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Metamorphosis is astonishingly common in the animal kingdom, but why this is the case is not really known.
By studying the skulls of salamanders in exquisite detail, a new study has shown that it could allow species greater flexibility to adapt to new environments.
Metamorphosis describes the process of juvenile animals changing dramatically as they mature into adults.
With up to 80% of insects and over half of all vertebrates undergoing metamorphosis, most animal species experience some form of this process during their lifetime.
But it is a complex undertaking. Habitat and diet are often different for the young and for adults, and body plans and bones dramatically reorganise during the transition. So why is it so common?
To understand this, researchers at the Museum have been exploring the evolution and shape diversity found in salamander skulls.
Dr Anne-Claire Fabre lead author of a paper published in Nature Ecology and Evolution.
'The benefits of metamorphosis are not obvious at first sight,' added Anne-Claire. 'It is a really risky period in an animal's life where the young are super vulnerable, exposed to predation and stresses.
'But there are obviously advantages, the young do not have to share their resources with the adults, thus there is less competition for food for example and this may favor population growth.'
To answer this, the team has been scanning the skulls of living salamanders, and then comparing their changes in skull shape over the group's 180-million-year history. This has shown that the ability to metamorphose has allowed salamanders to evolve their impressive diversity.
'I think it's interesting because metamorphosis is a super complex life cycle,' explains Prof Anjali Goswami, who is the senior author of the paper. 'Why would something that requires an animal to have two completely different phases of life and different adaptive pressures be sustained, and why is it so common in the animal kingdom?'
Even though there are only around 700 salamander species, they have evolved a whole range of different life cycles.
In general, they undergo metamorphosis like most amphibians. An adult lays fertilised eggs in water, which then hatch into a larval form, similar to the tadpoles of frogs. These free-living larvae swim around feeding themselves until they are ready to metamorphose, at which point they radically change their appearance and alter their body plan as they develop into their adult form.
There is, however, a lot of variation in this lifecycle among salamanders. Some species, such as fire salamanders, retain the eggs and give birth to live larvae, while others such as tropical climbing salamanders will lay their eggs on land.
There are species that have even got rid of some of the individual stages of metamorphosis. The axolotl, for example, remains in its juvenile larval stage and never matures to an adult, while some species skip the larval stage altogether and develop directly into adults.
'You see the repeated evolution of species which lose some of these metamorphic stages, while in others there is a re-emergence as species re-evolve them,' says Anjali. 'So there is huge variation in lifecycle evolution that you don't see in other groups.
'We were wanting to figure out whether those frequent shifts in lifecycles have an impact on salamander evolution and what is it about these animals that allow them to do it.'
Anne-Claire, Anjali and their colleagues used CT and surface scans to reconstruct the skulls from across every genus of salamander. They compared over 1,000 separate points on these skulls to track how they have changed over time between the genera.
They found that it is precisely this ability to change their body plan between juvenile and adult stages that has, over the past 180 million years, allowed salamanders to diversify into a huge variety of forms.
'Animals that are metamorphosing have this greater independence in individual parts of their skull,' explains Anjali. 'These species can then evolve a greater variety of forms, but it also means that they can specialise different parts of the skulls for different functions more easily than if all the individual parts of the skull were evolving in step.
'This might be why metamorphosis is such a good strategy for species, as maybe being metamorphic means you are a more evolutionarily flexible creature.'
This could explain why the majority of animals undergo metamorphosis at some point in their life.
'We are currently in a sixth mass extinction event and amphibians are among the hardest hit,' explains Anne-Claire. 'It is really important to understand whether development can be a driver of diversity and whether this may be a benefit for animals, allowing them to adapt rapidly to changing environments.
'Going forward, this will be a key question for my research programme.'
The work on salamanders is feeding into a much larger project looking at the evolution of skulls across all groups of land vertebrates. This has already included published studies on birds, caecilians, snakes and lizards, with those looking at frogs, mammals, turtles, dinosaurs and crocodiles in the works.
All the skull scans already published are now freely available to look at and download on the Phenome10k project website.
The overall goal of this larger-scale project is similar to what they have been analysing within the individual groups.
'We're taking these scans and using evolutionary trees to look at when there have been changes in the rates of skull evolution through time,' explains Anjali. 'There are periods in time where there are really fast rates of skull evolution, and we want to know whether these fast rates are associated with things such as changes in life history, diet, climate or extinction events.'
Not only that, but these reconstructions can even allow the team to peer tentatively back into the deep past.
Anjali continues, 'As we can reconstruct how the skull has evolved, we can also build a picture of the hypothetical ancestors to these major groups, and use that to figure out what the ecology of these ancestors may have been.'
For salamanders it seems that the first species were likely terrestrial animals with aquatic larvae underwent metamorphosis between two stages.
This project will be the most detailed analysis of skull shape and evolution that has even been conducted, and should help answer some of the most fundamental questions about the evolution of all land animals.