Why are there so few examples of entomopathogenic fungi that manipulate host sexual behaviors?

Hansen, Andreas N.; Licht, Henrik H. De Fine

doi:10.1016/j.funeco.2018.09.004

Cited by 12 publications

(7 citation statements)

References 51 publications

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“…It was recently revealed that M. cicadina releases psychoactive chemicals during infection, which are speculated to contribute to keeping the insect alive despite missing half of the body by increasing insect sexual behaviors and reducing insect feeding behaviors (Boyce et al 2019 ). That the highly host-specific entomophthoralean fungi may manipulate insect sexual behaviors would seem to be an ideal way of ensuring conspecific contact between susceptible hosts, but does not imply that these fungi can be considered as sexually transmitted diseases (Hansen and De Fine Licht 2019 ). In general, active host transmission is well known from a number of fungal pathogens (Lovett et al 2020a ), but is not the norm and can to some extent be considered as the pinnacle of host-specific adaptation because of the intricate fungal machinery likely required to keep the host alive during fungal sporulation.…”

Section: Infection and The Fungal Life-cycle Within The Hostmentioning

confidence: 99%

The genus Entomophthora: bringing the insect destroyers into the twenty-first century

Elya

Licht

2021

IMA Fungus

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The fungal genus Entomophthora consists of highly host-specific pathogens that cause deadly epizootics in their various insect hosts. The most well-known among these is the “zombie fly” fungus E. muscae, which, like other Entomophthora species, elicits a series of dramatic behaviors in infected hosts to promote optimal spore dispersal. Despite having been first described more than 160 years ago, there are still many open questions about Entomophthora biology, including the molecular underpinnings of host behavior manipulation and host specificity. This review provides a comprehensive overview of our current understanding of the biology of Entomophthora fungi and enumerates the most pressing outstanding questions that should be addressed in the field. We briefly review the discovery of Entomophthora and provide a summary of the 21 recognized Entomophthora species, including their type hosts, methods of transmission (ejection of spores after or before host death), and for which molecular data are available. Further, we argue that this genus is globally distributed, based on a compilation of Entomophthora records in the literature and in online naturalist databases, and likely to contain additional species. Evidence for strain-level specificity of hosts is summarized and directly compared to phylogenies of Entomophthora and the class Insecta. A detailed description of Entomophthora’s life-cycle and observed manipulated behaviors is provided and used to summarize a consensus for ideal growth conditions. We discuss evidence for Entomophthora’s adaptation to growth exclusively inside insects, such as producing wall-less hyphal bodies and a unique set of subtilisin-like proteases to penetrate the insect cuticle. However, we are only starting to understand the functions of unusual molecular and genomic characteristics, such as having large > 1 Gb genomes full of repetitive elements and potential functional diploidy. We argue that the high host-specificity and obligate life-style of most Entomophthora species provides ample scope for having been shaped by close coevolution with insects despite the current general lack of such evidence. Finally, we propose six major directions for future Entomophthora research and in doing so hope to provide a foundation for future studies of these fungi and their interaction with insects.

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Section: Infection and The Fungal Life-cycle Within The Hostmentioning

confidence: 99%

The genus Entomophthora: bringing the insect destroyers into the twenty-first century

Elya

Licht

2021

IMA Fungus

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“…The willingness to mate is for example exploited by certain insect pollinated flowers (Schiestl et al, 2000;Cohen et al, 2021;Hayashi et al, 2021), which use sexual mimicry to attract pollinators by resembling the opposite sex visually and/or chemically. Exploitation of mate recognition systems can be highly advantageous for obligate pathogens as it increases the chance of pathogen transmission by ensuring contact with new potential hosts of the right species (Hansen and De Fine Licht, 2019).…”

Section: Mainmentioning

confidence: 99%

Pathogenic fungus uses volatiles to entice male flies into fatal matings with infected female cadavers

et al. 2022

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To ensure dispersal, many parasites and pathogens behaviourally manipulate infected hosts. Other pathogens and certain insect-pollinated flowers use sexual mimicry and release deceptive mating signals. However, it is unusual for pathogens to rely on both behavioural host manipulation and sexual mimicry. Here, we show that the host-specific and behaviourally manipulating pathogenic fungus, Entomophthora muscae, generates a chemical blend of volatile sesquiterpenes and alters the level of natural host cuticular hydrocarbons in dead infected female house fly (Musca domestica) cadavers. Healthy male house flies respond to the fungal compounds and are enticed into mating with dead female cadavers. This is advantageous for the fungus as close proximity between host individuals leads to an increased probability of infection. The fungus-emitted volatiles thus represent the evolution of an extended phenotypic trait that exploit male flies' willingness to mate and benefit the fungus by altering the behavioural phenotype of uninfected healthy male host flies..

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“…The mechanism by which Massospora induces female-associated behaviors in infected male cicadas is unknown [22]. Males with conidia-producing infections (which are spread by close contact among abundant individuals) exhibit sexual behaviors directed at both sexes by additionally wing flicking in response to calls by other males.…”

Section: How Is Sexual Behavior Related To Aht?mentioning

confidence: 99%

Behavioral betrayal: How select fungal parasites enlist living insects to do their bidding

et al. 2020

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The retention of the power of locomotion is of great importance in so far as the spread of the disease is concerned. It enables the insects not only before the abdomen has ruptured, but even after the fruiting layer has been exposed and, during the time the conidia are being discharged, to wander over the trees and distribute the spores in a far more efficient manner than would be possible if death of the host resulted before the fruiting stage of the fungus was reached-as is usually the case."-Dr. Alan G. Dustan observing active host transmission by Entomophthora erupta-infected Lygus communis, 1923 [1].

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Why are there so few examples of entomopathogenic fungi that manipulate host sexual behaviors?

Cited by 12 publications

References 51 publications

The genus Entomophthora: bringing the insect destroyers into the twenty-first century

The genus Entomophthora: bringing the insect destroyers into the twenty-first century

Pathogenic fungus uses volatiles to entice male flies into fatal matings with infected female cadavers

Behavioral betrayal: How select fungal parasites enlist living insects to do their bidding

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