Stability in flexibility: Shifting alliances stabilize the symbioses of marine animals over 150 million years
5 affiliations
- 1Max Planck Institute for Marine Microbiology, Bremen, Germany
- 2North Carolina State University, Department of Plant and Microbial Biology, Raleigh, North Carolina, USA
- 3University of Gothenburg, Department of Biological and Environmental Sciences, Gothenborg, Sweden
- 4Deparment of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, California, USA
- 5University of Vienna, Department of Microbiology and Ecosystem Science, Vienna, Austria
Abstract
Multipartite symbioses, which involve intimate interactions among three or more species, have evolved independently numerous times in convergent evolution, and enable functional complexity and ecological flexibility. How stability is maintained in such relationships remains, however, poorly understood, and can only be fully understood by integrating processes across both micro- and macroevolutionary scales. In this study, we bridge these scales by examining the symbiotic communities of gutless marine oligochaetes - annelid worms that have become obligately dependent on their bacterial partners for nutrition and waste removal over the past 150 million years. Using metagenomic sequencing of 231 individuals from 63 host species, collected across 17 marine environments worldwide, we reconstructed host and symbiont phylogenies to investigate the composition, specificity, and evolutionary history of their symbiotic communities from the strain to genus level. Our results show that each gutless oligochaete harbors up to 10 symbiont species drawn from a restricted pool of 33 marine bacterial genera. Community composition was strongly shaped by host species at 90% explanatory power, and much less by geography or environment. Symbiont communities were highly stable within host species but shifted rapidly at short macroevolutionary scales as host species diverged. Ancestral state reconstructions revealed that the primary symbiont, Candidatus Thiosymbion, was an early and persistent acquisition, while secondary symbionts were gained multiple times through convergent evolution, enhancing the diversity and metabolic flexibility of the symbiotic communities. By linking fine-scale microevolutionary dynamics with broader macroevolutionary patterns, our study reveals how gutless oligochaetes achieve both stability and flexibility in their symbiotic partnerships - enabling long-term host dependency while driving innovation and adaptation. This evolutionary trajectory may underpin the ecological success and diversification of gutless oligochaetes in marine sediments, and may help explain the repeated emergence and persistence of other multipartite associations.
Related
- Plant–cyanobacterial symbioses: mutualism with emerging translational possibilities
- Cell-cycle dynamics in cnidarian-dinoflagellate symbioses
- An eco-evolutionary consumer-resource theory of host-microbe symbioses
- Gene Regulatory Network Reconstruction to Decipher the Molecular Mechanisms Governing Bacteriocyte-Based Symbioses
- Questioning the evidence for host–symbiont codiversification in mycorrhizal symbioses
BibTeX
@article{mankowski2026stability,
title = {{Stability in flexibility: Shifting alliances stabilize the symbioses of marine animals over 150 million years}},
author = {Anna Mankowski and Manuel Kleiner and Christer Erséus and Nikolaus Leisch and Yui Sato and Jean‐Marie Volland and Bruno Hüettel and Cecilia Wentrup and Tanja Woyke and Juliane Wippler and Nicole Dubilier and Harald R. Gruber‐Vodicka},
journal = {Science Advances},
year = {2026},
month = sep,
doi = {10.1126/sciadv.aed1476},
url = {https://www.science.org/doi/10.1126/sciadv.aed1476},
note = {CC BY-NC},
}
RIS
TY - JOUR
TI - Stability in flexibility: Shifting alliances stabilize the symbioses of marine animals over 150 million years
AU - Anna Mankowski
AU - Manuel Kleiner
AU - Christer Erséus
AU - Nikolaus Leisch
AU - Yui Sato
AU - Jean‐Marie Volland
AU - Bruno Hüettel
AU - Cecilia Wentrup
AU - Tanja Woyke
AU - Juliane Wippler
AU - Nicole Dubilier
AU - Harald R. Gruber‐Vodicka
PY - 2026
DA - 2026/09/30
JO - Science Advances
DO - 10.1126/sciadv.aed1476
UR - https://www.science.org/doi/10.1126/sciadv.aed1476
AB - Multipartite symbioses, which involve intimate interactions among three or more species, have evolved independently numerous times in convergent evolution, and enable functional complexity and ecological flexibility. How stability is maintained in such relationships remains, however, poorly understood, and can only be fully understood by integrating processes across both micro- and macroevolutionary scales. In this study, we bridge these scales by examining the symbiotic communities of gutless marine oligochaetes - annelid worms that have become obligately dependent on their bacterial partners for nutrition and waste removal over the past 150 million years. Using metagenomic sequencing of 231 individuals from 63 host species, collected across 17 marine environments worldwide, we reconstructed host and symbiont phylogenies to investigate the composition, specificity, and evolutionary history of their symbiotic communities from the strain to genus level. Our results show that each gutless oligochaete harbors up to 10 symbiont species drawn from a restricted pool of 33 marine bacterial genera. Community composition was strongly shaped by host species at 90% explanatory power, and much less by geography or environment. Symbiont communities were highly stable within host species but shifted rapidly at short macroevolutionary scales as host species diverged. Ancestral state reconstructions revealed that the primary symbiont, Candidatus Thiosymbion, was an early and persistent acquisition, while secondary symbionts were gained multiple times through convergent evolution, enhancing the diversity and metabolic flexibility of the symbiotic communities. By linking fine-scale microevolutionary dynamics with broader macroevolutionary patterns, our study reveals how gutless oligochaetes achieve both stability and flexibility in their symbiotic partnerships - enabling long-term host dependency while driving innovation and adaptation. This evolutionary trajectory may underpin the ecological success and diversification of gutless oligochaetes in marine sediments, and may help explain the repeated emergence and persistence of other multipartite associations.
SN - 2375-2548
ER -