Schistocephalus solidus

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Schistocephalus solidus
Stickleback with Schostocephalus (cropped).jpg
Schistocephalus solidus with its host, the three-spined stickleback
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Platyhelminthes
Class: Cestoda
Order: Diphyllobothriidea
Family: Diphyllobothriidae
Genus: Schistocephalus
Species:
S. solidus
Binomial name
Schistocephalus solidus
(Müller, 1776) Steenstrup, 1857
Synonyms [1]
  • Taenia solidusMüller, 1776

Schistocephalus solidus is a tapeworm of fish, fish-eating birds and rodents. This hermaphroditic parasite belongs to the Eucestoda subclass, of class Cestoda. This species has been used to demonstrate that cross-fertilization produces a higher infective success rate than self-fertilization. [2] [3]

Contents

Life cycle

Life cycle of Schistocephalus solidus Life cycle of Schistocephalus solidus.jpg
Life cycle of Schistocephalus solidus

It parasitizes fish and fish-eating water birds. The fish-eating water bird is the definitive host, and reproduction occurs in the bird's intestine. Eggs of the tapeworm are passed with the bird's feces and hatch in the water, where the first larval stage, the coracidium, is produced. The coracidium is then ingested by the first intermediate host, a cyclopoid copepod (e.g. Macrocyclops albidus ). The second larval stage then subsequently develops in the tissue of this host. Within one to two weeks, the infected copepod is ingested by the second intermediate host, the three-spined stickleback, Gasterosteus aculeatus. The third larval stage, the plerocercoid, grows in the abdomen of the fish. When the fish is eaten by a bird, the larvae mature and adults start to produce eggs within two days. Reproduction takes place within one to two weeks, after which the parasite dies. [4]

Ecology

Prevalence — the proportion of host population infected — in naturally infected populations of the first intermediate hosts is likely low. [5] Conversely, in populations where Schistocephalus solidus infects the second intermediate host (three-spined stickleback) it can reach high prevalence, up to 93% in both European and North American populations [6] [7]

The growth of S. solidus in the second intermediate host is largely dependent upon the environmental temperatures. At an increase of temperature from 15 °C to 20 °C the growth of S. solidus can grow four times as fast. At the same time, the growth rate of the stickleback is significantly reduced. [8]

Reproduction

Reproduction of S. solidus in the definitive bird host in which it resides for a maximum of two weeks. [4] Because adult worms are hermaphroditic eggs can be fertilised in three different ways; (1) self-fertilization (2) breeding with a sibling (3) breeding with an unrelated individual. [3] In most species outbreeding (mating with an unrelated individual) would be preferred, [9] but advantages and disadvantages of each of these breeding strategies have been argued. [10] In short, self-fertilization is advantageous when no mating partners are around, but might lead to inbreeding depression—the reduced fitness of offspring because of the unmasking of deleterious recessive alleles due to the breeding of closely related individuals. Similarly, breeding with a sibling, also known as incestuous mating, also shares some of the same disadvantages as self-fertilization does—inbreeding depression and lack of genetic variation. But incestuous mating is advantageous because it helps maintain gene complexes within the family which may be important for local adaptation. Breeding with unrelated individuals might seem to be most advantageous choice of mating because it increases genetic variation and avoids inbreeding depression, but it could be more time-consuming as partners might not always be available. [3]

In Schistocephalus solidus inbreeding is indeed disadvantageous, as mating between siblings generally produce a 3.5 times reduction in hatching success of the eggs produced from these matings compared to mating with unrelated individuals. [2] [10] Outcrossing also increases the chances of infecting the second intermediate host. [11] However, there is also a preference to pair with larger mates, and to avoid very small mates. [12] The later means that self-fertilisation can also occur when potential partners are available. Under some circumstances, there could exist a significant advantage for incestuous mating, despite inbreeding depression. [13] In species where there is low parental investment and sexual encounters are rare and sequential, incestuous breeding is indirectly beneficial. If the prospective mates are related there is an increase mutual interest in finding a resolution with respect to playing the unpreferred sexual role. With less time allotted to conflicting over sexual roles and dominating one another, procreation is more cost-effective. Under these conditions, the greater effectiveness of inbreeding prevails over the detriment of incestuous mating and evolutionarily select for a preference for related mates. [13]

Infectivity

Corracidia are more infective to male copepods than to female copepods. [14] This has been suggested to be due to the negative impacts sex hormones such as testosterone can have on the immune system.

Viruses

Schistocephalus solidus itself a parasite, can also get infected by parasites (known as hyperparasites), including viruses. [15] These viruses are likely to affect the evolution of the virulence and broader interactions of S. solidus with its hosts. [15] [16]

Host manipulation

The Schistocephalus solidus parasite is capable of host manipulation in both intermediate hosts, the copepod and the three-spined stickleback.

First intermediate host

In the copepod host, it is able to suppress activity while uninfective to the stickleback host. [17] This reduces the likelihood of the copepod host being consumed and consequently unsuccessful transmission of the parasite. [18] Once the parasite becomes infective, after approximately two weeks, activity increases [17] and, as a consequence, the risk of consumption by three-spined sticklebacks increases. [19] However, when multiple, non-simultaneous infections by S. solidus occur, host manipulation is orchestrated by the first infecting parasite. This increases the risk of premature consumption of the subsequent infections by the fish host. [20] Consistent differences in manipulation are seen between parasite genotypes [21] and populations. [22] Differences in host genotypes are maintained after infections, but less pronounced. [21]

Second intermediate host

In the fish host, host manipulation induces more risk taking behaviour like positive geotaxis [23] and negative thigmotaxis. [24] This change in behaviour is unlikely to be caused solely by the mechanical presence of the parasite. Phenotype modification, through injecting silicon "parasites", with densities and sizes similar to infective plerocercoids (~150 mg) did not alter behaviour. [24] Physiologically, S. solidus is a parasite that inhibits egg production in female three-spined sticklebacks in European populations, [6] but not in Alaskan populations where only egg mass is reduced. [7] [25] The egg mass of fish was correlated to the parasite index, which indicates that the reduction in egg mass is a non-adaptive side effect of parasite infection.

Model species

Schistocephalus solidus is effectively used a model species for studying the evolutionary dynamics of host-parasite interactions. [26] [27] More recently, it was proposed a model to study host-parasite-microbe interactions [28]

in vitro breeding

The option to breed S. solidus in the laboratory [29] makes them a useful model for studying host-parasite interactions. [26] For 'culturing' of the worm progenetic plerocercoids are dissected from the stickleback host. The worm can then be incubated in a dialysis tube embedded in culture medium and kept at 40 °C. [29] These worms are then ideally incubated in pairs of similar size to maximise outcrossing and egg hatching. [12] Optionally, large S. solidus worms can also be cut into smaller pieces and incubated separately. [30]

Related Research Articles

<span class="mw-page-title-main">Three-spined stickleback</span> Species of fish

The three-spined stickleback is a fish native to most inland and coastal waters north of 30°N. It has long been a subject of scientific study for many reasons. It shows great morphological variation throughout its range, ideal for questions about evolution and population genetics. Many populations are anadromous and very tolerant of changes in salinity, a subject of interest to physiologists. It displays elaborate breeding behavior and it can be social making it a popular subject of inquiry in fish ethology and behavioral ecology. Its antipredator adaptations, host-parasite interactions, sensory physiology, reproductive physiology, and endocrinology have also been much studied. Facilitating these studies is the fact that the three-spined stickleback is easy to find in nature and easy to keep in aquaria.

<i>Diphyllobothrium</i> Genus of flatworms

Diphyllobothrium is a genus of tapeworms which can cause diphyllobothriasis in humans through consumption of raw or undercooked fish. The principal species causing diphyllobothriasis is D. latum, known as the broad or fish tapeworm, or broad fish tapeworm. D. latum is a pseudophyllid cestode that infects fish and mammals. D. latum is native to Scandinavia, western Russia, and the Baltics, though it is now also present in North America, especially the Pacific Northwest. In Far East Russia, D. klebanovskii, having Pacific salmon as its second intermediate host, was identified.

<span class="mw-page-title-main">Pseudophyllidea</span> Order of flatworms

Pseudophyllid cestodes are tapeworms with multiple "segments" (proglottids) and two bothria or "sucking grooves" as adults. Proglottids are identifiably pseudophyllid as the genital pore and uterine pore are located on the mid-ventral surface, and the ovary is bilobed ("dumbbell-shaped").

Spirometra is a genus of pseudophyllid cestodes that reproduce in canines and felines, but can also cause pathology in humans if infected. As an adult, this tapeworm lives in the small intestine of its definitive host and produces eggs that pass with the animal's feces. When the eggs reach water, the eggs hatch into coracidia which are eaten by copepods. The copepods are eaten by a second intermediate host to continue the life cycle. Humans can become infected if they accidentally eat frog legs or fish with the plerocercoid stage encysted in the muscle. In humans, an infection of Spirometra is termed sparganosis.

<span class="mw-page-title-main">Eucestoda</span> Subclass of flatworms

Eucestoda, commonly referred to as tapeworms, is the larger of the two subclasses of flatworms in the class Cestoda. Larvae have six posterior hooks on the scolex (head), in contrast to the ten-hooked Cestodaria. All tapeworms are endoparasites of vertebrates, living in the digestive tract or related ducts. Examples are the pork tapeworm with a human definitive host, and pigs as the secondary host, and Moniezia expansa, the definitive hosts of which are ruminants.

Spirometra erinaceieuropaei is a parasitic tapeworm that infects domestic animals and humans. The medical term for this infection in humans and other animals is sparganosis. Morphologically, these worms are similar to other worms in the genus Spirometra. They have a long body consisting of three sections: the scolex, the neck, and the strobilia. They have a complex life cycle that consists of three hosts, and can live in varying environments and bodily tissues. Humans can contract this parasite in three main ways. Historically, humans are considered a paratenic host; however, the first case of an adult S. erinaceieuropaei infection in humans was reported in 2017. Spirometra tapeworms exist worldwide and infection is common in animals, but S. erinaceieuropaei infections are rare in humans. Treatment for infection typically includes surgical removal and anti-worm medication.

Sparganosis is a parasitic infection caused by the plerocercoid larvae of the genus Spirometra including S. mansoni, S. ranarum, S. mansonoides and S. erinacei. It was first described by Patrick Manson in 1882, and the first human case was reported by Charles Wardell Stiles from Florida in 1908. The infection is transmitted by ingestion of contaminated water, ingestion of a second intermediate host such as a frog or snake, or contact between a second intermediate host and an open wound or mucous membrane. Humans are the accidental hosts in the life cycle, while dogs, cats, and other mammals are definitive hosts. Copepods are the first intermediate hosts, and various amphibians and reptiles are second intermediate hosts.

Pomphorhynchus laevis is an endo-parasitic acanthocephalan worm, with a complex life cycle, that can modify the behaviour of its intermediate host, the freshwater amphipod Gammarus pulex. P. laevis does not contain a digestive tract and relies on the nutrients provided by its host species. In the fish host this can lead to the accumulation of lead in P. laevis by feeding on the bile of the host species.

<i>Hymenolepis</i> (flatworm) Genus of worms

Hymenolepis is a genus of cyclophyllid tapeworms that cause hymenolepiasis. They parasitise mammals, including humans. Some notable species are:

<span class="mw-page-title-main">Cestoda</span> Class of flatworms

Cestoda is a class of parasitic worms in the flatworm phylum (Platyhelminthes). Most of the species—and the best-known—are those in the subclass Eucestoda; they are ribbon-like worms as adults, known as tapeworms. Their bodies consist of many similar units known as proglottids—essentially packages of eggs which are regularly shed into the environment to infect other organisms. Species of the other subclass, Cestodaria, are mainly fish infecting parasites.

Diphyllobothrium mansonoides is a species of tapeworm (cestodes) that is endemic to North America. Infection with D. mansonoides in humans can result in sparganosis. Justus F. Mueller first reported this organism in 1935. D. mansonoides is similar to D. latum and Spirometra erinacei. When the organism was discovered, scientist did not know if D. mansonoides and S. erinacei were separate species. PCR analysis of the two worms has shown the two to be separate but closely related organisms.

<span class="mw-page-title-main">Fish diseases and parasites</span> Disease that affects fish

Like humans and other animals, fish suffer from diseases and parasites. Fish defences against disease are specific and non-specific. Non-specific defences include skin and scales, as well as the mucus layer secreted by the epidermis that traps microorganisms and inhibits their growth. If pathogens breach these defences, fish can develop inflammatory responses that increase the flow of blood to infected areas and deliver white blood cells that attempt to destroy the pathogens.

Bothriocephalus acheilognathi, also known as the Asian tapeworm, is a freshwater fish parasite that originated from China and Eastern Russia. It is a generalized parasite that affects a wide variety of fish hosts, particularly cyprinids, contributing to its overall success.

<i>Raillietina</i> Genus of flatworms

Raillietina is a genus of tapeworms that includes helminth parasites of vertebrates, mostly of birds. The genus was named in 1920 in honour of a French veterinarian and helminthologist, Louis-Joseph Alcide Railliet. Of the 37 species recorded under the genus, Raillietina demerariensis, R. asiatica, and R. formsana are the only species reported from humans, while the rest are found in birds. R. echinobothrida, R. tetragona, and R. cesticillus are the most important species in terms of prevalence and pathogenicity among wild and domestic birds.

<i>Hymenolepis microstoma</i> Species of flatworm

Hymenolepis microstoma, also known as the rodent tapeworm, is an intestinal dwelling parasite. Adult worms live in the bile duct and small intestines of mice and rats, and larvae metamorphose in the haemocoel of beetles. It belongs to the genus Hymenolepis; tapeworms that cause hymenolepiasis. H. microstoma is prevalent in rodents worldwide, but rarely infects humans.

Behavior-altering parasites are parasites capable of causing changes in the behavior of their hosts species to enhance their transmission, sometimes directly affecting the hosts' decision-making and behavior control mechanisms. By way of example, a parasite that reproduces in an intermediate host may require, as part of their life cycle, that the intermediate host be eaten by a predator at a higher trophic level, and some parasites are capable of altering the behavior of the intermediate host to make such predation more likely; a mechanism that has been called parasite increased trophic facilitation or parasite increased trophic transmission. Examples can be found in bacteria, protozoa, viruses, and animals. Parasites may also alter the host behavior to increase protection of the parasites or their offspring; the term bodyguard manipulation is used for such mechanisms.

<i>Raillietina tetragona</i> Species of flatworm

Raillietina tetragona is a parasitic tapeworm belonging to the class Cestoda. It is a cosmopolitan helminth of the small intestine of pigeon, chicken and guinea fowl, and is found throughout the world.

Flamingolepis liguloides is a parasitic tapeworm of the Cestoda class. There are several tapeworms that are found to infect Artemia; however, F. liguloides is the most prevalent species of infectious tapeworm among Artemia. F. liguloides infects brine shrimp (Artemia) as the intermediate host and flamingos as the definitive host. Effects of the tapeworm in flamingos is unclear, though researchers hypothesize that a high parasitemia could potentially be deadly to the host. The parasite appears to affect the Artemia spp. as it alters the behavior and color of its host.

<i>Diphyllobothrium dendriticum</i> Species of Cestoda

Diphyllobothrium dendriticum is a large pseudophyllid cestode of the family Diphyllobothriidae.

Glaridacris catostomi is a flatworm of the family Caryophyllaeidae. It is commonly found in freshwater environments of North America and is a known internal parasite of fishes of the family Catostomidae.

References

  1. ↑ "Schistocephalus solidus". Global Biodiversity Information Facility .
  2. 1 2 Christen M; Kurtz J; Milinski M (2002). "Outcrossing increases infection success and competitive ability: experimental evidence from a hermaphrodite parasite". Evolution. 56 (11): 2243–51. doi:10.1554/0014-3820(2002)056[2243:oiisac]2.0.co;2. PMID   12487354. S2CID   20906916.
  3. 1 2 3 Schjørring, Solveig (2004). "Delayed selfing in relation to the availability of a mating partner in the cestode Schistocephalus solidus". Evolution. 58 (11): 2591–2596. doi:10.1554/04-270. PMID   15612301. S2CID   198155264.
  4. 1 2 Dubinina, Mariia Nikolaevna (1980). Tapeworms (Cestoda, Ligulidae) of the fauna of the USSR.
  5. ↑ Zander, C. D.; Groenewold, S.; Strohbach, U. (1994). "Parasite transfer from crustacean to fish hosts in the Lübeck Bight, SW Baltic Sea". Helgoländer Meeresuntersuchungen. 48 (1): 89–105. Bibcode:1994HM.....48...89Z. doi: 10.1007/BF02366204 .
  6. 1 2 McPhail, J. D.; Peacock, S. D. (1983). "Some effects of the Cestode (Schistocephalus solidus) on reproduction in the threespine stickleback (Gasterosteus aculeatus), evolutionary aspects of a host-parasite interaction". Canadian Journal of Zoology. 61 (4): 901–908. doi:10.1139/z83-118.
  7. 1 2 Heins, David C; Singer, Scarlet S; Baker, John A (1999). "Virulence of the cestode Schistocephalus solidus and reproduction in infected threespine stickleback, Gasterosteus aculeatus". Canadian Journal of Zoology. 77 (12): 1967–1974. doi:10.1139/z99-180.
  8. ↑ Macnab, Vicki; Barber, Iain (2012). "Some (worms) like it hot: fish parasites grow faster in warmer water, and alter host thermal preferences". Global Change Biology. 18 (5): 1540–1548. Bibcode:2012GCBio..18.1540M. doi:10.1111/j.1365-2486.2011.02595.x. S2CID   86103632.
  9. ↑ Galvani, Alison P.; Coleman, Ronald M.; Ferguson, Neil M. (2003). "The maintenance of sex in parasites". Proceedings of the Royal Society of London. Series B: Biological Sciences. 270 (1510): 19–28. doi:10.1098/rspb.2002.2182. PMC   1691212 . PMID   12590767.
  10. 1 2 Schjørring, Solveig; Jäger, Ilonka (2007). "Incestuous mate preference by a simultaneous hermaphrodite with strong inbreeding depression". Evolution. 61 (2): 423–430. doi:10.1111/j.1558-5646.2007.00028.x. PMID   17348951. S2CID   2396487.
  11. ↑ Christen, M.; Milinski, M. (2003). "The consequences of self-fertilization and outcrossing of the cestode Schistocephalus solidus in its second intermediate host". Parasitology. 126 (4): 369–378. doi:10.1017/s0031182003002956. PMID   12741516. S2CID   21430425.
  12. 1 2 Lüscher, A.; Wedekind, C. (2002). "Size-dependent discrimination of mating partners in the simultaneous hermaphroditic cestode Schistocephalus solidus". Behavioral Ecology. 13 (2): 254–259. doi:10.1093/beheco/13.2.254.
  13. 1 2 Kokko, Hanna; Ots, Indrek (2006). "When not to avoid inbreeding". Evolution. 60 (3): 467–475. doi: 10.1111/j.0014-3820.2006.tb01128.x . PMID   16637492.
  14. ↑ Wedekind, Claus; Jakobsen, Per J. (1998). "Male-Biased Susceptibility to Helminth Infection: An Experimental Test with a Copepod". Oikos. 81 (3): 458. Bibcode:1998Oikos..81..458W. doi:10.2307/3546767. JSTOR   3546767.
  15. 1 2 Hahn, Megan A.; Rosario, Karyna; Lucas, Pierrick; Dheilly, Nolwenn M. (2020). "Characterization of viruses in a tapeworm: phylogenetic position, vertical transmission, and transmission to the parasitized host". The ISME Journal. 14 (7): 1755–1767. Bibcode:2020ISMEJ..14.1755H. doi:10.1038/s41396-020-0642-2. PMC   7305300 . PMID   32286546.
  16. ↑ Dheilly, Nolwenn M.; Poulin, Robert; Thomas, Frédéric (2015). "Biological warfare: Microorganisms as drivers of host–parasite interactions". Infection, Genetics and Evolution. 34: 251–259. Bibcode:2015InfGE..34..251D. doi:10.1016/j.meegid.2015.05.027. PMID   26026593.
  17. 1 2 Hammerschmidt, Katrin; Koch, Kamilla; Milinski, Manfred; Chubb, James C.; Parker, Geoff A. (2009). "When to go: optimization of host switching in parasites with complex life cycles". Evolution. 63 (8): 1976–1986. doi: 10.1111/j.1558-5646.2009.00687.x . PMID   19453381.
  18. ↑ Weinreich, F.; Benesh, D. P.; Milinski, M. (2012). "Suppression of predation on the intermediate host by two trophically-transmitted parasites when uninfective". Parasitology. 140 (1): 129–135. doi:10.1017/S0031182012001266. PMID   22906915. S2CID   25700997.
  19. ↑ Wedekind, C.; Milinski, M. (2009). "Do three-spined sticklebacks avoid consuming copepods, the first intermediate host of Schistocephalus solidus? — an experimental analysis of behavioural resistance" (PDF). Parasitology. 112 (4): 371–383. doi:10.1017/S0031182000066609. S2CID   83852280.
  20. ↑ Hafer, Nina; Milinski, Manfred (2015). "When parasites disagree: Evidence for parasite-induced sabotage of host manipulation". Evolution. 69 (3): 611–620. doi:10.1111/evo.12612. PMC   4409835 . PMID   25643621.
  21. 1 2 Benesh, Daniel P. (2019). "Tapeworm manipulation of copepod behaviour: parasite genotype has a larger effect than host genotype". Biology Letters. 15 (9): 20190495. doi: 10.1098/rsbl.2019.0495 . PMC   6769145 . PMID   31506036.
  22. ↑ Hafer, Nina (2018). "Differences between populations in host manipulation by the tapeworm Schistocephalus solidus – is there local adaptation?". Parasitology. 145 (6): 762–769. doi: 10.1017/S0031182017001792 . hdl: 21.11116/0000-0000-2CD7-D . PMID   29113596.
  23. ↑ Barber, Iain; Svensson, P. Andreas; Walker, Peter (2004). "Behavioural Responses to Simulated Avian Predation in Female Three Spined Sticklebacks: The Effect of Experimental Schistocephalus Solidus Infections". Behaviour. 141 (11–12): 1425–1440. doi:10.1163/1568539042948231.
  24. 1 2 Grécias, Lucie; Valentin, Julie; Aubin-Horth, Nadia (2018). "Testing the parasite mass burden effect on alteration of host behaviour in the Schistocephalus-stickleback system". The Journal of Experimental Biology. 221 (6): jeb174748. doi: 10.1242/jeb.174748 . PMID   29444843.
  25. ↑ Heins, David C.; Baker, John A. (2003). "Reduction of egg size in natural populations of threespine stickleback infected with a cestode macroparasite". Journal of Parasitology. 89 (1): 1–6. doi:10.1645/0022-3395(2003)089[0001:ROESIN]2.0.CO;2. PMID   12659295. S2CID   24098353.
  26. 1 2 Barber, Iain (2013). "Sticklebacks as model hosts in ecological and evolutionary parasitology". Trends in Parasitology. 29 (11): 556–566. doi:10.1016/j.pt.2013.09.004. PMID   24145060.
  27. ↑ Barber, I.; Scharsack, J. P. (2010). "The three-spined stickleback- Schistocephalus solidus system: an experimental model for investigating host-parasite interactions in fish". Parasitology. 137 (3): 411–424. doi:10.1017/S0031182009991466. hdl: 2381/8014 . PMID   19835650. S2CID   8041954.
  28. ↑ Hahn, Megan A.; Dheilly, Nolwenn M. (2016). "Experimental models to study the role of microbes in host-parasite interactions". Frontiers in Microbiology. 7: 1300. doi: 10.3389/fmicb.2016.01300 . PMC   4993751 . PMID   27602023.
  29. 1 2 Smyth, J.D.; McManus, D.P. (1989). The Physiology and Biochemistry of Cestodes. Cambridge: Cambridge University Press. doi:10.1017/CBO9780511525841. ISBN   9780511525841.
  30. ↑ Weinreich, Friederike; Kalbe, Martin; Benesh, Daniel P. (2014). "Making the in vitro breeding of Schistocephalus solidus more flexible". Experimental Parasitology. 139: 1–5. doi:10.1016/j.exppara.2014.02.002. hdl: 11858/00-001M-0000-0019-7F35-C . PMID   24560832.
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