In mycology, the terms teleomorph, anamorph, and holomorph apply to portions of the life cycles of fungi in the phyla Ascomycota and Basidiomycota: *Teleomorph: the sexual reproductive stage (morph), typically a fruiting body. *Anamorph: an ase ...
). These are different in terms of their function and characteristics. Generally, the asexual morphs identified for ''Ophiocordyceps'' are '' Hirsutella'' and ''
Hymenostilbe ''Hymenostilbe'' is a genus of fungi in the Ophiocordycipitaceae family. All members are anamorph names of ''Ophiocordyceps ''Ophiocordyceps'' is a genus of fungi within the family Ophiocordycipitaceae. The widespread genus, first described s ...
'', two genera of asexually reproducing fungi.


Morphological variation

''O. unilateralis'' species exhibit morphological variations which are most certainly due to their wide geographic range, from Japan to the Americas. Moreover, it has been hypothesized that their morphological variations may also be a result of one fungus species maximizing its infection on one specific host ant species (host-specific infections). Different
subspecies In biological classification, subspecies is a rank below species, used for populations that live in different areas and vary in size, shape, or other physical characteristics (morphology), but that can successfully interbreed. Not all species ...
of ant can occur within the same area, which means that in order to coexist they have to occupy different
ecological niches In ecology, a niche is the match of a species to a specific environmental condition. Three variants of ecological niche are described by It describes how an organism or population responds to the distribution of resources and competitors (for ...
. Consequently, the fungi may have evolved at the subspecies level in order to maximize its fitness.


''O. unilateralis'' core clade morphological characteristics

The ''O. unilateralis'' core clade, as described in 2018, has distinct morphological characteristics. It exhibits a single stroma with a ''Hirsutella'' asexual morph, which arises from the dorsal neck region of the dead ant and produces a dark brown perithecia attached to its stalk. These species are also recognizable through the host species they infect, which are only ''Camponotini'' species. Once the host is killed by the fungus, it is commonly found fixed through their mandibles onto the surfaces of leaves.


''O. kniphofioides'' subclade morphological characteristics

The ''O. kniphofioides'' subclade, as described in 2018, also has distinct morphological characteristics. Its species produce a stroma that grows laterally from the host's thorax which itself generates an orange ascoma. Moreover, species within this subclade share a ''Hirsutella'' asexual morph. As for the core clade, these species are also recognizable through the hosts they infect, which are usually neotropical ant species. The subclade does not present the same extended phenotype with the famous "death grip" that O. unilateralis species typically exhibit. Their hosts usually die at the base of large trees in the Amazonian rainforest, among the moss carpets.


Life cycle

In tropical forests, the ant species ''Camponotus leonardi'' lives in the high canopy and has an extensive network of aerial trails. Sometimes the canopy gaps are too difficult to cross, so the ants' trails descend to the forest floor where they are exposed to ''O. unilateralis'' spores. The spores attach to their
exoskeleton An exoskeleton (from Greek ''éxō'' "outer" and ''skeletós'' "skeleton") is an external skeleton that supports and protects an animal's body, in contrast to an internal skeleton (endoskeleton) in for example, a human. In usage, some of the ...
s and eventually break through using mechanical pressure and enzymes. Like other fungi pathogenic to insects in the genus ''Ophiocordyceps'', the fungus targets a specific host species, ''Camponotus leonardi''; despite this, the fungus may parasitize other closely related species of ants with lesser degrees of host manipulation and reproductive success. Yeast stages of the fungus spread in the ant's body and presumably produce compounds that affect the ant's
hemocoel The blood circulatory system is a organ system, system of organs that includes the heart, blood vessels, and blood which is circulated throughout the entire body of a human or other vertebrate. It includes the cardiovascular system, or vascula ...
, using the evolutionary trait of an
extended phenotype ''The Extended Phenotype'' is a 1982 book by the evolutionary biologist Richard Dawkins, in which the author introduced a biological concept of the same name. The main idea is that phenotype should not be ''limited'' to biological processes such ...
to manipulate the behavioral patterns exhibited by the ant. An infected ant exhibits irregularly timed full-body convulsions that dislodge it from its canopy nest to the forest floor. The changes in the behavior of the infected ants are very specific, giving rise to the popular term "zombie ants". Behaviors are tuned for the benefit of the fungus in terms of its growth and its transmission, thereby increasing its fitness. The ant climbs up the stem of a plant and uses its mandibles with abnormal force to secure itself to a leaf vein, leaving dumbbell-shaped marks on it. The ants generally clamp to a leaf's vein at a height of 26cm above the forest floor, on the northern side of the plant, in an environment with 94–95% humidity and temperatures between . Infections may lead to 20 to 30 dead ants per square meter. When the dead ants are moved to other places and positions, further vegetative growth and sporulation either fails to occur or results in undersized and abnormal reproductive structures. In
temperate forest A temperate forest is a forest found between the tropical and boreal regions, located in the temperate zone. It is the second largest biome on our planet, covering 25% of the world's forest area, only behind the boreal forest, which covers abou ...
s, the typical behaviour of zombie ants is to attach themselves to the lower side of twigs, not leaves. A search of plant-fossil databases revealed similar marks on a fossil leaf from the Messel Pit, which is 48 million years old. Once the mandibles of the ant are secured to the leaf vein,
atrophy Atrophy is the partial or complete wasting away of a part of the body. Causes of atrophy include mutations (which can destroy the gene to build up the organ), poor nourishment, poor circulation, loss of hormonal support, loss of nerve supply t ...
quickly sets in, destroying the sarcomere connections in the muscle fibers and reducing the
mitochondria A mitochondrion (; ) is an organelle found in the Cell (biology), cells of most Eukaryotes, such as animals, plants and Fungus, fungi. Mitochondria have a double lipid bilayer, membrane structure and use aerobic respiration to generate adenosi ...
and sarcoplasmic reticular. The ant is no longer able to control the muscles of the mandible and remains fixed in place, hanging upside-down on the leaf. This lockjaw trait is popularly known as the death grip and is essential in the fungus's lifecycle. A study led in Thailand revealed that there is a synchronization of this manipulated biting behavior at solar noon. The fungus then kills the ant and continues to grow as its
hyphae A hypha (; ) is a long, branching, filamentous structure of a fungus, oomycete, or actinobacterium. In most fungi, hyphae are the main mode of vegetative growth, and are collectively called a mycelium. Structure A hypha consists of one or ...
invade more soft tissues and structurally fortify the ant's exoskeleton. More
mycelia Mycelium (plural mycelia) is a root-like structure of a fungus consisting of a mass of branching, thread-like hyphae. Fungal colonies composed of mycelium are found in and on soil and many other substrates. A typical single spore germinates in ...
then sprout out of the ant, securely anchoring it to the plant substrate while secreting antimicrobials to ward off competition. When the fungus is ready to reproduce, its fruiting bodies grow from the ant's head and rupture, releasing the spores. This process takes 4–10 days. Dead ants are found in areas termed "graveyards" which contain high densities of dead ants previously infected by the same fungus. The term "zombie ants" has been used in popular media as well as scientific articles, but has also been described as "catchy, yet misleading".


Natural products

''O. unilateralis life cycle includes and depends on the infection and the manipulation of a carpenter ant, principally ''C. leonardi''. The behavioral manipulation of the ant, which gives rise to the name "zombie-ant", is an extended phenotype of the fungus. It first affects the ant's behavior through convulsions that make it fall from its high canopy nest onto the forest floor. This is followed by the fungus controlling the climbing of the ant and the locking of its jaw (and subsequent death) onto a leaf around 25 centimetres above the ground, which is thought to be the optimal height for fungal spore growth and dispersion. Throughout the lifecycle, unique challenges must be met by equally unique metabolic activities. The fungal pathogen must attach securely to the arthropod exoskeleton and penetrate it—avoiding or suppressing host defenses—then, control the behavior of the host before killing it; and finally, it must protect the carcass from microbial and scavenger attack. The behavioral manipulation of the ant would not be possible without the presence of huge fungal cell populations beside the host's brain and within muscles because these lead to the secretion of various metabolites known to have important behavioral consequences. During the infection the parasite comes across an array of environments such as different host tissues or the
immune response An immune response is a reaction which occurs within an organism for the purpose of defending against foreign invaders. These invaders include a wide variety of different microorganisms including viruses, bacteria, parasites, and fungi which could ...
. Studies have shown that ''O. unilateralis'' reacts heterogeneously by secreting different metabolites according to the host tissue it encounters and whether they are live or dead. The identification of these natural products is important in order to understand which aspects of the ants are under control and consequently how ''O. unilateralis'' manipulates the ant. More in depth research is needed for the identification of other fungal compounds which act to atrophy the mandibular muscles, and for the understanding of their exact effects on the ant.


Natural products are host specific

Effects of ''O. unilateralis'' on host have been found to vary according to host species. The ant species which are normally found infected in nature exhibit a manipulated behavior, whereas the species which are not typically infected are killed by the infection, but their behaviour is not altered. This is likely due to the heterogeneous nature of the fungus which secretes different metabolites according to host species.


Geographic distribution

Many studies describe ''Ophiocordyceps unilateralis'' distribution as
pantropical A pantropical ("all tropics") distribution is one which covers Tropics, tropical regions of both hemispheres. Examples of species include caecilians, modern sirenians and the plant genera ''Acacia'' and ''Bacopa''. ''Neotropical'' is a zoogeogra ...
since it occurs mainly in
tropical forest Tropical forests (a.k.a. jungle) are forested landscapes in tropical regions: ''i.e.'' land areas approximately bounded by the tropic of Cancer and Capricorn, but possibly affected by other factors such as prevailing winds. Some tropical fores ...
ecosystems. However, there are some reports of the zombie-ant fungus in warm-temperate ecosystems. Its distribution includes tropical rainforests located in Brazil, Australia and Thailand, and
temperate forest A temperate forest is a forest found between the tropical and boreal regions, located in the temperate zone. It is the second largest biome on our planet, covering 25% of the world's forest area, only behind the boreal forest, which covers abou ...
s found in South Carolina, Florida and Japan.


Host impact

When ''O. unilateralis''-infected ants die, they are mainly located in regions containing a high density of ants which were previously manipulated and killed. These areas are termed "graveyards" and can be of 20 to 30 meters in range (with a local density of dead ants possibly exceeding 25 meters square). The density of dead ants within these graveyards can vary according to climatic conditions. This means that environmental conditions such as humidity and temperature can influence ''O.unilateralis'' effects on the host population. In fact, studies have described seasonal patterns in the density of previously infected dead ants, with an increase during the rainy season and a decrease during the dry season. It is thought that large precipitation events at the beginning and the end of the rainy season stimulates fungal development, which leads to more spores being released and ultimately more individuals being infected and killed.


Medicinal potential

''Ophiocordyceps'' are known in the pharmaceutical world to be a medically-important group. ''O. unilateralis'' fungi produce various known secondary metabolites, as well as several structurally uncharacterised substances. These natural products are reportedly being investigated as potential leads in discovery efforts toward immunomodulatory,
antitumor Cancer can be treated by surgery, chemotherapy, radiation therapy, hormonal therapy, targeted therapy (including immunotherapy such as monoclonal antibody therapy) and synthetic lethality, most commonly as a series of separate treatments (e.g. ...
,
hypoglycemic Hypoglycemia, also called low blood sugar, is a fall in blood sugar to levels below normal, typically below 70 mg/dL (3.9 mmol/L). Whipple's triad is used to properly identify hypoglycemic episodes. It is defined as blood glucose belo ...
, and
hypocholesterolemic Lipid-lowering agents, also sometimes referred to as hypolipidemic agents, cholesterol-lowering drugs, or antihyperlipidemic agents are a diverse group of pharmaceuticals that are used to lower the level of lipids and lipoproteins such as cholestero ...
targets. In an ''Ophiocordyceps'' species within Japanese cicadas, the ''Ophiocordyceps'' replaces the symbiotic bacteria within the cicadas to help the host process sap as nutrients, unlike other related species, such as the ''Ophiocordyceps sinensis'', which is a traditional immune booster and cancer treatment in Tibetan and Chinese culture.


Naphthoquinone derivatives

Naphthoquinone derivatives are an example of secondary metabolite with important pharmaceutical potentials produced by ''O. unilateralis''. Six known naphthoquinone derivatives have been isolated from ''O. unilateralis'', namely erythrostominone, deoxyerythrostominone, 4-''O''-methyl erythrostominone, epierythrostominol, deoxyerythrostominol, and 3,5,8-trihydroxy-6-methoxy-2-(5-oxohexa-1,3-dienyl)-1,4-naphthoquinone, which have shown activity in ''
in vitro ''In vitro'' (meaning in glass, or ''in the glass'') studies are performed with microorganisms, cells, or biological molecules outside their normal biological context. Colloquially called "test-tube experiments", these studies in biology an ...
'' assays related to antimalarial drug discovery. In addition to having antimalarial activities, all six of these secondary metabolites have been demonstrated to have anticancer and antibacterial activities. Moreover, the use of red naphthoquinone pigments produced by ''O. unilateralis'' has been studied as a dye for food, cosmetic, and pharmaceutical manufacturing processes. In fact, naphthoquinone derivatives produced by the fungus show a red color under acidic conditions, and a purple color under basic conditions. These pigments are stable against
acid In computer science, ACID ( atomicity, consistency, isolation, durability) is a set of properties of database transactions intended to guarantee data validity despite errors, power failures, and other mishaps. In the context of databases, a sequ ...
/
alkaline In chemistry, an alkali (; from ar, القلوي, al-qaly, lit=ashes of the saltwort) is a base (chemistry), basic, ionic compound, ionic salt (chemistry), salt of an alkali metal or an alkaline earth metal. An alkali can also be defined as ...
conditions and light and are not
cytotoxic Cytotoxicity is the quality of being toxic to cells. Examples of toxic agents are an immune cell or some types of venom, e.g. from the puff adder (''Bitis arietans'') or brown recluse spider (''Loxosceles reclusa''). Cell physiology Treating cells ...
, which makes them applicable for food coloring and as a dye for other materials. These attributes also make it a prime candidate for antituberculosis testing in secondary TB patients, by improving symptoms and enhancing immunity when combined with
chemotherapeutic drugs Chemotherapy (often abbreviated to chemo and sometimes CTX or CTx) is a type of cancer treatment that uses one or more anti-cancer drugs (chemotherapeutic agents or alkylating agents) as part of a standardized chemotherapy regimen. Chemotherap ...
.


Polyketides

In 2009, a study showed that ''O. unilateralis'' also produces polyketides. These secondary metabolites have been used in antibiotics such as patulin, cholesterol medication such as
compactin Mevastatin (compactin, ML-236B) is a hypolipidemic agent that belongs to the statins class. It was isolated from the mold ''Penicillium citrinum'' by Akira Endo in the 1970s, and he identified it as a HMG-CoA reductase inhibitor, i.e., a statin. ...
, and antifungal treatments. It has also been reported that polyketides have other therapeutic effects such as antitumor, antioxidant and antiaging activities.


Fungal hyperparasite

''O. unilateralis'' suffers from an unidentified fungal
hyperparasite A hyperparasite, also known as a metaparasite, is a parasite whose host, often an insect, is also a parasite, often specifically a parasitoid. Hyperparasites are found mainly among the wasp-waisted Apocrita within the Hymenoptera, and in two othe ...
, reported in the lay press as the "antizombie-fungus fungus", that results in only 6–7% of
sporangia A sporangium (; from Late Latin, ) is an enclosure in which spores are formed. It can be composed of a single cell or can be multicellular. Virtually all plants, fungi, and many other lineages form sporangia at some point in their life cy ...
being viable, limiting the damage ''O. unilateralis'' inflicts on ant colonies. The hyperparasite moves in to attack ''O. unilateralis'' as the fungal stalk emerges from the ant's body, which can stop the stalk from releasing its spores. The graveyards of dead ants are numerous and spread throughout the surrounding area of the colony. Though ''O. unilateralis'' is very virulent, only about 6.5% of all fruiting bodies are viable spore producers. This is caused by the weakening of the fungus by the hyperparasite, which may limit the viability of infectious spores. Ants also groom each other to combat microscopic organisms that could potentially harm the colony. Additional fungi grant beneficial assistance to the colony, as well.


Parasite adaptation

In hostparasite dynamics, both the host and the parasite are under selective pressure: the parasite evolves to increase its transmission, whereas the host evolves to avoid and/or resist the infection by the parasite.


Extended phenotype

Some parasites have evolved to manipulate their host's behavior in order to increase their transmission to uninfected susceptible individuals, thereby increasing their fitness. This host manipulation is termed the "extended phenotype" of the parasite and is a form of adaptation. Host ant manipulation by ''O. unilateralis'' represents one of the best-known examples of extended phenotypes. The extended phenotype of ''O. unilateralis'' typically depicts the infected ant leaving its canopy nest and its normal foraging path to reach the forest floor and subsequently climb up 25 cm above ground level. This height is considered to be optimal for fungal growth due to its humidity level and temperature. This is followed by a "death grip" of the infected ant once it is to be found at what are considered to be optimal conditions for post-mortem fungal development. This leads to the fungus continuing its growth and releasing fungal spores onto the forest floor. These spores will then be encountered by the ants which, when the aerial foraging route is not possible, have to occasionally descend to ground level. Therefore, ''O. unilateralis'' controls the ant's behaviour and this manipulation represents an adaptation for the fungus where
natural selection Natural selection is the differential survival and reproduction of individuals due to differences in phenotype. It is a key mechanism of evolution, the change in the heritable traits characteristic of a population over generations. Charle ...
acts on its
genes In biology, the word gene (from , ; "...Wilhelm Johannsen coined the word gene to describe the Mendelian units of heredity..." meaning ''generation'' or ''birth'' or ''gender'') can have several different meanings. The Mendelian gene is a ba ...
, increasing the fungus' fitness.


Somatic investment

Some studies proposed a theory in which ''O. unilateralis'' has another possible form of adaptation which ensures its repeated reproduction. This would be crucial for ''O. unilateralis s.l.'' species as they can produce and release within the air, clear and thin-walled spores which are susceptible to environmental conditions such as
UV radiation Ultraviolet (UV) is a form of electromagnetic radiation with wavelength from 10 nm (with a corresponding frequency around 30  PHz) to 400 nm (750  THz), shorter than that of visible light, but longer than X-rays. UV radiation i ...
and dryness. In fact, studies suggest that the short viability of the fungal spores lead to the need of
somatic Somatic may refer to: * Somatic (biology), referring to the cells of the body in contrast to the germ line cells ** Somatic cell, a non-gametic cell in a multicellular organism * Somatic nervous system, the portion of the vertebrate nervous sys ...
investment (growth/survival) by the parasite in order to sustain the growth of the fungus' fruiting body on its host, thereby enabling successive reproduction. To do so, ''O. unilateralis'' fortifies the ant cadaver to prevent its decay, which consequently ensures the growth of the fruiting body. Therefore, the zombie-ant fungus adapts to the short viability of its spores by increasing their production using the dead ant.


Host adaptation

The principal hosts of ''O. unilateralis'' evolved adaptive behaviours able to limit the contact rate between uninfected susceptible hosts and infected hosts, thereby reducing the risk of transmission. ''O.unilateralis'' principal hosts evolved efficient behavioral forms of social immunity. In fact, the ants clean the exoskeletons of one another in order to decrease the presence of spores which are attached to their cuticle. Also, ants can sense that a member of the colony is infected, resulting in healthy ants carrying the ''O. unilateralis''-infected individual far away from the colony to avoid fungal spore exposure. Plus, there are reports testifying that most worker ants remain inside the nest boundaries; consequently, only foragers are at risk of infection. Moreover, one of the fungus' principal hosts, ''Camponotus leonardi'', provided evidence for the avoidance of the forest floor by the host ants as a defence method. In areas where ''O. unilateralis'' is present, ''C. leonardi'' builds its nests high in the canopy, and has a broad network of aerial trails. These trails occasionally move down to the ground level, where infection and graveyards occur, due to canopy gaps too difficult for the ants to cross. When the trails descend to the forest floor, their length is only of three to five meters before going back up into the canopy. This demonstrates the avoidance of the zones of infection by the ants. Additionally, more evidence participates in the favour of this defence method being adaptive as it is not observed in undisturbed forests where the zombie-ant fungus is not present.


See also

* Massospora cicadina


References


Further reading

* * * * *


External links


Ophiocordyceps unilateralis
at UniProt.org. Accessed on 2010-08-22.
An Electronic Monograph of Cordyceps and Related Fungi
{{Taxonbar, from=Q127353 Fungi described in 1865 Fungi of Africa Fungi of Asia Fungi of South America Ophiocordycipitaceae Mind-altering parasites Parasitic fungi Suicide-inducing parasitism