Presence of Ribeiroia ondatrae in the developing anuran limb disrupts retinoic acid levels

Szuroczki, Dorina; Vesprini, Nicholas D.; Jones, Timothy R. B.; Spencer, Gaynor E.; Carlone, Robert L.

doi:10.1007/s00436-011-2451-z

Cited by 8 publications

(6 citation statements)

References 32 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Therefore, the teratogenic effects appear to be taxon specific. The teratogenic factor was supposed to be retinoic acid in the trematode Ribeiroia ondatrae [48]. In the case of anomaly P, the teratogenic factor can influence the expression levels of HoxD genes [49,50] and lead to a peculiar morphology with the reduction of the hind limb's proximal parts (brachymely) and multiplication of the distal parts (polydactyly).…”

Section: Discussionmentioning

confidence: 99%

Strigea robusta causes polydactyly and severe forms of Rostand’s anomaly P in water frogs

et al. 2020

View full text Add to dashboard Cite

Background: Cases of polydactyly in natural populations of amphibians have attracted great interest from biologists. At the end of the 1940s, the French biologist Jean Rostand discovered a polymorphic syndrome in some water frog (Anura: Pelophylax) populations that included polydactyly and some severe morphological anomalies (he called it 'anomaly P'). The cause of this anomaly remains unknown for 70 years. In a previous study, we obtained anomaly P in the laboratory in tadpoles of water frogs that developed together with molluscs Planorbarius corneus (Mollusca: Gastropoda) collected in the field. We thus proposed the 'trematode hypothesis' , according to which the infectious agent responsible for anomaly P is a trematode species. Methods: Metacercariae from tadpoles with anomaly P were identified using ITS2 gene sequencing as Strigea robusta (Trematoda: Strigeidae). To verify teratogenic features of the species, cercariae of S. robusta were tested for the possibility to cause anomalies. Identification of cercariae species was made using morphological and molecular methods (sequencing of ITS2 and 28S rRNA). The tadpoles were exposed to parasites at four doses of cercariae (control, low, medium and high) and divided into two groups: "early" (at 25-27 Gosner stages) and "late" (at 29-34 Gosner stages) exposure. Results: A total of 58 (72.5%) tadpoles survived until metamorphosis under the dose-dependent experiment with the trematode S. robusta. Differences in the survival rates were observed between the exposed and unexposed tadpoles both in the group of "early" tadpoles and "late" tadpoles. The exposure of tadpoles to the cercariae of S. robusta induced anomaly P in 82% of surviving tadpoles. The severe forms developed only in "early" stages under all doses of cercariae exposure. Polydactyly predominantly developed in the "late" stages; under a light exposure dose, polydactyly also developed in "early" tadpoles. Laboratory-hatched tadpoles reared together with infected snails had different rates of survival and complexity of deformations associated with the period of coexistence. Conclusions: The experiments with direct cercariae exposure provide compelling evidence that S. robusta leads to anomaly P in tadpoles of water frogs. The manifestation of anomaly P turned out to be dependent on the stage of development, cercariae dose, and the location of the cysts.

show abstract

Section: Discussionmentioning

confidence: 99%

Strigea robusta causes polydactyly and severe forms of Rostand’s anomaly P in water frogs

et al. 2020

View full text Add to dashboard Cite

show abstract

“…In this host, however, all 47 specimens examined during 2014-2015 from the Lake Balaton exhibited this malformation. The cause of the bifurcation of the gill filaments caused by the Echinochasmus infection in ruffe is not known, but it may be a similar mechanism to that of R. ondatrae infection in amphibians, where Szuroczki et al (2012) have suggested that an increased level of retinoic acid might result in the malformations.…”

Section: Discussionmentioning

confidence: 99%

Malformations of the gill filaments of the ruffe Gymnocephalus cernuus (L.) (Pisces) caused by echinostomatid metacercariae

Molnár

Gibson

Majoros

et al. 2016

Journal of Fish Diseases

View full text Add to dashboard Cite

In parasite surveys of fishes from Lake Balaton and its tributaries in Hungary, infections with metacercariae of a species of the digenean genus Echinochasmus (Trematoda: Echinostomatidae) were found in seven species of fish. In ruffe, Gymnocephalus cernuus, malformations of the gill filaments apparently caused by these infections were observed. These malformations were in the form of bifurcations of the filaments at about their mid‐length. At the point where the filaments bifurcate, an Echinochasmus metacercaria was always embedded in the cartilaginous ray of the gill filament. All specimens of the ruffe were found to be infected by these metacercariae, and each ruffe specimen was infected by 30–300 metacercariae. Such a bifurcation was found in all of the ruffe specimens, but, apart from these gill malformations, the metacercariae produced only local changes in the cartilage. In the other six infected fish species, only local signs were observed in the cartilage. Experimental infections of chicks with metacercariae resulted in the finding of the sexual adult (marita) of an unidentified species of Echinochasmus. ITS sequences of the adult and metacercaria corresponded with each other, and also with a cercaria isolated from a gravel snail (Lithoglyphus naticoides), with a 99.5–100% similarity.

show abstract

“…Полиморфная природа также наблюдалась в случае аномалий Войткевича (Woitkewich 1961), деформаций у головастиков и сеголеток зеленых жаб (Henle et al 2017c,d), массовых аномалий задних конечностей, полученных в лабораторных экспериментах у шпорцевой лягушки Xenopus laevis (Коваленко [Kovalenko] 2000), а также при «аномалии P» (Rostand 1971) у зелёных лягушек рода Pelophylax, которой посвящен настоящий обзор. Механизмы индукции таких полиморфных синдромов, даже в самых изученных случаях с инвазией трематод рода Ribeiroia, до сих пор до конца непонятны и оставляют множество нерешенных вопросов (Szuroczki et al 2012).…”

Section: C Dunclassified

“…Сешен с соавторами (Session et al 1999) в этом же номере журнала "Science" показали, что дублирование конечностей под действием метацеркарий трематод было связано с механическими причинами, а не с влиянием ретиноидов. Тем не менее, спустя 12 лет было обнаружено, что концентрация различных форм ретиноевой кислоты в развивающейся аномальной конечности головастика выше на 70% по сравнению с контролем (Szuroczki et al 2012). По мере накопления новых данных было выявлено, что эта трематода вызывает деформации конечностей у порядка 60 видов амфибий как минимум в 46 штатах США (Johnson and Sutherland 2003).…”

Section: трематодная гипотеза развития аномалииunclassified

The anomaly P syndrome in green frogs: the history of discovery, morphological features and possible causes

et al. 2020

View full text Add to dashboard Cite

The anomaly P in green frogs was firstly found in 1952 in France by French writer and scientist Jean Rostand. Mild form of anomaly P manifestation includes polydactyly, while complex morphological transformations affect the fore and hindlimbs and include combinations of traits: polydactyly, brachymely, hind limb flexion, small additional limbs, bone outgrowths, tumors and edema in the hind limbs. Rostand experimentally showed that this anomaly is not inherited and is caused by some environmental factors. It was recorded only in Western Palearctic green frogs of the genus Pelophylax and was absent in other amphibian species, despite their syntopic occurrence. The severe cases of anomaly P were not found for a long time by researchers and were re-discovered after half a century since its last observation. A new record was made in 2016 in the central part of Russia in the Privolzhskaya Lesostep’ nature reserve. The morphological features of the anomalous frogs in the study area turned out to be similar to those described by Rostand. Symmetric polydactyly, brachymely, hind limb flexion, edema of hind limbs, small additional limbs in thighs, outgrowths, and concomitant anomalies – mandibular hypoplasia, unmoved hind limb, open opercular chamber. The frequency of occurrence of the anomaly in the studied population reached 24.7% (n = 384). Moreover, the “severe forms” of the anomaly P were noted in 4.7% of cases, and the “light” (polydactyly) in 20.0%. Growing tadpoles together with freshwater mollusks allowed us to obtain the anomaly P in the laboratory. It was revealed that the mollusks Planorbarius corneus are the intermediate hosts (vectors) for the “infectious agent” of this anomaly. As the most possible cause of the anomaly, the infection by trematodes species is considered.

show abstract

Presence of Ribeiroia ondatrae in the developing anuran limb disrupts retinoic acid levels

Cited by 8 publications

References 32 publications

Strigea robusta causes polydactyly and severe forms of Rostand’s anomaly P in water frogs

Strigea robusta causes polydactyly and severe forms of Rostand’s anomaly P in water frogs

Malformations of the gill filaments of the ruffe Gymnocephalus cernuus (L.) (Pisces) caused by echinostomatid metacercariae

The anomaly P syndrome in green frogs: the history of discovery, morphological features and possible causes

Contact Info

Product

Resources

About