Periodic Reporting for period 1 - META-MORPHOSIS (Metamorphosis as a driver of biodiversity? From a single genome to multiple phenomes)
Reporting period: 2021-09-01 to 2023-08-31
Metamorphosis is one of the most fascinating phenomena in animals, implying an abrupt change in morphology and ecology during the lifetime of an individual, transforming it from a larva into an adult (tadpoles to frogs or caterpillars to butterflies, for example). From insects to sea urchins, fishes, and frogs, most animals on our planet undergo metamorphosis. Life cycle complexity is consequently a widespread phenomenon and may be an important driver of biodiversity. Yet, the origin and evolution of different life-history stages and their impact on species diversification remain poorly understood. As species with complex life cycles have the genetic and developmental programs to change their morphology and allowing them to use different ecological niches during their lifetime, understanding whether and how life cycle complexity is a driver of biodiversity is critical. Consequently, it is of prime importance to understand how and why complex developmental strategies appeared and were maintained during evolution. The aim of my project is to understand why metamorphosis is so common in animals and whether it is an advantage for them to be able to produce different morphologies in comparison to animals that do not show metamorphosis (including mammals like us, for example). To do so, I use salamanders and newts as a model system as they display a tremendous diversity of species and ecologies, and show the largest variation in life cycle types among tetrapods.
The variety of developmental strategies and thus the differences in lifestyle and feeding modes should be reflected by changes in morphology during ontogeny in salamanders. In this project, I focused on different parts of the head as their morphology is impacted by changes in feeding strategy during ontogeny. I used interdisciplinary approaches combining functional morphology, developmental biology, and statistical modelling to disentangle the factors driving diversity at different ontogenetic stages in deep-time. More specifically, I addressed the following research objectives: 1) How do developmental strategies foster the patterns of morphological and functional variation among species throughout ontogeny? Here, I tested whether larval stages overlap in morphology and function with adults, and how this translates into morphological and functional variation. 2) Does the fossil record shed light on the origin and evolution of complex life cycles? For this part I aimed to explore morphofunctional variation in deep time and to assess if extinct species can be used in reconstructing the evolution of metamorphosis evolution in salamanders. 3) Does metamorphosis drive morpho-functional diversity and its impact on biodiversity? Here I aimed to test whether there is a decoupling within and/or between the different structures of the head and their function depending on life cycle.
The variety of developmental strategies and thus the differences in lifestyle and feeding modes should be reflected by changes in morphology during ontogeny in salamanders. In this project, I focused on different parts of the head as their morphology is impacted by changes in feeding strategy during ontogeny. I used interdisciplinary approaches combining functional morphology, developmental biology, and statistical modelling to disentangle the factors driving diversity at different ontogenetic stages in deep-time. More specifically, I addressed the following research objectives: 1) How do developmental strategies foster the patterns of morphological and functional variation among species throughout ontogeny? Here, I tested whether larval stages overlap in morphology and function with adults, and how this translates into morphological and functional variation. 2) Does the fossil record shed light on the origin and evolution of complex life cycles? For this part I aimed to explore morphofunctional variation in deep time and to assess if extinct species can be used in reconstructing the evolution of metamorphosis evolution in salamanders. 3) Does metamorphosis drive morpho-functional diversity and its impact on biodiversity? Here I aimed to test whether there is a decoupling within and/or between the different structures of the head and their function depending on life cycle.
I used an interdisciplinary approach combining morphological and functional analyses, development, and phylogenetic comparative methods in order to understand the impact of life cycle variation on morpho functional diversity in different ontogenetic stages (larvae and adults) across salamanders and newts. In this project, I investigated the patterns of morphological and functional variation using adults and larvae of salamanders with different life-history strategies (bi-phasic, direct-developing, and paedomorphic). To do so, I reviewed the literature on the kinematics of feeding and acquired new data on feeding for six species including different life-history stages (i.e. paedomorphic and metamorphosed) for some species. In addition, I performed morphological analyses of the head system using geometric morphometrics. I explored the patterns of morphological and functional variation using comparative analyses. My results show strong differences in morphology and feeding kinematics depending on life-history stage and life cycle. Interestingly, species that rarely metamorphose in the wild retained an aquatic motor program despite feeding on land. Finally, I found that larval stages do not share the same morphological space as adults for the lower jaw. The results of the morphological disparity analyses performed on the cranial shape across larval and adult stages in Caudata show that the morphological disparity is higher in adult than in larval stages. Interestingly, an opposite trend was found for the lower jaw. These results could suggest that metamorphosis constrains the lower jaw evolution in adults. I presented parts of this project at the SICB and SICB + international meeting in January 2022 and in several scientific seminars. I also disseminated the results of this project to different schools in several countries (France, Romania, Italy, Spain) via ‘Science is Wonderful’. As I obtained a permanent position in Switzerland, I was only working 9 months on this project and future studies and analyses need to be performed. This is what I plan to do on my ERC Starting grant that was transfer to Switzerland via SERI.
This project investigated the impact of life cycle variation on head diversity in salamanders and newts. Using an integrative approach combining state of the art phenomic methods, functional and phylogenetic comparative analyses, I was able to show that larval stages do not share the same morphological space for cranium but do so for the lower jaw. In addition, cranial morphology is more diverse in adults than in larvae, whereas the opposite trend is observed for the lower jaw. Finally, strong differences in feeding kinematics were found in adults depending on feeding medium. I demonstrate that species that rarely metamorphose in the wild retained an aquatic motor program despite feeding on land. These results are novel and open up new areas of research on how development may be fostering biodiversity. This is particularly important in the face of the sixth mass extinction where one-fifth of all living species are threatened. It is indeed crucial to identify whether life cycle complexity may allow organisms to cope with environmental change by producing significant morphological variation during their life span. Importantly, a large part of this endangered diversity remains hidden because it is represented by larval stages in species with complex life cycles. Such a project, taking into account all ontogenetic stages, will provide new insights into whether life cycle variation complexity plays a major role in shaping past, current, and future biodiversity.