Howardula aoronymphium

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Howardula aoronymphium
Scientific classification
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H. aoronymphium
Binomial name
Howardula aoronymphium
Welch, 1959
Dissected Drosophila falleni infected with juvenile Howardula aoronymphium nematodes

Howardula aoronymphium is a species of nematode that infects specialist mushroom-feeding fruit flies such as Drosophila falleni and Drosophila neotestacea . Mated female nematodes pierce the fly larva cuticle and take up residence in the hemolymph (insect blood) where they mature alongside the fly. When the adult fly ecloses, the nematode motherworm has reached full size and sheds juvenile nematodes into the hemolymph which are eventually excreted by either the fly anus or ovipositor. Howardula nematodes can severely impact fly egg development, as infection can effectively sterilize some species. [1]

Howardula aoronymphium are attracted to mushroom sites by cuing in on specific odourants that are common in rotting mushrooms. However the odourants that attract H. aoronymphium to mushrooms are different from the odours that attract its fly host D. falleni . Yet when D. falleni are infected by H. aoronymphium, their olfactory preferences differ. Infected flies become more averse to acetate-containing compounds such as ethyl acetate or propyl acetate. Conversely, infected flies become more attracted to 1-nonanol. [2]

Howardula aoronymphium can be compared to other insect-infecting nematodes such as Steinernema and Heterorhabiditis . These nematodes are used as biological control agents, as they efficiently kill their insect prey within days after infection. However unlike these nematodes, Howardula aoronymphium requires its host fly to survive into adulthood, and does not increase larval mortality. [3] Moreover Howardula aoronymphium is quite specific to mushroom-feeding flies, while other insect-infecting nematodes can be more generalist worms capable of infecting a wide variety of insects.

The inherited bacterial symbiont Spiroplasma poulsonii can defend flies against Howardula infection by attacking the nematodes using toxins analogous to sarcin or ricin. [4] [5]

See also

Related Research Articles

<i>Drosophila</i> Genus of flies

Drosophila is a genus of fly, belonging to the family Drosophilidae, whose members are often called "small fruit flies" or pomace flies, vinegar flies, or wine flies, a reference to the characteristic of many species to linger around overripe or rotting fruit. They should not be confused with the Tephritidae, a related family, which are also called fruit flies ; tephritids feed primarily on unripe or ripe fruit, with many species being regarded as destructive agricultural pests, especially the Mediterranean fruit fly.

<span class="mw-page-title-main">Endosymbiont</span> Organism that lives within the body or cells of another organism

An endosymbiont or endobiont is an organism that lives within the body or cells of another organism. Typically the two organisms are in a mutualistic relationship. Examples are nitrogen-fixing bacteria, which live in the root nodules of legumes, single-cell algae inside reef-building corals, and bacterial endosymbionts that provide essential nutrients to insects.

<i>Wolbachia</i> Genus of bacteria in the Alphaproteobacteria class

Wolbachia is a genus of gram-negative bacteria that can either infect many species of arthropod as an intracellular parasite, or act as a mutualistic microbe in filarial nematodes. It is one of the most common parasitic microbes of arthropods, and is possibly the most common reproductive parasite in the biosphere. Its interactions with its hosts are often complex. Some host species cannot reproduce, or even survive, without Wolbachia colonisation. One study concluded that more than 16% of neotropical insect species carry bacteria of this genus, and as many as 25 to 70% of all insect species are estimated to be potential hosts.

<i>Spiroplasma</i> Genus of bacteria

Spiroplasma is a genus of Mollicutes, a group of small bacteria without cell walls. Spiroplasma shares the simple metabolism, parasitic lifestyle, fried-egg colony morphology and small genome of other Mollicutes, but has a distinctive helical morphology, unlike Mycoplasma. It has a spiral shape and moves in a corkscrew motion. Many Spiroplasma are found either in the gut or haemolymph of insects where they can act to manipulate host reproduction, or defend the host as endosymbionts. Spiroplasma are also disease-causing agents in the phloem of plants. Spiroplasmas are fastidious organisms, which require a rich culture medium. Typically they grow well at 30 °C, but not at 37 °C. A few species, notably Spiroplasma mirum, grow well at 37 °C, and cause cataracts and neurological damage in suckling mice. The best studied species of spiroplasmas are Spiroplasma poulsonii, a reproductive manipulator and defensive insect symbiont, Spiroplasma citri, the causative agent of citrus stubborn disease, and Spiroplasma kunkelii, the causative agent of corn stunt disease.

<i>Drosophila falleni</i> Species of fly

Drosophila falleni is a species of fly found in northeastern North America. A mycophagous insect, it is known to feed on the fruit bodies (mushrooms) of several genera of fungi, including Agaricus, Amanita, Agrocybe, Boletus, Cortinarius, PluteusGrifola, Polyporus, Hypholoma, Russula, Mycena, Stropharia, and Xerula. The fly can be infested by the parasitic nematode Howardula aoronymphium, which enters the fly larvae when it is feeding on mushrooms.

Arsenophonus nasoniae is a species of bacterium which was previously isolated from Nasonia vitripennis, a species of parasitoid wasp. These wasps are generalists which afflict the larvae of parasitic carrion flies such as blowflies, houseflies and flesh flies. A. nasoniae belongs to the phylum Pseudomonadota and family Morganellaceae. The genus Arsenophonus, has a close relationship to the Proteus (bacterium) rather than to that of Salmonella and Escherichia. The genus is composed of gammaproteobacterial, secondary-endosymbionts which are gram-negative. Cells are non-flagellated, non-motile, non-spore forming and form long to highly filamentous rods. Cellular division is exhibited through septation. The name 'Arsenophonus nasoniae gen. nov., sp. nov.' was therefore proposed for the discovered bacterium due to its characteristics and its microbial interaction with N. vitripennis. The type strain of A. nasoniae is Strain SKI4.

<i>Steinernema carpocapsae</i> Species of roundworm

Steinernema carpocapsae is an entomopathogenic nematode and a member of the family Steinernematidae. It is a parasitic roundworm that has evolved an insect-killing symbiosis with bacteria, and kills its hosts within a few days of infection. This parasite releases its bacterial symbiont along with a variety of proteins into the host after infection, and together the bacteria and nematode overcome host immunity and kill the host quickly. As a consequence, S. carpocapsae has been widely adapted for use as a biological control agent in agriculture and pest control. S. carpocapsae is considered a generalist parasite and has been effectively used to control a variety of insects including: Webworms, cutworms, armyworms, girdlers, some weevils, and wood-borers. This species is an example of an "ambush" forager, standing on its tail in an upright position near the soil surface and attaching to passing hosts, even capable of jumping. As an ambush forager, S. carpocapsae is thought to be especially effective when applied against highly mobile surface-adapted insects. S. carpocapsae can sense carbon dioxide production, making the spiracles a key portal of entry into its insect hosts. It is most effective at temperatures ranging from 22–28 °C (72–82 °F).

<i>Drosophila neotestacea</i> Species of fly

Drosophila neotestacea is a member of the testacea species group of Drosophila. Testacea species are specialist fruit flies that breed on the fruiting bodies of mushrooms. These flies will choose to breed on psychoactive mushrooms such as the Fly Agaric Amanita muscaria. Drosophila neotestacea can be found in temperate regions of North America, ranging from the north eastern United States to western Canada.

<i>Drosophila testacea</i> Species of fly

Drosophila testacea is a member of the testacea species group of Drosophila. Testacea species are specialist fruit flies that breed on the fruiting bodies of mushrooms. Drosophila testacea can be found in temperate regions of Europe, extending to East Asia. Drosophila testacea and Drosophila orientacea can produce viable hybrids, though they are separated by geography and behavioural barriers. Drosophila testacea females will also readily mate with Drosophila neotestacea males, but viable hybrids are never produced. This hybrid inviability ) may be due to selfish X chromosomes and co-evolved suppressors. Alternately, differences in sex pheromone reception could underlie female readiness and male willingness to copulate.

<i>Drosophila testacea</i> species group Species group of the subgenus Drosophila

The Drosophila testacea species group belongs to the Immigrans-tripunctata radiation of the subgenus Drosophila, and contains 4 species: Drosophila putrida, Drosophila neotestacea, Drosophila testacea, and Drosophila orientacea. Testacea species are specialist mushroom-feeding flies, and can metabolize toxic compounds in Amanita mushrooms. The Testacea species group is studied for its specialist ecology, population genetics, and bacterial endosymbionts. The North American species Drosophila neotestacea is perhaps the best-studied of the group for its interactions with parasitic wasps and nematodes, bacterial endosymbionts, and trypanosomatid parasites. Of note, selfish X chromosomes have been discovered in three of the four Testacea group species.

Spiroplasma poulsonii are bacteria of the genus Spiroplasma that are commonly endosymbionts of flies. These bacteria live in the hemolymph of the flies, where they can act as reproductive manipulators or defensive symbionts.

<i>Howardula</i> Genus of roundworms

Howardula is a genus of nematode that infests the larvae of mushroom-feeding flies, beetles, and other insects. Various Howardula species and strains infest mushroom-feeding Drosophila, including Howardula aoronymphium and Howardula neocosmis. Howardula husseyi can infest the mushroom phorid Megaselia halterata.

<i>Drosophila quinaria</i> species group Species group of the subgenus Drosophila

The Drosophila quinaria species group is a speciose lineage of mushroom-feeding flies studied for their specialist ecology, their parasites, population genetics, and the evolution of immune systems. Quinaria species are part of the Drosophila subgenus.

Mushroom-feeding <i>Drosophila</i> Species group of the subgenus Drosophila

Mushroom-feeding Drosophila are a subset of Drosophila flies that have highly specific mushroom-breeding ecologies. Often these flies can tolerate toxic compounds from Amanita mushrooms.

<i>Drosophila innubila</i> Species of fly

Drosophila innubila is a species of vinegar fly restricted to high-elevation woodlands in the mountains of the southern USA and Mexico, which it likely colonized during the last glacial period. Drosophila innubila is a kind of mushroom-breeding Drosophila, and member of the Drosophila quinaria species group. Drosophila innubila is best known for its association with a strain of male-killing Wolbachia bacteria. These bacteria are parasitic, as they drain resources from the host and cause half the infected female's eggs to abort. However Wolbachia may offer benefits to the fly's fitness in certain circumstances. The D. innubila genome was sequenced in 2019.

Jaenimonas drosophilae is a trypanosomatid parasite of mushroom-feeding flies, first characterized in Drosophila neotestacea and Drosophila falleni. Jaenimonas takes up residence in the gut of the fly, and infection leads to reduced fecundity of its fly host. The species is named for John Jaenike, a prominent ecologist and evolutionary biologist whose work on mushroom-feeding flies laid the foundation for studies on mycophagous Drosophila.

Jaenimonas is a genus of trypanosomatid parasite that infects mushroom-feeding Drosophila, similar to Crithidia parasites of Bumblebees. Jaenimonas drosophilae is the sole representative of this genus. The genus is named in honor of John Jaenike, a prominent ecologist and evolutionary biologist whose work on mushroom-feeding flies laid the foundation for studies on mycophagous Drosophila. Jaenike was also an early proponent of the Red Queen hypothesis.

John Jaenike is an ecologist and evolutionary biologist, and currently a professor at the University of Rochester New York. Jaenike was an early proponent of the Red Queen hypothesis, using the idea to explain the maintenance of sex. Jaenike is also known for his extensive work on mushroom-feeding Drosophila and the evolution of their inherited bacterial symbionts Wolbachia and Spiroplasma poulsonii.

<span class="mw-page-title-main">Allantonematidae</span> Family of roundworms

Allantonematidae is a family of insect-parasitic nematodes from the order Tylenchida. Allantonematid nematodes infect a variety of insects including beetles, butterflies, flies, thrips, ants, and more. For instance, the nematode Howardula aoronymphium parasitizes mushroom-feeding fruit flies, Formicitylenchus oregonensis parasitizes carpenter ants, and Metaparasitylenchus hypothenemi parasitizes a pest of coffee beans, the coffee berry borer.

<span class="mw-page-title-main">Morganellaceae</span> Family of bacteria

The Morganellaceae are a family of Gram-negative bacteria that include some important human pathogens formerly classified as Enterobacteriaceae. This family is a member of the order Enterobacterales in the class Gammaproteobacteria of the phylum Pseudomonadota. Genera in this family include the type genus Morganella, along with Arsenophonus, Cosenzaea, Moellerella, Photorhabdus, Proteus, Providencia and Xenorhabdus.

References

  1. Perlman, Steve J.; Jaenike, John (2003). "Infection Success in Novel Hosts: An Experimental and Phylogenetic Study of Drosophila-Parasitic Nematodes". Evolution. 57 (3): 544–57. doi: 10.1111/j.0014-3820.2003.tb01546.x . PMID   12703944.
  2. Cevallos, James A.; Okubo, Ryo P.; Perlman, Steve J.; Hallem, Elissa A. (2017). "Olfactory Preferences of the Parasitic Nematode Howardula aoronymphium and its Insect Host Drosophila falleni". Journal of Chemical Ecology. 43 (4): 362–373. doi:10.1007/s10886-017-0834-z. PMC   5673469 . PMID   28315996.
  3. Jaenike, John; Anderson, Timothy J. C (September 1992). "Dynamics of Host-Parasite Interactions: The Drosophila-Howardula System" . Oikos. 64 (3). doi:10.2307/3545172 . Retrieved 16 June 2021.
  4. Jaenike, J.; Unckless, R.; Cockburn, S. N.; Boelio, L. M.; Perlman, S. J. (2010). "Adaptation via Symbiosis: Recent Spread of a Drosophila Defensive Symbiont". Science. 329 (5988): 212–215. Bibcode:2010Sci...329..212J. doi:10.1126/science.1188235. PMID   20616278.
  5. Hamilton, Phineas T.; Peng, Fangni; Boulanger, Martin J.; Perlman, Steve J. (2016). "A ribosome-inactivating protein in a Drosophiladefensive symbiont". Proceedings of the National Academy of Sciences. 113 (2): 350–355. Bibcode:2016PNAS..113..350H. doi:10.1073/pnas.1518648113. PMC   4720295 . PMID   26712000.