User:Jojones0805/Massospora

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Massospora is a genus of fungi within the order Entomophthorales of the Zygomycota. It includes more than a dozen obligate, sexually transmissible pathogenic species that infect adult gregarious cicadas (Hemiptera) worldwide. At least two species are known to produce psychoactive compounds during infection. While cicadas exhibit specific mating behaviors and life cycles in nature, infection by Massospora can cause disruption these processes where normal mating processes and reproductive behaviors of the cicada host are thrown into disorder. Infection is achieved through horizontal and vertical transfer of infectious spores between individuals leading into psychological manipulation and further spread of conidia to others within the population. Species of Massospora that exist in nature include Massospora cicadina, M. levispora, M. platypediae, and M. diceroproctae. The entomopathogenic characteristics of these fungi explain why cicadas are the primary sources of fungal infections and may provide useful insight into other areas of research.

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Reproduction of cicadas

A reproductive tactic exhibited by cicadas is called wing-flick signaling. Wing-flick is a sexual signaling mechanism used by adult periodical cicadas and is normally observed only in females responding to male mating calls. A sonogram observed the mating behavior between the sexes of cicadas where males produced a series calls during a copulation attempt resulting in female wing-flick response. Males were shown to produce three separate calls resulting in wing-flick from females after each call. After the final fourth call, the male cicada was able to approach the female leading to a successful mating attempt. The sonogram reveals normal behavior exhibited through healthy cicadas uninfected by a fungal parasite. However, those infected by Massospora exhibit abnormal behavior through wing-flick signaling where both infected females and males respond to calls. The nature of wing-flick signaling between cicadas creates various opportunities for Massospora to spread among the population. Manipulation of the sexual behavior of its host is crucial for the survival of Massospora since wing-flick behavior involves close proximity between individuals increasing the chances of successful fungal transmission.

Massospora cicadina

Upon successful infection by Massospora, the behavior of the host cicada is impacted where infected cicadas remain stationary, make shorter flights, and drag their abdomens while walking leaving behind a trail of infectious spores. The abdomen of the host is destroyed by Massospora with the colonization of visible white fungus. It is relatively common to find a healthy cicada with its genitalia plunged into the infected abdominal spore mass of an infected partner or healthy cicadas attached to fragments of abdomen torn free from infected partners. While there are severe physical damages that occur, cicada hosts continue to live, reproduce, and transmit infectious spores to others through the abnormal behaviors adopted upon infection. These events that occur are a prime example of the parasitic interaction that exist by Massospora cicadina infections and reveal how efficient Massospora are in infecting a host population. Transmission is a crucial step in Massospora survival and manipulation of their host's reproductive behavior further enables the fungus to live, grow, and spread. Resting spores also play a role in infection rates as they lie dormant in the soil until a cicada nymph encounters it. The stages of infection, modes of transmission, and chemical signaling by Massospora cicadina explain the mechanisms of infection through an ecological, evolutionary, and psychological standpoint.

Infection

Massospora cicadina is a common fungal infection amongst the species of the cicada Magicicada spp. Magicicada spp. are a species of periodical cicadas that emerge from the soil every 13 or 17 years depending on the region in which they live. Massospora cicadina is the only known pathogen to Magicicada spp. There are two stages of infection that occur: Stage I and Stage II. During Stage I, male cicadas that are infected with Massospora cicadina produce conidia that are directly spread to other adults during the process of wing-flick signaling. In contrast, males with "Stage II" produce resting spores that will infect the next cicada generation of nymphs that emerge from the soil 13 or 17 years later. Regardless of the infection stage, Massospora hijacks the behavior of cicadas and turns them into fungal transmission vehicles. This phenomenon can be observed through wing-flick signaling where conidia are able to easily travel by wing flick between individuals during the process of mating. Cicadas infected with Massospora cicadina and exhibit abnormal wing-flick behavior create a significantly higher chance of spreading infectious conidia to others.

Stage I

During Stage I infections by Massospora cicadina, fungal conidia are spread throughout the adult population of cicadas. This stage is usually accomplished through wing-flick signaling and as mentioned, wing-flick is usually observed in females responding to a male call. When individuals are infected with Massospora cicadina however, males respond using wing-flick signaling for the further spread of conidia among the population. Males who are infected will exhibit wing-flick behavior as a response to copulation attempts from conspecific males in the chorus resulting in the further spread of infective conidiospores to other healthy males. Stage I infections use direct contact between individuals to achieve successful transmission. Data suggest that cicadas with Stage I infections spend more time leaving behind trails of conidiospores for others to encounter than Stage II infected cicadas.

Stage II

In contrast to Stage I, cicadas with Stage II infections spend more time flying and releasing spores from their damaged abdomens. Males with Stage II infections produce diploid resting spores that will infect the next cicada generation emerging in 13 or 17 years. Resting spores that remain in the soil during Stage II rather than conidia released into the environment during Stage I is the main difference observed between the two stages of infection. Nymphs who emerge every 13 or 17 years depending on the region in which they live will eventually encounter these resting spores leading to further infection of the population as a whole.

Horizontal and Vertical Transfer

The are two modes of transmission that exist in nature: horizontal transfer and vertical transfer. Horizontal transfer can be seen during the transmission of Massospora cicadina through the reproduction process of two adult cicadas. The fungus Massospora produces two main types of spores, conidia that are released into the environment for adult cicadas to encounter and resting spores that remain dormant in the soil for emerging nymphs to encounter. Since horizontal transfer relies on direct contact between fungi and host, horizontal transmission is said to be more risky than vertical transmission. However, wing flick and the manipulation of a host's mating process ensures successful transmission with both correct timing and close contact between individuals. The resting spores left behind by adult cicadas that burrow into the soil during verticle transmission can germinate for variable lengths of time before eventually leading to infection. This means that the spores produced by Massospora must become active at the correct period of time in order to successfully infect their host cicada. However, spore availability regardless of synchronization with emerging cicadas has been found to play a factor in successful infection. In one study, Massospora cicadina spores appeared to be capable of germinating after less than a year. These results suggest that Massospora cicadina resting spores do not require a 13 or 17 year dormant period along with their emerging host cicada during vertical transmission in order for infection to occur and can freely infect hosts they come into close contact with during mating. During horizontal gene transfer of Massospora to it's periodical cicada host, it ultimately involves close contact between the two. Timing does play a role during vertical transmission, however the fungi seems to have evolved into being time-independent during the infection process. These modes of transmission are important in understanding the processes by which infection occurs and the behavioral manipulations that result from it.

Chemical Signaling

When discussing the chemical pathways that occur during a fungal infection, there are two modes of action that occur: direct action and indirect action. Direct action of chemical signaling describes secreted factors (effectors) that could act directly on neurons to change behavioral output. Indirect action involves a change in the internal state or integrity of tissue. For behavior-manipulating fungi, both direct and indirect chemical signaling are possible mechanisms. One study found metabolite effectors such as the alkaloids psilocybin (the active ingredient in magic mushrooms) and amphetamine cathinone in M. platypediae , and M.cicadina. Alkaloids such as psilocybin and cathinone are well-known for having behavioral effects and are a example of direct action of chemical signaling that cause behavioral changes observed in infected cicadas. Indirect action can be seen through the dispersal of conidia to others after production of these alkaloids resulting in a behavioral change. Behavior-altering chemicals such as these are important to understanding how fungi manipulate the psychology of their host to benefit themselves.

Other cicada species infected by Massospora and evolutionary relationships

The fungal pathogen Massospora levispora was discovered in populations of another cicada species named Okanagana rimosa and prompted an epizootilogical investigation of the host-pathogen system. A 1960s investigation observed the prevalence of conidia in female and male cicadas. Certain features of the fugus life cycle allowed direct measurment of both initial infection prevalence and the rate of spread within the population. The study aimed to relate infection to host  density, inoculum density, moisture conditions, and temperature. Large cicada populations occured in1967 and 1969 as expected with periodical cicadas who emerge every 13 or 17 years. The study showed that the proportion of males remained constant while a slight increase was noticed in females in 1967 but was constant in 1969. Evolutionary relationships among Massospora spp. have also been investigated. The evolutionary relationships and host associations of Massospora spp. are not well understood. However, a study conducted in 2020 provided phylogenetic analyses and morphological studies to investigate whether the taxonomy among the differing species of ''Massospora. M. diceroproctae from Arizona, M.tettigatis from Chile, and M. platypediae'' from California and Colarado were acquired to investigate whether these fungi represent a monophyletic group. Through phylogenetic analyses, Massospora was found to represent a strongly supported monophyletic group with four well-supported genealogically exclusive lineages. Massospora levispora and M.platypediae formed a single lineage in these analyses while M. diceroproctae was sister to M. cicadina. Another extremely long branch relative to other species of Massospora and outgroup taxa was also observed and may reflect incomplete taxon sampling. Based on the results of this study, research involving the ecology and evolution of Massospora is needed in an effort to better understand the relationships between cicada hosts and fungal entomopathogens.

Fungal Entomopathogens and Pest Control

Massospora is entomopathogenic (entomo- meaning "insect"). When defining entomopathogenic fungi, they are soil-dwelling microorganisms that form spores/conidia which adhere to and germinate the surface of an insect’s exoskeleton leading to penetration of the cuticle. Once the fungus has passed through the cuticle of insect dermis, invasion of the insect body and circulatory system occurs where the fungi aim to infect, kill, or greatly impact the mobility of their host. The first entomopathogenic fungus discovered was in 1835 by Agostino Bassi and was later named Beauveria bassiana. Beauveria bassiana has been known to infect silkworms causing white muscadine, a disease that proliferates throughout the body of an insect host. Massospora cicadina and Beauveria bassiana infections are comparable through white fungal infections that colonize the host body causing decreased mobility, physical changes, and even death. Beauveria bassiana infections had a negative affect in the silk-worm industry during the 18th and 19th centuries as it infected and killed large populations of silkworm larvae. The mechanism through which fungal entomopathogens such as Massospora and Beauveria bassiana negatively affect their host is indeed a problem for insect populations. However, although fungal entomopathogens have a direct impact on their host through infection they may also indirectly benefit other species endangered by those insects. Currently, species of entomopathogens are being used as biocontrol agents against insect plant pests and play a vital role in pest management. A problem that arises in pest management is that although fungi exist as natural parasites within a population they are not synchronized with infection of the pest in time to limit crop damage. However, the process of "inundative augmentation" is used to combat asynchronization where the parasitic fungi is applied in large amounts to a crop for rapid short-term control of pests without the expectation of a secondary infection. Beauveria bassiana for example, has been developed as a commercial insecticide primarily sold in North America since the late 1980s. Mass-production of the fungal conidia of B.bassiana was later termed "Mycotrol" and was fully registered in 1999 by the Environmental Protection Agency of the USA. This allowed for the use of the fungi on a large variety of field crops for the control of insect pests such as grasshoppers, whiteflies, aphids etc. In the case of B.bassiana, field-crop pests can be controlled using their own natural enemies of fungi rather than chemical insecticides for a more eco-friendly approach to pest control.