Keys to evolutionary success: untangling drivers of hyperdiversification

Project Information

HYPERDIVERSE

Grant agreement ID: 865101

DOI

10.3030/865101

Project closed

EC signature date 19 March 2020

Start date 1 October 2020

End date 31 March 2026

Funded under

• EXCELLENT SCIENCE - European Research Council (ERC)

Total cost

€ 1 949 788,00

EU contribution

€ 1 949 788,00

Coordinated by

MUSEUM NATIONAL D'HISTOIRE NATURELLE
France

Periodic Reporting for period 3 - HYPERDIVERSE (Keys to evolutionary success: untangling drivers of hyperdiversification)

Reporting period: 2023-10-01 to 2025-03-31

Summary of the context and overall objectives of the project

Explaining why some taxa are more diversified than their closest relatives remains one of the major challenges in evolutionary biology. However, much of Earth’s biodiversity is concentrated in few diverse non-vertebrate animal lineages, whose analysis of diversification dynamics is hampered by the lack of empirical data.
The HYPERDIVERSE project will focus on one hyperdiverse and poorly-known taxon of molluscs, the marine predators Neogastropoda. Their high species diversity (>15,000 species), largely undescribed, and the key innovations they evolved, linked to their feeding habits and dispersal abilities, make them a perfect model system to test hypotheses related to the diversification of hyperdiverse taxa. The first objective of the project will be to reconstruct a robust, precise and complete phylogeny of the group by using cutting-edge omic technologies.
The second goal will be to test correlations between two traits – the exogenome diversity as proxy of feeding habits, and the type of larval development as a proxy of dispersal capabilities, which are keys for understanding diversification dynamics, using genomic, transcriptomic and proteomic approaches.
The same data will also be used to fulfil the last objective: identifying the genetic determinants of the two traits, the molecular mechanisms at the origin of their diversity, and the processes by which these traits interact with the environment to mediate the diversification of the neogastropods. The major breakthrough of the project will thus rely on the joint analysis of the correlation between traits and diversification and of the causal factors at the origin of this correlation. Furthermore, the project will also impact other fields of research, with the production of unique data on many culturally, economically and scientifically important species, including the first complete genomes for the group, and the characterization of numerous compounds potentially promising in human therapeutics and biotechnologies.

This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement No 865101). It is hosted by the MNHN, Paris, France.

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

One of the main challenges of the project is its interdisciplinary nature. The project is organized in work packages, all of them interconnected, and link to different approaches and methodologies.
The first axis of the project concerns the revision of the alpha-taxonomy and phylogeny of the neogastropods. It relies primarily on the MNHN collections: at the middle of the project, the first objective (40000 specimens registered in the “DNA” collection of the MNHN) is already achieved, with 41080 specimens. Most of them (c.a. 90%) are now photographed, and with the recent barcoding of more than 10000 additional samples, c.a.60% of them are sequenced. Thanks to the organization of taxonomic workshops and the development of the Hyperdiverse platform (http://www.hyperdiverseproject.com/platform) a tool to collectively propose identifications for the MNHN specimens, we re-identified c.a.7000 specimens. This step also led to the identification of c.a.250 putative new species, and our international network of taxonomists is involved to describe them.
Identifying the MNHN specimens was mandatory to build a dataset representative of the genus-level diversity of the neogastropods. A total of 725 specimens, representing as many genera, has been sequenced using an exon-capture approach to reconstruct a robust phylogeny of the neogastropods.
The second axis of the project aims at identifying the molecular processes that would explain the hyperdiversification of the neogastropods. Two chromosom-level genomes have been produced, and they confirmed that all the neogastropods experienced a whole-genome duplication event, followed by the apparition of new genes, including toxin-coding genes, that would, at least partly, explain their evolutionary success. This study is complemented by the sequencing of transcriptomes of venom-producing glands: 100 transcriptomes have been sequenced so far, and they revealed an unexpected diversity of toxins produced by the neogastropods.

These results have been published in several articles (see http://www.hyperdiverseproject.com/news for more details), and three members of the ERC teams presented the project results at the World Congress of Malacology in August 2022.

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)

The taxonomic workflow proposed in the project is innovative and probably constitute a very efficient way to speed up the species description process and the reconstruction of robust and as complete as possible phylogenies. Hyperdiverse and mostly unknown groups such as the neogastropods are difficult to tackle with traditional approaches and strategies, and the combination of intensive DNA barcoding of all the available material, taxonomic workshops with international experts, use of the Hyperdiverse platform and application of the exon-capture approach was very efficient to quickly identify new taxa and resolve long-standing phylogenetic issues. We aim at continuing this strategy until the end of the project, in order to tackle the other groups of neogastropods, describe as many as possible new species, and complete the neogastropod phylogeny.
This systematic framework is mandatory to test the hypotheses related to the evolutionary success of the neogastropods. It provides the evolutionary framework in which the hypotheses related to the variability in genome and transcriptome composition can be tested. In the second part of the project, we will continue to produce genomic and transcriptomic data, first to confirm the hypotheses tested during the first part of the project (impact of the whole genome duplication on neogastropod diversification, presence of toxins in all the lineages of the neogastropod), but also to test new hypotheses related to the processes linked to the apparition and diversification of the toxin-coding genes, and to the diversification of these toxins in the different lineages of neogastropods. However, producing such data remain challenging for non-model organisms, and the second part of the project will focus on the toxin diversity, leaving aside the second hypothesis that we planned to tackle during the project (impact of larval development on diversification). In this context, recent progresses, in particular in the framework of the Hyperdiverse project, makes it feasible to clarify the evolution patterns and processes at the origin of the diversification of the group.

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