In this article we will discuss about Neoteny:- 1. History of Neoteny 2. Types of Neoteny 3. Factors 4. Genetics 5. Significance.
Contents:
- History of Neoteny
- Types of Neoteny
- Factors for Neoteny
- Genetics of Neoteny
- Significance of Neoteny
1. History of Neoteny:
Since many years the size difference of the adult and larval phase of spotted salamander was noted. The larvae of salamander usually attain the size of 8 cm while the metamorphosed adults measure only 4 cm.
Sexually mature gilled larvae of Triton are also known to exist since long time. De Filippi recorded 40 such sexually mature gilled larvae of 5.5 cm in size in one locality of Lombardy. He has also found that similar specimens were available in a lake of Val Formazzo located on the Italian slope of the Alps.
The adult Ambystoma and its larval phase (now known as Axolotl) were known since long time. They were earlier erroneously regarded to be the adult of different species of Urodele related to a per-ennibranchiate form, specially to Siren. But Cuvier suspected the biological status of Axolotl larva and regarded it to be a urodele larva.
The so-called Axolotl was variously named as Siredon axolotl, Siredon mexicanus, Siredon pisciformis, etc. The larvae were noticed by the Spanish settlers in different lakes in Mexico. The natives used to take the larvae as food and called them as Axolotl, meaning ‘play in the water’.
Dumeril was the first to establish the truth that the axolotl larvae could metamorphose into the entirely lung-breathing and land-dwelling adult Ambystoma.
Five male and one female axolotl larvae were collected by Jardin des Plantes at Paris in the year 1863. In the month of February, 1865 the axolotl larvae started breeding. The eggs laid by the female developed into full-fledged axolotls within a few months.
Attainment of reproductive faculty by these larvae led many to hold the adult nature of the larvae and they also considered them to be adults of some species of Urodele. But in the next autumn all were astonished to note that most of the axolotls lost their larval features and ultimately metamorphosed into adult terrestrial Ambystoma tigrinum.
The gills were lost, the gill-clefts became closed and the dorsal and tail fins disappeared during such metamorphosis. The remaining members of the same brood retained their aquatic larval stage. The transformation of several axolotls into Ambystoma established conclusively the larval nature of axolotls.
Besides, the metamorphosis of Siredon iichenoides into Ambystoma mavortium was observed by Marsh. Extensive experimentations have been done by Marie Von Chauvin, Koelliker, Camerans and many others. Several anurans and urodeles are known to become sexually mature in pre-adult stage and retain larval characters.
2. Types of Neoteny:
Kollmann (1882) classified neoteny into two categories, viz., Partial neoteny and Total neoteny.
i. Partial neoteny:
Partial neoteny involves the simple postponement of metamorphosis beyond the normal period. Retardation of metamorphosis may be due to temporary change in ecological condition or due to sudden physiological abnormality.
Wintering of the tadpdles of Pelobates fuscus, Pelodytes punctatus, Alytes obstetricans, Hyla arborea, Bufo vulgaris, Bufo viridis, Rana temporaria, Rana esculenta, Bombinator pachypus and many others furnish the typical examples of partial neoteny.
In Alytes the broods usually complete their development within autumn. But the larvae which hatched later in the months of July or August usually hibernate and retain their larval features up to the next autumn.
In Rana esculenta most of the larvae attain much larger size than the normal and remain in an under-developed stage, i.e., the hind limbs reach the budding stage, the head and the body attains a blotted and unhealthy look. Majority of the larvae remain in this sluggish stage for one or two years after which metamorphosis takes place.
ii. Total neoteny:
In this category the specimens become sexually mature at the larval stage but retain larval characters, like (i) external gills, (ii) tail-fin, (iii) ill-developed eyes, (iv) ill-developed fin on the back and (v) very weak limbs. Total neotenic animals are paedo-genic.
Because paedogenesis involves the capability of reproduction at the larval stage. In this case of total neoteny the sexually functional larvae cease to metamorphosis. In extreme cases of total neoteny (e.g., Necturus, Proteus, etc.) the larvae attain sexual maturity and they remain in that stage without undergoing metamorphosis.
Intermediate stages between partial and total neoteny are also recorded where the larvae become sexually functional and may metamorphose into adults with the advent of favourable conditions. The sexually mature axolotl larvae come under this category.
Total neoteny is seen in many urodele (e.g., Necturus, Amphiuma, Triturus vulgaris, Triton cristatus, Triton waltli, Ambystoma, Triturus alpestris, Siren, Proteus, etc.). The phenomenon of neoteny has been extensively studied in case of Ambystoma which, however, does not show an extreme case of neoteny. The axolotl larvae of Ambystoma can metamorphose into adult Ambystoma under favourable conditions.
Each axolotl larva possesses three pairs of delicate bushy external gills, four pairs of gill-slits, a flat long tail with prominent tail- fin and a dorsal fin merged with tail-fin. The axolotl larvae possess the power of regeneration. Chauvin has experimentally shown that both accidental and experimental damaging of the gill is followed by quick healing without affecting the process of metamorphosis.
The axolotl larvae become sexually mature when they attain the age of 6 months only. It has been recorded by Metzdorff that the sexually mature axolotls breed during December or April to June. The spermatopores deposited by the male members are drawn by the females into their cloacal chambers in the following night.
On the following day, each female axolotl collects a leaf of aquatic plant and pushes it against her vent. A few packets of eggs (each packet containing 6-10 eggs) are expelled violently into the surrounding water. Such violent expulsion of the eggs is caused by the twisting and turning of the body of the female.
About 30 eggs are normally laid at a time. After a rest for a considerable period, the female axolotls again start lying the eggs. The new-born larvae are hatched out within 15 days. The optimum temperature for the development of the eggs is 18-24°C. Bedriaga has recorded that the larvae at first feed on Daphnia, Infusoria, etc.
At the age of 6 months, the axolotls attain a length of 2.0-2.5 cm and become sexually mature to start breeding. At this stage, the axolotls take up Tubifex, scraped meat and may even scramble with the external gills of other fellows. The damaged gills, however, are quickly regenerated.
3. Factors for Neoteny:
The significance and cause of neoteny in Amphibians are not properly understood. Several extrinsic and intrinsic factors are considered to be responsible for such unusual phenomenon.
Extrinsic factors influencing neoteny:
Gadow (1901) advanced the idea that the cause of retention of larval features in axolotl is the abundance of food and other favourable requisites in aquatic life. Shufeldt holds that deep water and coldness inhibit thyroxine secretion which retards metamorphosis.
Drying up of swamps, lack of adequate food supply and rise in temperature in surrounding water induce metamorphosis. Weissmann again claimed that the retardation of metamorphosis of the axolotls is possibly due to the saline nature of the water of the lakes where they live.
In an investigation to establish the role of physical factors in neoteny, tadpoles were kept in water-holes with high vertical walls, so that they were not allowed to reach the land above the water-holes. It has been observed that this forced and prolonged use of larval gills and tails cause their further development, whereas the growth of limbs and other structures necessary for terrestrial life remained suspended.
Marie Von Chauvin in the University of Freeburg undertook similar experiments with axolotl larvae and also came to the above conclusion. It has further been observed that the axolotls which were not likely to metamorphose in normal habitat could be forced to metamorphose by slowly accustoming them to land-life.
Reverse phenomenon also happened in the life of axolotls. Partly metamorphosed axolotls accustomed to land-life could again the induced to return to larval life. All these experimental evidences emphasised the effect of physical factors on metamorphosis.
Huxley (1929) undertook an investigation on temperature-coefficient on metamorphosis. Several half-grown anuran tadpoles were cultured in variable temperatures ranging from 3-30°C for same span of time. But the culture solution has same concentration of thyroxine.
The larvae exposed to temperature range below 5°C could not complete their metamorphosis even when exposed to higher temperature. But the larvae exposed to higher temperature from the beginning completed metamorphosis very quickly.
Despite extensive researches on the role of extrinsic factors on metamorphosis, there is no sound reason to believe the exclusive role of the extrinsic factors. It is commonly observed that the neotenic as well as normal over-grown larvae occur side by side in the same habitat having similar environment.
So the existence of other factors besides the extrinsic factors becomes apparent. There are internal and physiological factors which control neoteny. But the extrinsic or environmental factors exert influence on the internal or intrinsic factors.
Intrinsic factors influencing neoteny:
Many experimental evidences have been advanced by different investigators. Zondeck and Leiter (1923) established that calcium delays metamorphosis in axolotls. Gressner (1928) also advanced that insulin hormone inhibits metamorphosis.
But recent researches incline to reveal that the metamorphosis is primarily influenced (i) by varying threshold levels of thyroxine and its analogs and (ii) by the degree of responsiveness of the larval tissue to hormones.
During early pre-metamorphic stage in amphibian development, the level of thyroxine (T4) is kept very low in the body by genetic mechanism. Etkin and his collaborators have also established the role of prolactin on metamorphosis.
They have shown that the level of prolactin which acts as an inhibitor in the overall control of metamorphosis remains high at this time. In the light of modern genetics it may be suggested that the structural genes guiding the synthesis of thyroxine are ‘switched off’ by some operator genes whereas the genes guiding the formation of prolactin are ‘switched on’.
In such condition the hypothalamus becomes sensitive to the available level of thyroid hormone in the blood stream. The neurosecretory apparatus of the hypothalamus produces a substance, called thyrotropin-releasing factor (TRF). TRF stimulates the anterior lobe of pituitary to produce thyroid-stimulating hormone (TSH) which in turn enhances the rate of thyroid secretion.
As the level of TSH rises during pro-metamorphosis, the level of prolactin suddenly falls. So the metamorphosis starts. The time of shift in hormone balance is possibly determined by the initiation of positive thyroid feed-back to the hypothalamus. Poor secretion of thyroid glands and the irresponsiveness of the larval tissues to the hormone are responsible for neoteny.
Kuhn (1925) studied the thyroid glands of neotenous larvae of the warty newt and observed that the alveoli which secrete thyroxine remain in undeveloped state (only about half the size of those in normal full- fledged specimens). He has further noted that the axolotls possessing normally developed thyroid glands failed to pour their secretion in the blood stream.
Transplantation of at least two more thyroid glands in addition to the normal glands causes the metamorphosis of axolotls. This result indicated that the thyroid gland of axolotls is able to produce one-third of the required quantity of thyroxine and that the larval tissues are only one-third responsive in contrast to normal specimens.
Bytenski and Saez have experimentally exchanged the pituitary gland between a salamander larva and an axolotl larva and found that axolotl’s pituitary gland is as efficient as that of salamander larva. But the tissues of axolotl failed to respond to the pituitary gland of the salamander. This indicates the irresponsive nature of axolotl’s tissues to hormones.
The investigations carried on by Etkin (1968) indicated that ‘spacing’ of events during metamorphosis depends on thyroxin-concentration, while the ‘sequence’ of events is inherent in the larval tissues. In amphibian development the tadpole larva undergoes progressive metamorphosis and transforms into an adult. This is a normal occurrence in amphibians.
But deviation from the normal pathway of development is found in the life-cycle of many urodeles. Such deviated pathway of development in axolotls due to extrinsic as well as intrinsic environmental factors may be regarded as ‘canalisation’, i.e., buffering of development against environmental change.
4. Genetics of Neoteny:
The role of thyroxine in urodele metamorphosis has been revealed by studies in genetics. The thyroid hormone binds to nuclear receptors that are in immediate contact with DNA. The hormone helps to change the transcription of genes that also influence to develop the larval characteristics to one, these gradually change into juvenile and adult characteristics.
But the exact role of genetics in paedomorphosis or neoteny has not clearly understood. However, a single gene hypothesis is thought to control the axolotl’s life cycle. 1: 1 Mendelian segregation results of paedomorph or metamorphic backcrosses between A. mexicanum and A. tigrinum.
If this theory is correct, then there are two alternate alleles at a major locus primarily responsible for determining the expression of metamorphosis or paedomorphosis.
5. Significance of Neoteny:
Neoteny is looked upon as a consequence of adaptation to neighbouring environments where retention of larval gills and other larval features may be advantageous.
Weissmann (1875) regarded neoteny as a case of reversion to atavistic ancestral conditions by assuming that all amphibia were originally gill-breathing aquatic creatures and that every feature seen in a larva represented a phylogenetic stage and the axolotl as such is a case of reversion to an ancestral stage.
External gills of urodeles have been evolved as an adaptation to aquatic life. The external gills actually developed first in the embryos as additional respiratory organs. The external gills were first initially restricted to embryonic life, which may be prolonged in aquatic larval life.
Possession of long external gills in the viviparous embryos of Salamandra altra supports the contention that the external gills are embryonic but not larval features. So existence of such gills in neotenous larvae is a secondary but not an atavistic feature. Besides external gills, the tail with tail-fin and epidermal sense organs of the neotenous larvae are secondary acquisitions rather than ancestral reminiscences.
G. K. Noble (1931) regarded that the retention of larval features during sexual maturity has nothing to do in the phylogeny of the amphibians. This is quite evident from the heterogeneous characters of the Perennibranchiata where all the neotenous species are included. Neoteny as such may have some importance in the individual groups.