Unravelling the developmental origins of parallel evolution

Project Information

EvoOnRepeat

Grant agreement ID: 948126

DOI

10.3030/948126

EC signature date 18 November 2020

Start date 1 March 2021

End date 28 February 2027

Funded under

• EXCELLENT SCIENCE - European Research Council (ERC)

Total cost

€ 1 498 198,88

EU contribution

€ 1 498 198,88

Coordinated by

MAX-PLANCK-GESELLSCHAFT ZUR FORDERUNG DER WISSENSCHAFTEN EV
Germany

Periodic Reporting for period 3 - EvoOnRepeat (Unravelling the developmental origins of parallel evolution)

Reporting period: 2024-03-01 to 2024-05-31

Summary of the context and overall objectives of the project

A classic problem in evolutionary biology is to understand why evolution is often on repeat. Despite that the diversity of life may seem endless, a closer look reveals that some trait combinations evolve over and over again, resulting in parallel evolution. A possible explanation is that development produces some phenotypes readily and frequently, while others are rare or impossible. The ERC Starting Grant EvoOnRepeat is putting the role of development in evolution to the test by studying Mediterranean wall lizards. Several species of wall lizards have independently evolved a complex syndrome, including striking coloration, stout bodies, large heads and aggressive behavior. All these traits share a developmental origin in the same cell type, neural crest cells, and this project is testing whether this developmental coupling allows seemingly unrelated traits (coloration, morphology and behavior) to co-vary and co-evolve.
The overall objectives are to quantitatively assess patterns of parallel evolution across the diversification of Mediterranean wall lizards, and test if neural crest cell biology has facilitated the repeated evolution of the syndrome. Specifically, the objectives are to (1) reveal if independent origins of the syndrome share the same transcriptional and epigenetic modifications of neural crest cells, (2) identify how parallelism at the phenotypic level is mirrored at the genomic level and (3) validate the results using gene editing.
The societal value of this project lies in generating a deeper understanding of the evolutionary process. Our insights are expected to demonstrate that deciphering the developmental rules that build organisms will make evolution more predictable. Failure to attend to the ‘Arrival of the fittest’ has left us poorly equipped to predict how invasive species evolve, or if species will adapt to environmental challenges. This project aims to fill this explanatory gap by showing that it is possible to understand the rules by which individuals vary, and use this knowledge to explain why evolution proceeds some ways rather than others.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

The three objectives outlined above map onto three independent work packages that have distinct methodologies, challenges and objectives. WP1 (comparative developmental biology) uses sophisticated cell sorting combined with transcriptome and methylome analyses to reveal if independent origins of the syndrome share the same modifications of NCCs. WP2 (evolutionary genomics) applies exhaustive genome sequencing across the entire Podarcis genus to establish how the parallelism at the phenotypic level is mirrored at the genomic level. WP3 (experimental developmental biology) includes gene editing to target a mechanistic dissection of developmental pathways and a reconstruction of the likely evolutionary steps at the origin of the syndrome.
During the first 30 month of the project, the team working with the EvoOnRepeat project has achieved several milestones. Regarding WP1, the establishment of a novel methodology that allows sorting of neural crest cells in wall lizard embryos was identified as a high-risk element, but most obstacles have been overcome thanks to our dedicated efforts towards this methodological innovation. For three consecutive years, my team has collected a large number of lizards eggs (> 500 per year) and collaborated with a biomedical center and the eukaryotic single cell genomics center (both in Sweden), to improve and fine-tune the methodology. Thanks to these achievements, we are now in a position to launch the main experiment, which will inform us on differences in the transcriptomic state of neural crest cells in lizard lineages with and without the syndrome phenotype. Similarly, WP2 has proceeded largely according to our initial plans. A core element of WP2 is the sampling of lizards in the wild. Despite that the first field season (2021) could not be conducted as planned due to Covid19-related travel restrictions, we have conducted two highly successful field expeditions in 2022 and 2023. We have successfully sampled eight wall lizard species, and thanks to our newly developed phenotyping protocol, we have collected highly informative multivariate data at an unprecedented resolution. Analyses of phenotypic and genomic data are currently ongoing, and one major publication is currently under review. Regarding WP3, initial failure to recruit a suitable postdoc has paused this part of the project. However, a new attempt to attract a suitable co-worker are currently underway.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

At this time point, most elements of the EvoOnRepeat project are ongoing and it is therefore challenging to forecast what the final results may be, and what progress beyond the state of the art these might entail. What follows is a projection based on the insights gained so far and a realistic scenario for the second half of the project.
Given that we have solved most methodological challenges associated with the enrichment of neural crest cells from wall lizard embryos, I anticipate that we will be able to definitely answer whether neural crest cells are indeed associated with the repeated evolution of the syndrome in wall lizards. An in-depth analysis of the genomic basis of the syndrome in a wall lizard species (Podarcis muralis) shows evidence for neural crest cell regulators as being highly differentiated between syndrome- and non-syndrome lizards. I take this as strong support for the role of neural crest cells in coupling seemingly unrelated traits and thus facilitating those traits to co-vary and co-evolve. While this result is at present suggestive only, the EvoOnRepeat project will deliver more results in the next 30 month that will allow us to confidently answer this question.
Regardless of whether we find support for the idea that developmental linkage through neural crest cells facilitates parallel evolution or not, I expect this project to deliver insights that allow us to better understand the factors that confer evolvability on living systems. Our preliminary results show great variation between different wall lizard lineages in terms of their propensity to diversify, and this research program will allow us to identify the developmental and genomic features that explain this variation. Taken together, no matter what the exact results of the next 30 month will reveal, I envision that this project will pave the way for future research programs that aim to decipher the generative processes that guide evolutionary outcomes. I expect this EvoOnRepeat project to set a leading example of how opening the black box of development has the power to make seemingly idiosyncratic quirks of evolution understandable and even predictable.

Examples of the extreme phenotypes in the common wall lizard Podarcis muralis.

Field work sampling Podarcis gaigeae on an islet outside of Skyros.