Ophiocordyceps unilateralis: Zombie Fungi

Pathogens make up a significant portion of biodiversity worldwide and have independently developed to take advantage of various host lineages (plants, animals, insects, etc.). For diseases to be managed, it is essential to comprehend how they change over time, especially how new species emerge. The idea of host specificity refers to the tendency of the parasite to appear on one or a small number of host species as a result of the coexistence and coevolution of both parasite and host lineages [1]. It has been demonstrated that several “generalist” parasites that are connected to a variety of hosts exhibit variable degrees of host specificity, even demonstrating enough genetic difference across host-specific lineages to be regarded as host-race lineages. Thus, hosts could be considered to be a key factor in the speciation and diversification of parasites [2,3].

Figure 1: Ant fungus Ophiocordyceps unilateralis. (August 8, 2011), Access Date: 19.12.2022

There are many cases of harmful fungi becoming adapted to their host, and they are observed in a wide variety of taxonomic affiliations [4-6]. Entomopathogenic fungi are parasites that only affect insects. Insect-parasitizing fungi known as hypocrealeans (from the Order Hypocreales) first evolved independently in various lineages of the order, with fossil evidence of their connection dating from the Early Cretaceous [7]. Given the parasite’s host-specificity, it would be expected to see genetic diversity in a parasite species that infect many host species and displays symptoms of host infection. Due to their potential for commercialization and bioactive ingredients, Cordyceps and Ophiocordyceps are the focus of the majority of investigations on tropical species. The ascomycete fungal diseases of arthropods with sexual spore-producing structures (ascospores) in or on noticeable stalks (stromata) emerging from the host corpses were the main forces for the genus Cordyceps formation [8].

A parasitic fungus species named Ophiocordyceps unilateralis (Clavicipitaceae: Hypocreales), this term was given to the sexual state (also known as the “teleomorph”), also the Hirsutella formicarum term was given to the asexual state (also known as the “anamorph”) of the organism, which is distributed in both hemispheres’ tropical regions have been consistently explored for its zombie-like infection (altering the behavior of the ants to facilitate its propagation concerns) property and nerve system manipulations on formicine ants (Formicinae, Hymenoptera) although entomopathogenic fungus species are unquestionably rare [9-13].

The host’s behavior is altered by this “quasi-zombie” effect, which causes them to die while clinging to or biting onto the adaxial surface of plant leaves in a hanging position.

Figure 2: An illustration of the natural compounds released by Ophiocordyceps unilateralis’s modulation of ant behavior. (April 15, 2020), Access Date: 23.12.2022

The relationship between formicine ants and Ophiocordyceps unilateralis is an intriguing demonstration of how parasites might influence host behavior in order to improve their fitness [11], [13]. Infected ants turn away from their colonies and foraging pathways on a global scale, exhibiting unpredictable behavior. They climb trees, use their mandibles to bite the leaves, and hang upside down until they die [14,15]. As fungal stroma grows on the back of the ant’s head, making it easier for ascospores to disperse to the soil, this is thought to be an adaptation of the fungus to control the ant’s behavior and boost the dispersal ability of its spores [15].

Ophiocordyceps unilateralis’s taxonomical status is not entirely apparent. The leaf-cutting ant Atta cephalotes, which was initially mistaken for the carpenter ant Camponotus sericeiventris, was the subject of the type specimen’s first description [16,17].  O. unilateralis has only been observed in ants of the tribe Camponotini (Formicinae, Formicidae) in the past  [8,14,18].  Carpenter ants, especially Camponotus leonardi, are the primary hosts of Ophiocordyceps unilateralis, according to earlier research on the ant species that was carried out in southern Thailand, with a few Polyrhachis ants also showing modest supplementary infections [11,12].

In recent observations, this fungus was found on four different Camponotus species in Brazil. As a result, Ophiocordyceps unilateralis appears to be a complex species with a remarkable local diversity of related hosts and a global range. It is conceivable that Ophiocordyceps unilateralis has a preference for particular ant species, which could result in speciation. 

To respond to these challenges, samples from various Camponotus and Polyrhachis ant species found in northeastern Thailand were used to rearrange the molecular phylogeny of Ophiocordyceps unilateralis [1].

After the observations and studies conducted with the samples of O. unilateralis⁄H. Formicarum, a series of methods were performed to see whether the host ant differentiation complexity. In this study, the first molecular phylogenetic studies of populations of Ophiocordyceps unilateralis and H. formicarum infecting various formicine ant species were performed [17]. The results demonstrate genetic divergence within this species’ complexity by the infection of the host ant species, indicating a high degree of host specificity for the pathogens.

This particularity might encourage speciation processes and the formation of new species. It was demonstrated that O. unilateralis, which is connected to four distinct formicine ant species in Brazil (Camponotus rufipes, Camponotus. balzani, Camponotus melanoticus, and Camponotus novogranadensis), could be distinguished into various species using micro-morphology criteria, but it did not provide information on levels of genetic variation [17].

Figure 3: A schematic representation of Ophiocordyceps unilateralis’s development in an infected ant host. (December 5, 2022), Access Date: 23.12.2022

This investigation of a population that frequents various ant species in Thailand reveals a pronounced pattern of host-specific molecular variation, pointing to the existence of distinct phylogenetic species  [7]. These results provide credence to the idea that O. unilateralis has evolved in response to its many hosts through host specificity. One of the biggest families of entomopathogenic fungi is Ophiocordyceps. It affects various insect species and includes a set of anamorphs, including Hirsutella, Hymenostilbe, Paraisaria, and Byssostilbe [7].

Ophiocordyceps, which infects ants, includes the independently developed anamorphs of Hirsutella and Hymenostilbe [19]. The insect order appears to be the main explanation for the diversity in both groups.

A new species, Ophiocordyceps halabalaensis, which is only found on the ant Camponotus gigas and is closely related to O. unilateralis, has also been reported [19].

Ophiocordyceps have not yet been shown to exhibit any pattern of intraspecific host-specific molecular differentiation in any investigation. Despite the applicability of such questions for these models [20], focused on the regional molecular diversity in natural populations of Ophiocordyceps sinensis, which has a wide range of insect hosts including more than 50 species from the family Hepialidae. In this investigation, it was shown for the first time that Ophiocordyceps does exhibit host-species-level specialization. Based on this research’s findings and other research, it was hypothesized that Ophiocordyceps attack ants frequently exhibit great host-species specificity.

Ophiocordyceps unilateralis has never been seen to engage in assortative mating. Allochrony appears just somewhat probable, to sum up. This fungus’s life cycle is yet unknown for its ant hosts, on which it alone depends.

Their findings showed that Ophiocordyceps unilateralis and Hirsutella formicarum infections on several ant species occur throughout the year in a time-dependent manner (unpublished data). With all of this in mind, the most likely theory would be premating isolation by host specialization [5,21].

In entomopathogenic fungi, the trend of strong host specificity leading to divergence is uncommon [22,23]. Numerous variables impede the evolution of host specificity in species complexes with extensive host ranges, such as Metarhizium. Specialist strains of M. anisopliae are phylogenetically distinct from generalist strains, differentiating multiple times [24,25].

According to transcriptomic research on this species, specialists have lost the genes needed to survive in different hosts [20,26]. Specialist strains may adapt to beat the immune response of particular insects and kill their hosts progressively to take full advantage of living hosts to make up for the absence of toxins and metabolites which might facilitate the rapid kill-off of the hosts [20,27]. The benefit of dying ant hosts gradually for Ophiocordyceps unilateralis could rely on the potential to influence host behavior for fungus spread. O. unilateralis would use this technique to develop inside the skulls of infected ants and then control them through as-yet unidentified metabolic pathways [20].

Based on this supposition, revealed that Ophiocordyceps unilateralis cells were widely distributed in the infected ants’ heads and that the ants had irregular wandering behavior before dying under a leaf [13,17,28]. As a result, this “slow killer” tactic would encourage specialization and adaptability to various ant species, ultimately promoting the evolution of reproduction and, thus, genetic isolation [28].

This research proves that Ophiocordyceps unilateralis species complexes have evolved through speciation due to their host-specificity for ants. Further investigation into the host-parasite interactions and reproductive isolation processes that led to the observed divergence is encouraged by these findings. In order to fully understand the interaction between the fungus and its host, it is important to understand how the hosts defend themselves from O. unilateralis infection. Answering these concerns and comprehending the proliferation of the zombie-like O. unilateralis species complex and related species requires knowledge of the biogeography, co-evolution, and ecology of the ant hosts [1].

References:

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  13. D. P. Hughes, S. B. Andersen, N. L. Hywel-Jones, W. Himaman, J. Billen, and J. J. Boomsma, “Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection,” BMC Ecol, vol. 11, no. 1, pp. 1–10, May 2011, doi: 10.1186/1472-6785-11-13/FIGURES/5.
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Figure References:

  1. https://www.flickr.com/photos/13084997@N03/60785948
  2. https://en.wikipedia.org/wiki/Ophiocordyceps_unilateralis
  3. https://ekog.org/2022/12/05/zombilestiren-fungus-ophiocordyceps-unilateralis/

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