Marine annelids as a model for disentangling the molecular basis underlying the evolution of reproductive strategies and reproductive timing

Project Information

MOM-OR-DAD

Grant agreement ID: 101109842

DOI

10.3030/101109842

Project closed

EC signature date 4 May 2023

Start date 2 April 2024

End date 1 April 2026

Funded under

• Marie Skłodowska-Curie Actions (MSCA)

Total cost

No data

EU contribution

€ 188 590,08

Coordinated by

UNIVERSITA DEGLI STUDI DI PADOVA
Italy

Periodic Reporting for period 1 - MOM-OR-DAD (Marine annelids as a model for disentangling the molecular basis underlying the evolution of reproductive strategies and reproductive timing)

Reporting period: 2024-04-02 to 2026-04-01

Summary of the context and overall objectives of the project

The overarching goal of the project is to provide ground-breaking insights into how animal molecular machinery is rewired to generate novel and adaptive combinations of reproductive traits. By combining expertise in animal reproductive dynamics with proficiency in molecular biology and comparative transcriptomics, the project pursued two main specific objectives. The first objective was to dissect the molecular basis of drastically divergent reproductive strategies in the closely related marine species Platynereis dumerilii and P. massiliensis. The second objective, taking advantage of the same models, was to decode the molecular basis of lunar reproductive periodicity. This project addresses fundamental unresolved questions in Evolutionary biology, Marine biology, and Chronobiology. Because annelid genomes retain key genes for both vertebrate and arthropod development/reproduction, that have been lost in other bilaterian clades, this project provides crucial insights into how reproductive machinery evolved in major animal lineages. Furthermore, the project addresses the pressing need to unravel the elusive molecular nature of lunar reproductive timing and circalunar clocks. These are key mechanisms particularly in marine environments that are currently threatened by light pollution and climate change.

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

During the first year, robust laboratory culturing conditions for the target marine bristleworms were established, and a targeted field sampling campaign was successfully completed to collect the specimens necessary to sustain the experimental design. An extensive sampling effort covered seven critical developmental transitions for both target species, yielding four to six biological replicates per stage. High quality RNA was extracted from 158 distinct samples for RNA sequencing. Bioinformatic analyses are actively identifying differentially expressed genes to generate transcriptional profiles that describe species-specific developmental trajectories and to identify the complex transcriptional changes underlying their divergent developmental and reproductive dynamics (WP1). These findings are currently in preparation for publication in peer reviewed journals. In the second year, the project deployed a state-of-the-art naturalistic environmental light intensity system. This allowed the simulation of sunlight and moonlight spectra, including intensity changes associated with the rotation of the Earth and the revolution of the Moon, exactly as perceived at about 5 meters below the sea surface. Using these advanced environmental simulations, the project successfully mapped the behavioral responses (reproductive rhythms) of both species to naturalistic moonlight, and is currently in the process of unveiling the underlying molecular dynamics. For this, the project established a highly detailed temporal sampling over the course of multiple lunar cycles to reveal and profile how these two species process lunar cues, findings that are currently in preparation for publication in peer reviewed journals. To achieve this, tissues were sampled at high resolution every three to four days across fully entrained lunar months and lunar free-running months to discriminate between environment driven and endogenous driven molecular dynamics. Additionally, a global network of collaborators was established to collect fixed specimens worldwide. The project extracted, sequenced, and molecularly identified about 700 DNA barcoding sequences to resolve population structure and update the phylogeny of the genus. In terms of exploitation and dissemination, the project actively engaged the general public through outreach events featuring custom designed educational board games to enhance social knowledge on evolution and marine biodiversity. Scientifically, molecular and morphological datasets will be made openly accessible, and the findings will be disseminated through international conferences.

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 project achieved/is achieving results significantly beyond the state of the art by successfully deploying a powerful and previously unexploited comparative strategy to study diverging developmental/reproductive trajectories and lunar reproductive timing. While environmental simulation systems have been used previously with simple rectangular on/off light profiles, this project was the first (to our knowledge) to successfully mimic the complex light changes associated with natural planetary movements to strictly entrain marine organisms in the laboratory for advanced molecular profiling.
The socioeconomic impact of these results is substantial. By identifying key molecular dynamics for sexual development and reproductive timing, the project establishes crucial baselines for understanding processes that are highly vulnerable to light pollution and endocrine disruption. This knowledge directly contributes to improving current strategies for marine biodiversity preservation. Furthermore, the findings potentially hold broader translational relevance and societal interest for human physiology, as the lunar cycle affects human behavior, sleep, and menstrual periodicity.
Economically, the progress made in culturing and sampling validates these marine bristleworms as highly accessible and cost-effective laboratory models. They feature high regeneration potential and easy sex staging. Thus, the project proves they can serve as practical and economic valuable alternatives to more challenging and economically relevant species, such as farmed fish or corals, for studying sequential hermaphroditism and lunar regulated spawning.