Drosophila neotestacea

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Drosophila neotestacea
Dneo f2.tif
A Drosophila neotestacea female on the gills of an Agaricus mushroom
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Diptera
Family: Drosophilidae
Subfamily: Drosophilinae
Genus: Drosophila
Subgenus: Drosophila
Species group: testacea
Species:
D. neotestacea
Binomial name
Drosophila neotestacea
Grimaldi, James, and Jaenike, 1992 [1]

Drosophila neotestacea is a member of the testacea species group of Drosophila . [2] 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 . [3] Drosophila neotestacea can be found in temperate regions of North America, ranging from the north eastern United States to western Canada. [4]

Contents

Immunity

A dissected Drosophila infected with Howardula aoronymphium nematodes

Drosophila neotestacea and other mushroom-breeding Drosophila have been studied extensively for their interactions with Howardula nematode parasites, particularly Howardula aoronymphium . Unlike related species, D. neotestacea is sterilized by H. aoronymphium infection. The genetic basis of this susceptibility is unknown, and is nematode-dependent. For instance, a related Howardula species from Japan does not sterilize D. neotestacea, even though the European and North American Howardula species do. Moreover, the related Drosophila orientacea is resistant to infection by the European Howardula nematodes, but susceptible to the Japanese Howardula nematodes. [5] Accordingly, nematode infection strongly suppresses genes involved in egg development. [6] Comparisons between D. neotestacea and nematode-resistant members of the Testacea species group can help tease apart interactions of fly immunity genetics and nematode parasitism genetics.

Initially discovered in D. neotestacea, mushroom-feeding flies are commonly infected with the trypanosomatid parasite Jaenimonas drosophilae . [7]

The major innate immunity pathways of Drosophila are found in D. neotestacea, however the antimicrobial peptide Diptericin B has been lost. [8] This loss of Diptericin B is also common to the related Drosophila testacea and Drosophila guttifera, but not the also-related Drosophila innubila. As such, these loss events appear to have been independent, suggesting that Diptericin B is actively selected against in these species; indeed, Diptericin B is conserved in all other Drosophila species. [9] It also seems that unrelated Tephritid fruit flies have independently derived a Diptericin gene strikingly similar to the DrosophilaDiptericin B gene. Like mushroom-feeding flies, these Tephritids also have a non-frugivorous sub-lineage that has similarly lost the Tephritid Diptericin B gene. These evolutionary patterns in mushroom-breeding Drosophila and other fruit flies suggests that the immune system's effectors (like antimicrobial peptides) are directly shaped by host ecology. [9]

Symbiosis

Mushroom sites are infested with nematodes and other natural enemies Dneo f3.tif
Mushroom sites are infested with nematodes and other natural enemies

Drosophila neotestacea can harbour bacterial symbionts including Wolbachia and notably Spiroplasma poulsonii . The S. poulsonii strain of D. neotestacea has spread westward across North America due to the selective pressure imposed by the sterilizing nematode parasite Howardula aoronymphium . [4] While S. poulsonii can be found in other Drosophila species, the D. neotestacea strain is unique in defending its host against nematode infestation. Like other S. poulsonii strains, the D. neotestacea strain also protects its host from parasitic wasp infestation. [10]

The mechanism through which S. poulsonii protects flies from nematodes and parasitic wasps relies on the presence of toxins called ribosome-inactivating proteins (RIPs), similar to Sarcin or Ricin. [11] [12] These toxins cut a conserved structure in ribosomal RNA, ultimately changing the nucleotide sequence at a specific site. This leaves a signature of RIP attack in nematode and wasp RNA. Spiroplasma poulsonii likely avoids damaging its host fly by carrying parasite-specific complements of RIP toxins encoded on bacterial plasmids. This allows genes for RIP toxins to readily move between species by horizontal gene transfer, as D. neotestaceaSpiroplasma RIPs are shared by Spiroplasma of other mushroom-feeding flies, such as Megaselia nigra . [13]

Selfish genetic elements

The Testacea species group is used in population genetics to study sex-ratio distorting 'selfish' or 'driving' X chromosomes. Selfish X chromosomes bias the offspring of males such that fathers only produce daughters. This increases the spread of the selfish X chromosome, as Y chromosome-bearing sperm are never transmitted. In wild populations, up to 30% of D. neotestacea individuals can harbour a selfish X chromosome. The spread of the D. neotestacea selfish X is limited by climatic factors, predicted by the harshness of winter. Thus, its frequency in the wild may be affected by ongoing climate change. [14] The mechanism of X chromosome drive may be related to a duplication of an importin gene, a type of nuclear transport protein. [15]

Often, selfish X chromosomes suppress genetic recombination during meiosis. This process maintains the gene clusters that promote X chromosome drive, but also can lead to an accumulation of deleterious mutations via a process known as Muller's ratchet. The D. neotestacea selfish X suppresses recombination in lab settings, but occasional recombination occurs in the wild evidenced by recombinant genetic regions in wild-caught flies. [16] Other Testacea species harbour selfish X chromosomes, raising the question of whether X chromosome drive played a role in speciation of the Testacea group. [17] At least one selfish X in Testacea group flies is old enough to have been present in the last-common ancestor of Drosophila testacea and Drosophila orientacea . [18]

See also

Related Research Articles

<i>Drosophila</i> Genus of flies

Drosophila is a genus of flies, 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.

<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.

Meiotic drive is a type of intragenomic conflict, whereby one or more loci within a genome will affect a manipulation of the meiotic process in such a way as to favor the transmission of one or more alleles over another, regardless of its phenotypic expression. More simply, meiotic drive is when one copy of a gene is passed on to offspring more than the expected 50% of the time. According to Buckler et al., "Meiotic drive is the subversion of meiosis so that particular genes are preferentially transmitted to the progeny. Meiotic drive generally causes the preferential segregation of small regions of the genome".

Immigrans-tripunctata radiation Species group of the subgenus Drosophila

The immigrans-tripunctata radiation is a speciose lineage of Drosophila flies, including over 300 species. The immigrans-tripunctata radiation is a sister lineage to most other members of the subgenus Drosophila. A number of species have had their genomes or transcriptomes sequenced for evolutionary studies using Drosophila.

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

.

Providencia rettgeri, is a Gram negative bacterium that is commonly found in both water and land environments. P. rettgeri is in the genus Providencia, along with Providencia stuartii, Providencia alcalifaciens, and Providencia rustigianii. P. rettgeri can be incubated at 37 °C in nutrient agar or nutrient broth. It was first discovered in 1904 after a waterfowl epidemic. Strains of the species have also been isolated from nematodes of the genus Heterorhabditis. Providencia rettgeri also found in marine environment.

<i>Howardula aoronymphium</i> Species of roundworm

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 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.

<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.

Drosophila orientacea 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 orientacea is found in northern Japan on the island of Hokkaido. However, the European species Drosophila testacea and D. orientacea can produce viable hybrids, blurring the level of speciation between the two species. While viable hybrids are produced, extreme behavioural barriers likely prevent mating in the wild. While D. orientacea readily mates with Drosophila neotestacea, viable hybrids are never produced. This hybrid inviability may be due either to issues during copulation, or selfish X chromosomes and co-evolved suppressors.

<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.

<span class="mw-page-title-main">Diptericin</span>

Diptericin is a 9 kDa antimicrobial peptide (AMP) of flies first isolated from the blowfly Phormia terranova. It is primarily active against Gram-negative bacteria, disrupting bacterial membrane integrity. The structure of this protein includes a proline-rich domain with similarities to the AMPs drosocin, pyrrhocoricin, and abaecin, and a glycine-rich domain with similarity to attacin. Diptericin is an iconic readout of immune system activity in flies, used ubiquitously in studies of Drosophila immunity. Diptericin is named after the insect order Diptera.

<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">Drosophila immigrans species group</span> Species group of the subgenus Drosophila

The Drosophila immigrans species group is a polyphyletic and speciose lineage of Drosophila flies, including over 100 species. Immigrans species belong to the Immigrans-tripunctata radiation of the subgenus Drosophila. Well-described species include Drosophila immigrans, and the sister species Drosophila albomicans and Drosophila nasuta. The genome of D. albomicans was sequenced in 2012 in an effort to characterize novel sex chromosome development in D. albomicans. Immigrans group species are related to mushroom-breeding Drosophila of the Quinaria and Testacea species groups.

References

  1. ↑ Grimaldi, David; James, Avis C.; Jaenike, John (1992). "Systematics and Modes of Reproductive Isolation in the Holarctic Drosophila testacea Species Group (Diptera: Drosophilidae)". Annals of the Entomological Society of America. 85 (6): 671–685. doi:10.1093/aesa/85.6.671.
  2. ↑ Jaenike, John; Stahlhut, Julie K.; Boelio, Lisa M.; Unckless, Robert L. (2010). "Association between Wolbachia and Spiroplasma within Drosophila neotestacea: an emerging symbiotic mutualism?". Molecular Ecology. US. 19 (2): 414–425. doi: 10.1111/j.1365-294X.2009.04448.x . PMID   20002580.
  3. ↑ Jaenike, John (1978). "Host Selection by Mycophagous Drosophila". Ecology. 59 (6): 1286–1288. doi:10.2307/1938245. JSTOR   1938245.
  4. 1 2 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. S2CID   206526012.
  5. ↑ Perlman, Steve J.; Jaenike, John (2003). "Infection Success in Novel Hosts: An Experimental and Phylogenetic Study of Drosophila-Parasitic Nematodes". Evolution. 57 (3): 544–557. doi: 10.1111/j.0014-3820.2003.tb01546.x . PMID   12703944. S2CID   20459223.
  6. ↑ Hamilton, Phineas T.; Leong, Jong S.; Koop, Ben F.; Perlman, Steve J. (2014). "Transcriptional responses in a Drosophiladefensive symbiosis". Molecular Ecology. 23 (6): 1558–1570. doi:10.1111/mec.12603. hdl: 1828/8389 . PMID   24274471.
  7. ↑ Hamilton, Phineas T.; Votýpka, Jan; Dostálová, Anna; Yurchenko, Vyacheslav; Bird, Nathan H.; Lukeš, Julius; Lemaitre, Bruno; Perlman, Steve J. (2015). "Infection Dynamics and Immune Response in a Newly Described Drosophila-Trypanosomatid Association". mBio. 6 (5): e01356-15. doi:10.1128/mBio.01356-15. PMC   4600116 . PMID   26374124.
  8. ↑ Hanson MA, Hamilton PT, Perlman SJ (October 2016). "Immune genes and divergent antimicrobial peptides in flies of the subgenus Drosophila". BMC Evolutionary Biology. 16 (1): 228. doi: 10.1186/s12862-016-0805-y . PMC   5078906 . PMID   27776480.
  9. 1 2 Hanson, Mark Austin; Lemaitre, Bruno; Unckless, Robert L. (2019). "Dynamic evolution of antimicrobial peptides underscores trade-offs between immunity and ecological fitness". Frontiers in Immunology. 10: 2620. doi: 10.3389/fimmu.2019.02620 . ISSN   1664-3224. PMC   6857651 . PMID   31781114.
  10. ↑ Haselkorn, Tamara S.; Jaenike, John (2015). "Macroevolutionary persistence of heritable endosymbionts: Acquisition, retention and expression of adaptive phenotypes in Spiroplasma". Molecular Ecology. 24 (14): 3752–3765. doi:10.1111/mec.13261. PMID   26053523.
  11. ↑ 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.
  12. ↑ Ballinger, Matthew J.; Perlman, Steve J. (2017). "Generality of toxins in defensive symbiosis: Ribosome-inactivating proteins and defense against parasitic wasps in Drosophila". PLOS Pathogens. 13 (7): e1006431. doi: 10.1371/journal.ppat.1006431 . PMC   5500355 . PMID   28683136.
  13. ↑ Ballinger, Matthew J.; Gawryluk, Ryan M. R.; Perlman, Steve J. (2019). "Toxin and Genome Evolution in a Drosophila Defensive Symbiosis". Genome Biology and Evolution. 11 (1): 253–262. doi: 10.1093/gbe/evy272 . PMC   6349354 . PMID   30576446.
  14. ↑ Dyer, Kelly A. (2012). "Local Selection Underlies the Geographic Distribution of Sex-Ratio Drive in Drosophila Neotestacea". Evolution. 66 (4): 973–984. doi: 10.1111/j.1558-5646.2011.01497.x . PMID   22486683. S2CID   17513583.
  15. ↑ Pieper, Kathleen E.; Unckless, Robert L.; Dyer, Kelly A. (2018). "A fast‐evolving X‐linked duplicate of importin‐α2 is overexpressed in sex‐ratio drive in Drosophila neotestacea". Molecular Ecology. 27 (24): 5165–5179. doi:10.1111/mec.14928. PMC   6312747 . PMID   30411843.
  16. ↑ Pieper, K. E.; Dyer, K. A. (2016). "Occasional recombination of a selfish X-chromosome may permit its persistence at high frequencies in the wild". Journal of Evolutionary Biology. 29 (11): 2229–2241. doi:10.1111/jeb.12948. PMC   5089913 . PMID   27423061.
  17. ↑ Keais, G. L.; Hanson, M. A.; Gowen, B. E.; Perlman, S. J. (2017). "X chromosome drive in a widespread Palearctic woodland fly, Drosophila testacea". Journal of Evolutionary Biology. 30 (6): 1185–1194. doi: 10.1111/jeb.13089 . PMID   28402000.
  18. ↑ Keais, G. L. (2018). X chromosome drive in Drosophila testacea (Thesis).
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