Newts that never grow up – paedomorphosis in salamanders
The majority of pond-breeding salamanders have a biphasic metamorphic life cycle where free-swimming larvae living in ponds and other water bodies metamorphose into terrestrial living adults. The advantage of this life history is that it allows adults to exploit different habitats to larvae, utilise a wider range of ecological niches and escape from potentially hostile environments e.g. a desiccating pond. However, a number of salamander species within Europe and North America have evolved a unique life history where free-swimming larvae to do not metamorphose into terrestrial living adults, but remain within the water and retain larval characteristics. Known as paedomorphosis these individuals develop into sexually reproductive adults but retain larval traits e.g. free-swimming larval form (Figure 1). It appears that the phenomenon of paedomorphosis has evolved several times within salamanders and has been of great interest to biologists for centuries. One theory suggests that paedomorphosis is most likely to evolve when environmental conditions experienced by adults are inhospitable relative to conditions experienced by larvae. For example, if water bodies remain constant throughout the year but temperature regimes and environmental factors on the land are hostile, such as in mountainous regions, arid landscapes or nutrient poor regions, it may be more favourable to remain in the larval form. Within southern Europe, paedomorphic populations often occur in deep, permanent and cool alpine lakes, where the terrestrial habitat has poor nutrient availability (Denoël et al., 2005). In an attempt to resolve many questions relating to the evolution of paedomorphosis in salamanders Bonnett et al. (2014) examined DNA sequences of a sub-family of plethodontid salamanders from North America. The authors concluded that within this group, paedomorphosis is more likely to occur in species dwelling in caves and those occurring in more arid climates. Here there are more resources in water bodies than in terrestrial habitats. An interesting finding of this study is that paedomorphosis has evolved and re-evolved serval times in the same species. The Valdina Farms Salamander (Eurycea troglodytes), from the western Edward Plateau, Texas, existed in a paedomorphic form 22 million years ago, before evolving into a metamorphic form (i.e. larvae metamorphosed into terrestrial adults). Subsequently, several million years later, it re-evolved back into a paedomorphic form (Bonnett et al., 2014). This is likely to be due to changing environmental conditions over this time period. However, there is a cost to being paedomorphic. Bonnett et al. (2014) found that paedomorphic spelerpine plethodontids from eastern North America have significantly smaller geographic range sizes than metamorphosing species and have not dispersed between biogeographic regions. This has resulted in these species being more at risk from environmental events or human disturbance than species with wider geographic ranges and as a result have a higher rate of extinction.
In some populations of salamanders, individuals exhibit facultative paedomorphosis, i.e. when both metamorphic and paedomorphic forms coexist and the occurrence of the latter within a given population depends on the advantages of living in the aquatic and terrestrial habitats. Whether an individual is metamorphic or paedomorphic may depend on a range of environmental factors including temperature, pond desiccation rate, terrestrial aridity and resource availability. Facultative paedomorphosis is an adaptive strategy which has been reported from several European newts. For example, great crested newt (Triturus cristatus), palmate newt (Lissotriton helveticus), alpine newt (Ichthyosaura alpestris) and southern banded newt (Omatotriton vittatus) all exhibit paedomorphosis, especially in the south of their range (Oromi et al., 2014). Facultative paedomorphosis has been regularly observed in populations of the smooth newt (L. vulgaris), particularly those in southern and eastern Europe (Figure 2). In this species, the key environmental factors are prey and predator abundance and habitat composition, with paedomorphosis generally occurring in areas with permanent, nutrient-rich water bodies without predators (Bozkurt et al., 2015). When fish are introduced to water bodies, paedomorphosis generally disappears since the aquatic environment becomes a less favourable habitat (Denoël et al., 2005).
In 2017, Mathiron et al. (2017) tested theories in relation to how climatic factors impact on paedomorphosis in facultative populations of the palmate newt (L. helveticus) living in the Department of Hérault, France. The authors found that temperature and water availability each play a significant role in metamorphosis and explain the persistence of paedomorphosis in certain populations. These results have major implications as they show that droughts through evolutionary history have been a primary factor in promoting the evolution of paedomorphosis in this species. When terrestrial environments experience persistent drought, this has promoted the evolution of paedomorphic populations. This has significance in relation to a warming climate where the occurrence of severe droughts in Mediterranean parts of this species’ range, may result in an increase in paedomorphic populations in the near future. Mathiron et al. (2017) also found a sex-biased effect highlighting the role of sex in the metamorphosis of paedomorphs. Both water level and temperature affected the metamorphosis of males more than females. More metamorphic males occurred than females and, in drying conditions, started metamorphosis earlier than did females, which resulted in a female biased sex-ratio of paedomorphs. The reason why males metamorphose more than do females may be due to differences in levels of hormones in males compared to females. Also, males tend to disperse more than females so being metamorphic and turning into terrestrial adults would allow them to seek new water bodies and promote gene flow between populations.
Bonnett, R.M., Steffen, M.A., Lambert, S.M., Wiens, J.J. & Chippindale, P.T. (2014) Evolution of paedomorphosis in plethodontid salamanders: ecological correlates and re-evolution of metamorphosis. Evolution 68 (2): 466–482.
Bozkurt, E., Olgun, K. & Wielstra, B. (2015) First record of facultative paedomorphism in the Kosswig’s newt Lissotriton (vulgaris) kosswigi (Freytag, 1955) (Urodela; Salamandridae), endemic to northwestern Turkey. Turkish Journal of Zoology, 39: 976-980.
Denoël, M., Joly, P. & Whiteman, H.H. (2005) Evolutionary ecology of facultative paedomorphosis in newts and salamanders. Biological Reviews, 80: 663–671.
Mathiron, A.G.E., Lena, J., Baouch, S. & Denoël, M. (2017) The ‘male escape hypothesis’: sex-biased metamorphosis in response to climatic drivers in a facultatively paedomorphic amphibian. Proceedings of the Royal Society B: Biological Sciences, 284 (1853):
Oromi, N., Amat, F., Sanuy, D. & Carranza, S. (2014) Life history trait differences between a lake and a stream-dwelling population of the Pyrenean brook newt (Calotriton asper). Amphibia-Reptilia, DOI:10.1163/15685381-00002921.