I was looking at old copies of Animal Life magazine, published in Britain in the early 1960s when I came across an article I remembered reading 62 years ago. It was by the French author and self-funded biologist Jean Rostand (1894-1977).
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| Animal Life No 2. October 1962 pp 34-38 |
Jean Rostand was wealthy enough to give up an ‘official’ career in science in order to continue research in his laboratory at home. Well known as a writer about science, the history of science and the human condition in the light of scientific discovery, much of his own research was on the development of amphibians from the egg. Some of his findings were overlooked, ignored or forgotten, only to be rediscovered decades later. He did achieve recognition in France, however, both scientific and literary.
In this article I will only consider one aspect of Rostand’s research: polydactyly in frogs and toads. He had found polydactyly of the hind limb (six toes in this case) in the Common Toad (Bufo bufo) and established it to be genetically determined. But then, in his own words:
...in a pond near Concarneau in Brittany I was surprised to find frogs with six, seven, eight and even nine toes. There was in fact a massive variation, affecting from ten to fifteen per cent of the population of the pond. Unlike the polydactyly of the toad, the polydactyly of the frog is not transmissible to its descendants: it is not, at any rate, transmitted in accordance with the accepted rules. It is simply the benign symptom of a much more serious anomaly which strikes the tadpole larvae and causes therein a considerable modification of the bone structure, the growth of supernumerary feet and the formation of various types of excrescence. All the tadpoles that are severely attacked perish before changing into frogs: the polydactylic adults are therefore survivors. What is the cause of this singular anomaly, which, in some respects, recalls certain malignant proliferations? Must one blame a physico-chemical factor, such as chemical substances or radiations, which are present in the surroundings? Or is it due to an infectious agent, a virus? The first hypothesis seems rather unlikely, because we know of no inorganic factor capable of producing such effects. If the second hypothesis can be proved—which is what I am trying to do at the moment—it is possible that the study of these abnormal larvae will throw some light on the formation mechanism of certain tumours. In any case the exhaustive study of anomalies, whether hereditary or acquired, among toads and frogs could, in one way or another, assist the study of human anomalies.
Rostand had in fact redescribed the syndrome. It had been first observed and reported in France in 1937.
Some observations were compatible with the variable presence of some agent. In some years ponds which had shown the anomaly in tadpoles were completely free of the condition but the cause remained unknown.
In 2017 Alain Dubois reviewed what was known and what was not known about Anomaly P. It has been found in a number of countries in Palaearctic water or green frogs, now separated off in their own genus, Pelophylax but not in frogs of the genus Rana. It may affect all species of Pelophylax including the kleptons between some of those species. The Edible Frog, Rana esculenta, now Pelophylax kl. esculentus, was the form studied by Rostand. Dubois wrote:
Much still remains to be known about the anomaly P: its cause, its geographic distribution, exactly which taxa are affected and why, what is the impact of this syndrome on frog populations, etc. Although this problem attracted the attention, especially of an amateur naturalist, Jean Rostand, mostly in the years 1950-1970, no studies are apparently under way nowadays, in any laboratory or European country, to elucidate these questions. This is surprising and even shocking, especially in view of the strong interest raised in recent years by amphibian anomalies in conservation biology.… Given the fact that this syndrome involves facts of cellular abnormal multiplication and tissue differentiation and growth, its understanding might throw interesting or important lights on some developmental biology problems. More attention should certainly be paid to this unsolved problem by the international scientific community.
But then things did start to happen. A group of Russian workers, later joined by the French, including Alain Dubois, found that Anomaly P is caused by the trematode Strigea robusta, i.e. a fluke. That work was mirrored by studies in North America which showed the devastating effects of trematode infection on some amphibian populations.
The life cycle of S. robusta involves three hosts: planorbid (ramshorn) snails as the first intermediate, then the larvae of amphibians as the second intermediate, with anatid birds (ducks, geese and swans) as the definitive host. An important clue was the occurrence of Anomaly P in water frog tadpoles when raised in tanks containing a species of planorbid snail.
Current evidence is that some amphibians are affected by S. robusta while others are not. In Russia the limbs of other amphibians that live alongside P. ribibundus, the Marsh Frog, and are infected show no abnormalities. Those unaffected are the Smooth Newt (Lissotriton vulgaris)(but see below), Great Crested Newt (Triturus cristatus), Pallas’s Spadefooi Toad (Pelobates vespertinus), Red-bellied Toad (Bombina bombina) and Moor Frog (Rana arvalis). However, there is evidence that when S. robusta appeared in a pond in Germany, the population of Smooth Newts (of which 73% were infected) declined. By contrast, there was no effect on the population of Great Crested Newts, none of which became infected. More recent work indicates that Anomaly P can be induced in toads (Common Toad, Bufo bufo; Green Toad, Bufotes viridis; Batura Toad, Bufotes baturae) by the presence of S. robusta.
Rostand’s experiments in the late 1940s and 50s indicated the existence of a sensitive period for during the early stages of a tadpole’s development for an infectious agent to act. This was confirmed with the experiments in which tadpoles were exposed to S. robusta. Once the toes had formed, the tadpole was safe. There was also evidence that the severe forms of Anomaly P depend on the stage of exposure, the parasite load, the location of the parasites and the degree of immunological protection.
Given the complex nature of the lifecycle of the parasite, variations in the populations of planorbid snails and ducks in a particular pond at a particular time it is perhaps not surprising that the occurrence of Anomaly P at a particular locale varies greatly in intensity.
The mechanism by which the trematode exerts its effect on the tadpole is beyond the scope of this article. However, research on trematode infection on development of the limb in North American amphibians suggested the production by the cercariae stage of the trematode of an excess of a Vitamin A metabolite which affects gene expression adversely.
There are, of course, unanswered questions, many on the ecological consequences of infection with the parasite. It also seems odd the parasite seems to be acting in a very unparasitical way—the selection pressure on parasites lies strongly against killing their hosts.
Rostand—the great ‘amateur’ developmental biologist—was right to conclude that the cause of Anomaly P is an infectious agent. However, it was not a virus but something much bigger, the fluke Strigea robusta.
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| From Svinin et al. 2020 |
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| From Svinin et al 2023 |
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| Jean Rostand Animal Life No 2. October 1962 |
Dubois A. 2017. Rostand’s anomaly P in Palaearctic green frogs (Pelophylax) and similar anomalies in amphibians. Mertensiella 25, 49-56
Svinin A, Bashinskiy I, Ermakov O, Litvinchuk S. 2023. Effects of minimum Strigea robusta (Digenea: Strigeidae) cercariae doses and localization of cystson the anomaly P manifestation in Pelophylax lessonae (Anura: Ranidae) tadpoles. Parasitology Research 122, 889-894. doi: 10.1007/s00436-022-07778-z
Svinin AO, Bashinskiy IV, Litvinchuk SN, Ermakov OA, Ivanov AY, Neymark LA, Vedernikov AA, Osipov VV, Drobot GP, Dubois A. 2020. Strigea robusta causes polydactylyand severe forms of Rostand’s anomaly P in water frogs. Parasites & Vectors 13, 381 doi.org/10.1186s13071-020-04256-2
Svinin AO, Chikhlyaev IV, Bashinskiy IW, Osipov VV, Neymark LA, Ivanov AY, Stoyko TG, Chernigova PI, Ibrogimova PK, Litvinchuk SN, Ermakov OA. 2023. Diversity of trematodes from the amphibian anomaly P hotspot: Role of planorbid snails. PLoS ONE 18(3): e0281740. doi.org/10.1371/journal.pone.0281740
Svinin A, Ermakov O, Litvinchuk S. 2022. The incidence of the anomaly P syndrome in water frogs (Anura, Ranidae, Pelophylax) from the Middle Volga River (Russia). Herpetozoa 35, 283–288 doi: 10.3897/herpetozoa.35.e95928
Svinin AO, Matushkina KA, Dedukh DV, Bashinskiy IV, Ermakov, OA, Litvinchuk SN. 2022. Strigea robusta (Digenea: Strigeidae) infection effects on the gonadal structure and limb malformation in toad early development. Journal of Experimental Zoology A 337, 675-686 doi.org/10.1002/jez.2599
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