Cotesia congregata

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Cotesia congregata
Cotesia9061.8.15.07.c.jpg
C. congregata on hornworm Manduca sexta
Male C. congregata courtship song
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Hymenoptera
Family: Braconidae
Genus: Cotesia
Species:
C. congregata
Binomial name
Cotesia congregata
(Say, 1836)
Synonyms
  • Microgaster congregata Say, 1836 [1]
  • Apanteles congregata(Say, 1838)
  • Apanteles congregatus
  • Microgaster utilisFrench, 1880
  • Cotesia utilis(French, 1880)
  • Apanteles (Protapanteles) augustusViereck, 1917
  • Cotesia augusta(Viereck, 1917)
Cocoons of Cotesia congregata on Manduca sexta Cotesia congregata on Manduca sexta.jpg
Cocoons of Cotesia congregata on Manduca sexta

Cotesia congregata is a parasitoid wasp of the genus Cotesia . The genus is particularly noted for its use of polydnaviruses. Parasitoids are distinct from true parasites in that a parasitoid will ultimately kill its host or otherwise sterilize it.

Contents

Life cycle

Adult wasps lay their eggs in tobacco hornworm (Manduca sexta) and tomato hornworm (Manduca quinquemaculata) larvae in their 2nd or 3rd instar (each instar is a stage between moltings, i.e. the second instar is the life stage after the first molt and before the second molting) and at the same time injects symbiotic viruses into the hemocoel of the host along with some venom. The viruses knock down the internal defensive responses of the hornworm. The eggs hatch in the host hemocoel within two to three days and simultaneously release special cells from the egg's serosa. These special cells, called teratocytes, grow to become giant cells visible to the naked eye. The teratocytes secrete hormones which work in tandem with the virus and the wasp venom to arrest the development of the host. [2] Following hatching in the caterpillar, the wasp larvae will undergo 2 molts inside the host caterpillar’s hemocoel and, after 12 to 16 days post oviposition, the 3rd instar wasp larvae will emerge from the caterpillar and spin cocoons from which the adult wasps fly about 4 to 8 days later. [3]

Not all of the parasite larvae will successfully emerge from the host. Dissection of post-emergence caterpillars revealed three categories of remaining larvae: [4]

  1. Dead or dying wasp larvae, in various stages of development, which had been partially or completely encapsulated by the host's immune system. The parasite has significant immunosuppressive capabilities, but the host's immune system is able to partially recover over a period of several days, so these may have been encapsulated at a very late stage.
  3. Wasp larvae that were alive, but had exhibited reduced growth compared to the other larvae and might not have been able to reach the second instar stage.
  5. Wasp larvae in the second instar, similar to those which had emerged successfully.

This insect has the shortest flagellated spermatozoa in animals, being 6.6 µm long (nucleus and flagellum), 8800 times shorter than the longest ones (Drosophila bifurca). [5]

Cotesia pupae may themselves be hyperparasitized by wasps of the genus Hypopteromalus . [6]

Polydnavirus symbiosis

An important aspect of the symbiotic polydnavirus is the fact that the virus does not and cannot replicate on its own- it does not contain the genes necessary to replicate itself. Instead, the genes that code for the virus are contained within the genome of the wasp. The wasp contains special cells called calyx cells within its ovary, which in females will produce the virion particles. Male wasps contain the viral sequence, but do not have the capacity to produce it. The proteins and genetic payload of the virus are produced by these cells, and the virions are assembled within the nucleus of these cells. As the female matures, the nuclear membrane will dissolve, followed by the cell membrane, releasing the virions and cell debris into the lumen of the oviduct. Phagocytic cells will clean up the debris, and the virions will be injected into the host along with eggs and venom upon oviposition. [7] [8]

An average female wasp will produce over 600 ng of viral DNA in each ovary, more than enough for her lifetime. An average female will lay 1757 +/- 945 eggs in her lifetime, and only 0.1 ng of viral DNA is injected per egg. [7] [8]

Effects of the virus on the host

The polydnavirus will severely interfere with development of the host, Manduca sexta. Infected hosts will not undergo metamorphosis, and hosts with a particularly large number of parasites can reach higher weight in the first few instars than uninfected hosts. [9] However, most hosts weigh less than unparasitized caterpillars [9] and after they reach the fifth instar their feeding rate will reduce, causing their weight to decline significantly. [10] The infected host will sometimes reach a supernumerary sixth instar [10] if a high number of parasite larvae are present inside it. [4] [11] This is because there will be more competition for resources among the larger parasite population, causing them to develop more slowly. [4] By contrast, the parasites may emerge in the fourth or even third instar if there are less of them than average. With less competition for resources, they will develop more quickly and be ready to emerge sooner.

In some cases, none of the parasites will emerge from a sixth-instar host. All of them will either die or fail to emerge. [4] The hosts in this case would have been large enough to pupate at the end of the fifth instar. However, parasitized caterpillars have far higher levels of juvenile hormone (JH) than unparasitized caterpillars, and this prevents metamorphosis, causing the caterpillar to enter the supernumerary sixth instar instead. Some of these caterpillars will later reach a seventh instar stage, but they will still be unable to pupate and will die in this state.

Sixth-instar caterpillars below the threshold size for pupation at the end of the fifth instar are killed through parasite emergence.

Upon reaching the fifth instar, the caterpillar will enter a wandering stage, as is typical, but will not progress further and will not form a cocoon. The onset of the wandering stage is temporally delayed as well. [12]

Approximately 8 hours before the wasp larvae emerge, the parasitized caterpillar's food consumption significantly declines. [9] [10] [13] This change in behaviour may be a means to prevent the caterpillar from eating the wasp cocoons. [9] At the same time as the caterpillar's food consumption declines, its locomotion also decreases significantly (that is, it moves around less). [9] [14] Without human intervention, the reduced appetite and locomotion are both permanent - the caterpillar will never return to its normal behaviour, even after the parasites have emerged. [9]

Certain neuropeptides were found to accumulate in the neurosecretory system of the host, which were correlated to a change in molting behavior. Similar accumulation has been found in neural system of starving, unparasitized caterpillars, but not nearly to the same extent. The polydnavirus was found to inhibit development of the optic lobe of the host, causing morphological differences. One known hormone which has been focused upon, prothoracicotropic hormone (PTTH), was of particular interest. It is accumulated far more heavily in parasitized and starved hosts than in normal larvae. Other proteins found to increase in neurosecretory cells in both starved and parasitized larvae are: bombyxin, allatostatin, allatotropin, diuretic hormone, FMRFamide, and proctolin. Other proteins were found in increased concentration in hosts from which the wasps had already emerged, such as eclosion hormone and adipokinetic hormone. [10]

The polydnavirus disallows these proteins from being released into the nervous system, instead causing them to accumulate in neurosecretory cells. Specifically with PTTH, due to the accumulation, is not released in sufficient amounts to stimulate the synthesis of ecdysteroids by the prothoracic glands, which will prevent subsequent development of the larvae. These hormones also allow the parasitized larva to survive longer without food or water, due to a slowdown of diuresis (urine production) and gut purge. This would help the larva to conserve water. Starved larvae can also ultimately molt and pupate if they are large enough, but this can be explained by the temporal difference in the beginning of accumulation. The mechanism behind neuropeptide accumulation is unknown. The polydnavirus is not the only factor affecting development of the host; teratocytes will have a similar effect, and it is likely that a large combination of different factors is needed to replicate the biological effects of parasitization. [10]

Another extremely important effect of the virus is the suppression of the immune system of the host. This is accomplished by altering the behavior of host hemocytes, including inducing apoptosis. Within 24 hours of oviposition, the host is unable to encapsulate any antigen which enters its body, preventing it from attacking the wasp larvae.

Over a period of several days, the immune system will make a partial recovery. In experiments, its ability to encapsulate a harmless artificial stimuli had returned to near-normal after 8 days. [12] After 10 days hemocyte functioning against injected E. coli bacteria had fully recovered. [15] However, aspects of the immune system not involved in the initial response do not recover to the same extent. Parasitized caterpillars 10 days after oviposition were observed to suffer far higher mortality from the Pseudomonas aeruginosa bacterium than nonparasitized caterpillars, and had only very slight improvements in their immune response compared to caterpillars 1 hour post-oviposition.

Despite the immune system's partial recovery, by the 8-day point the wasp larvae have developed a resistance to the immune system by some other means. [12] From an evolutionary standpoint, it is beneficial for the wasp larva that the host should recover its resistance to external pathogens without regaining the ability to destroy the parasite.

Larvae which have reached 8 days old can survive and eclose when transplanted into a new host which has not been exposed to the virus, although their chances of survival are significantly reduced. In experiments, 50% of the host larvae successfully encapsulated all of the parasitoids, and the mortality rate of wasp larvae in the remaining hosts varied significantly. [12]

The wasp also injects venom along with the eggs and virus particles. The venom on its own will have a negligible effect on the host, but will enhance the effects of the virus when both are present. [2]

Changed effects resulting from surgical alteration to the parasitized host

Researchers were able to counter the decline in locomotion by surgically removing the host's supraesophageal ganglion (brain) during day 4 of the fifth instar, prior to parasite emergence. After the parasites emerged, the surgically-altered host moved about almost continuously, very similar to its "wandering" phase. [14] [9] However, this was not a restoration of the wandering phase, since during a genuine wandering phase the brain is necessary for locomotor activity. [14] This surgery rendered the caterpillar unable to feed, so it is not known whether its drive to do so was also restored. [9]

Genetic description of the virus

The Cotesia congregata bracovirus has one of the largest genomes known of any virus (567,670 base pairs), and is largely composed of introns, which is rare for a virus; 70% of the DNA is noncoding. The genome is arranged in 30 circles of DNA, which range in size from 5,000 to 40,000 base pairs. Of the 30, 29 circles code for at least one protein product. The genome is composed of 66% A-T residues. [16] The top gene products are:

The rest of the protein products have no known homologs and their function is not known. Much of what has been discovered makes it difficult to place the virus in a phylogenetic niche, and lends support to the theory that the virus was assembled, rather than evolved. The most closely related viruses are the nudiviruses and their baculovirus relatives, although this relatedness goes back approximately 75 million years. [16]

Related Research Articles

Juvenile hormones (JHs) are a group of acyclic sesquiterpenoids that regulate many aspects of insect physiology. The first discovery of a JH was by Vincent Wigglesworth. JHs regulate development, reproduction, diapause, and polyphenisms. The chemical formula for juvenile hormone is .

<i>Manduca sexta</i> Species of moth

Manduca sexta is a moth of the family Sphingidae present through much of the Americas. The species was first described by Carl Linnaeus in his 1763 Centuria Insectorum.

<span class="mw-page-title-main">Hyperparasite</span> Parasite of another parasite

A hyperparasite, also known as a metaparasite, is a parasite whose host, often an insect, is also a parasite, often specifically a parasitoid. Hyperparasites are found mainly among the wasp-waisted Apocrita within the Hymenoptera, and in two other insect orders, the Diptera and Coleoptera (beetles). Seventeen families in Hymenoptera and a few species of Diptera and Coleoptera are hyperparasitic. Hyperparasitism developed from primary parasitism, which evolved in the Jurassic period in the Hymenoptera. Hyperparasitism intrigues entomologists because of its multidisciplinary relationship to evolution, ecology, behavior, biological control, taxonomy, and mathematical models.

<span class="mw-page-title-main">Polydnavirus</span> Family of viruses

A polydnavirus (PDV) or more recently, polydnaviriform is a member of the family Polydnaviridae of insect viruses. There are two genera in the family: bracoform and Ichnoviriform. Polydnaviruses form a symbiotic relationship with parasitoid wasps. Ichnoviriforms (IV) occur in Ichneumonid wasps and Bracoviriforms (BV) in Braconid wasps. The larvae of wasps in both of those groups are themselves parasitic on Lepidoptera, and the polydnaviruses are important in circumventing the immune response of their parasitized hosts. Little or no sequence homology exists between BV and IV, suggesting that the two genera have been evolving independently for a long time.

<i>Manduca quinquemaculata</i> Species of moth

Manduca quinquemaculata, the five-spotted hawkmoth, is a brown and gray hawk moth of the family Sphingidae. The caterpillar, often referred to as the tomato hornworm, can be a major pest in gardens; they get their name from a dark projection on their posterior end and their use of tomatoes as host plants. Tomato hornworms are closely related to the tobacco hornworm Manduca sexta. This confusion arises because caterpillars of both species have similar morphologies and feed on the foliage of various plants from the family Solanaceae, so either species can be found on tobacco or tomato leaves. Because of this, the plant on which the caterpillar is found does not indicate its species.

<span class="mw-page-title-main">Braconidae</span> Family of wasps

The Braconidae are a family of parasitoid wasps. After the closely related Ichneumonidae, braconids make up the second-largest family in the order Hymenoptera, with about 17,000 recognized species and many thousands more undescribed. One analysis estimated a total between 30,000 and 50,000, and another provided a narrower estimate between 42,000 and 43,000 species.

<span class="mw-page-title-main">Parasitoid wasp</span> Group of wasps

Parasitoid wasps are a large group of hymenopteran superfamilies, with all but the wood wasps (Orussoidea) being in the wasp-waisted Apocrita. As parasitoids, they lay their eggs on or in the bodies of other arthropods, sooner or later causing the death of these hosts. Different species specialise in hosts from different insect orders, most often Lepidoptera, though some select beetles, flies, or bugs; the spider wasps (Pompilidae) exclusively attack spiders. More rarely, parasitoid wasps may use plant seeds as hosts, such as Torymus druparum.

<span class="mw-page-title-main">Saddleback caterpillar</span> Larva of an eastern North American moth

The saddleback caterpillar is the larva of a species of moth native to eastern North America. It is also found in Mexico. The species belongs to the family of slug caterpillars, Limacodidae.

<span class="mw-page-title-main">Juvenile-hormone esterase</span>

The enzyme juvenile hormone esterase (EC 3.1.1.59, systematic name methyl-(2E,6E,10R)-10,11-epoxy-3,7,11-trimethyltrideca-2,6-dienoate acylhydrolase, JH esterase) catalyzes the hydrolysis of juvenile hormone:

<i>Glyptapanteles</i> Genus of wasps

Glyptapanteles is a genus of endoparasitoid wasps found in all continents, except Antarctica. The larvae of the members of Glyptapanteles sp. are distinguished by their ability to manipulate their hosts into serving as bodyguards.

<i>Euplectrus</i> Genus of wasps

Euplectrus is a genus of hymenopteran insects of the family Eulophidae.

<span class="mw-page-title-main">Ibaliidae</span> Family of wasps

The Ibaliidae are a small family of hymenopteran superfamily Cynipoidea. Ibaliidae differ from most of the cynipoids by the larvae being parasitoids on other wasp larvae in the group Siricidae. The Ibaliidae comprise three extant genera of fairly large wasps, with a total of 20 species, and is a sister group to the rest of the cynipoids except the small subfamily Austrocynipidae.

<i>Cotesia glomerata</i> Species of wasp

Cotesia glomerata, the white butterfly parasite, is a small parasitoid wasp species belonging to family Braconidae. It was first described by Carl Linnaeus in his 1758 publication 10th edition of Systema Naturae.

<i>Cotesia</i> Genus of wasps

Cotesia is a genus of braconid wasps first described by Peter Cameron in 1891. Some species parasitize caterpillars of species considered pests, and are used as biocontrol agents. Cotesia congregata parasitizes the tomato and the tobacco hornworms. C. glomerata and C. rubecula feed on the cabbage white and other white butterfly caterpillars. C. gonopterygis and C. risilis are host-specific and parasitize the common brimstone.

<i>Copidosoma floridanum</i> Species of wasp

Copidosoma floridanum is a species of wasp in the family Encyrtidae which is primarily a parasitoid of moths in the subfamily Plusiinae. It has the largest recorded brood of any parasitoidal insect, at 3,055 individuals. The life cycle begins when a female oviposits into the eggs of a suitable host species, laying one or two eggs per host. Each egg divides repeatedly and develops into a brood of multiple individuals, a phenomenon called polyembryony. The larvae grow inside their host, breaking free at the end of the host's own larval stage.

Bracovirus is a genus of viruses, in the family Polydnaviridae. Bracoviruses are an ancient symbiotic virus contained in parasitic braconid wasps that evolved off of the nudivirus about 190 million years ago and has been evolving at least 100 million years. It is one of two genera belonging to the Polydnaviridae family, Ichnovirus being the other genus. There are 32 species in this genus.

Cotesia rubecula is a parasitoid wasp from the large wasp family Braconidae.

<i>Hemileuca lucina</i> Species of moth

Hemileuca lucina, the New England buck moth, is a species of moth in the family Saturniidae. This moth species is only found in the New England region of the United States. Larvae in early stages mainly feed on broadleaf meadowsweet whereas larvae in later stages show variation in food sources such as blackberry and black cherry leaves. Larvae have a black body with orange/black spines on their back that are used to deter predators. Pupation occurs during the summer and adult moths come out around September.

<span class="mw-page-title-main">Nancy Beckage</span> American entomologist

Nancy Elizabeth Beckage was an American entomologist known for her work on host–parasitoid interactions. She held professorships in entomology and in cell biology and neuroscience at the University of California, Riverside.

Vinnexin is a transmembrane protein whose DNA code is held in a virus genome. When the virus genome is expressed in a cell the vinnexin gene from the virus is made into a functioning protein by the infected cell. The vinnexin protein is then incorporated into the host's cell membranes to alter the way the hosts cells communicate with each other. The altered communication aids the transmission and replication of the virus in complex ways. The communication structure that the vinnexin is involved in is the gap junction and vinnexin forms part of a wider family of proteins that are innexin homologues referred to as pannexins. So far Vinnexins have only been found in Adenovirus and the way they affect the functioning of innexins is being studied in great detail.

References

  1. ↑ Say, T., 1836. Description of new species of North American Hymenoptera, and observations on some already described. Boston Journal of Natural History, Vol. 1, p. 262 (https://www.biodiversitylibrary.org/item/100882#page/265/mode/1up)
  2. 1 2 Beckage, Nancy E.; Tan, Frances F.; Schleifer, Kathleen W.; Lane, Roni D.; Cherubin, Lisa L. (1 January 1994). "Characterization and biological effects of cotesia congregata polydnavirus on host larvae of the tobacco hornworm, manduca sexta". Archives of Insect Biochemistry and Physiology. 26 (2–3): 165–195. doi:10.1002/arch.940260209.
  3. ↑ de Buron, Isaure; Beckage, Nancy E. (May 1992). "Characterization of a polydnavirus (PDV) and virus-like filamentous particle (VLFP) in the braconid wasp Cotesia congregata (Hymenoptera: Braconidae)". Journal of Invertebrate Pathology. 59 (3): 315–327. doi:10.1016/0022-2011(92)90139-U.
  4. 1 2 3 4 Beckage, N.E.; Riddiford, L.M. (1978). "Developmental interactions between the tobacco hornworm Manduca sexta and its Braconid parasite Apanteles congregatus". Entomologia Experimentalis et Applicata. 23 (2): 139–151. doi:10.1111/j.1570-7458.1978.tb03016.x. S2CID   83919666.
  5. ↑ Uzbekov, Rustem; Burlaud-Gaillard, Julien; Garanina, Anastasiia S.; Bressac, Christophe (2017). "The length of a short sperm: Elongation and shortening during spermiogenesis in Cotesia congregata (Hymenoptera, Braconidae)". Arthropod Structure & Development. 46 (2): 265–273. doi:10.1016/j.asd.2016.11.011. PMID   27939748.
  6. ↑ Orr, David (2018). "Hyperparasitoids". North Carolina Cooperative Extension. Retrieved 5 August 2020.
  7. 1 2 Marti, D. (January 2003). "Ovary development and polydnavirus morphogenesis in the parasitic wasp Chelonus inanitus. I. Ovary morphogenesis, amplification of viral DNA and ecdysteroid titres". Journal of General Virology. 84 (5): 1141–1150. doi: 10.1099/vir.0.18832-0 . PMID   12692279.
  8. 1 2 Wyler, T. (January 2003). "Ovary development and polydnavirus morphogenesis in the parasitic wasp Chelonus inanitus. II. Ultrastructural analysis of calyx cell development, virion formation and release". Journal of General Virology. 84 (5): 1151–1163. doi: 10.1099/vir.0.18830-0 . PMID   12692280.
  9. 1 2 3 4 5 6 7 8 Adamo, S.A.; Linn, C.E.; Beckage, N.E. (1997). "Correlation between changes in host behaviour and octopamine levels in the tobacco hornworm Manduca sexta parasitized by the gregarious Braconid parasitoid wasp Cotesia congregata" (PDF). Journal of Experimental Biology. 200 (1): 117–127. doi:10.1242/jeb.200.1.117. PMID   9317459.
  10. 1 2 3 4 5 Zitnan, D; Kingan, TG; Kramer, SJ; Beckage, NE (May 22, 1995). "Accumulation of neuropeptides in the cerebral neurosecretory system of Manduca sexta larvae parasitized by the braconid wasp Cotesia congregata". The Journal of Comparative Neurology. 356 (1): 83–100. doi:10.1002/cne.903560106. PMID   7629311. S2CID   44871854.
  11. ↑ Beckage, N.E.; Riddiford, L.M. (1983). "Growth and development of the endoparasitic wasp Apanteles congregatus: dependence on host nutritional status and parasite load". Physiological Entomology. 8 (3): 231–241. doi:10.1111/j.1365-3032.1983.tb00355.x. S2CID   85599283.
  12. 1 2 3 4 Lavine, M.D.; Beckage, N.E. (January 1996). "Temporal pattern of parasitism-induced immunosuppression in Manduca sexta larvae parasitized by Cotesia congregata". Journal of Insect Physiology. 42 (1): 41–51. doi:10.1016/0022-1910(95)00081-X.
  13. ↑ Adamo, S.A. (2005). "Parasitic Suppression of Feeding in the Tobacco Hornworm, Manduca sexta: Parallels With Feeding Depression After an Immune Challenge". Archives of Insect Biochemistry and Physiology. 60 (4): 185–197. doi:10.1002/arch.20068. PMID   16304613.
  14. 1 2 3 Beckage, N.E.; Templeton, T.J. (1986). "Physiological Effects of Parasitism by Apanteles Congregatus in Terminal-stage Tobacco Hornworm Larvae". Journal of Insect Physiology. 32 (4): 299–314. doi:10.1016/0022-1910(86)90043-0.
  15. ↑ Dunn, P.E.; Ross, D.R. (1989). "Effect of parasitism by Cotesia congregata on the susceptibility of Manduca sexta larvae to bacterial infection". Developmental and Comparative Immunology. 13 (3): 205–216. doi:10.1016/0145-305x(89)90001-3. PMID   2676631.
  16. 1 2 Espagne, E. (8 October 2004). "Genome Sequence of a Polydnavirus: Insights into Symbiotic Virus Evolution". Science. 306 (5694): 286–289. Bibcode:2004Sci...306..286E. doi:10.1126/science.1103066. PMID   15472078. S2CID   12260572.
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