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Shedding light: A phylotranscriptomic perspective illuminates the origin of photosymbiosis in marine bivalves
Jingchun Li
University of Colorado Boulder
Corresponding Author
ORCiD: https://orcid.org/0000-0001-7947-0950
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This work is licensed under a CC BY 4.0 License. Read Full License
Background: Photosymbiotic associations between metazoan hosts and photosynthetic dinoflagellates are crucial to the trophic and structural integrity of many marine ecosystems, including coral reefs. Although extensive efforts have been devoted to study the short-term ecological interactions between coral hosts and their symbionts, long-term evolutionary dynamics of photosymbiosis in many marine animals are not well understood. Within Bivalvia, the second largest class of mollusks, obligate photosymbiosis is found in two marine lineages: the giant clams (subfamily Tridacninae) and the heart cockles (subfamily Fraginae), both in the family Cardiidae. Morphologically, giant clams show relatively conservative shell forms whereas photosymbiotic fragines exhibit a diverse suite of anatomical adaptations including flattened shells, leafy mantle extensions, and lens-like microstructural structures. To date, the phylogenetic relationships between these two subfamilies remain poorly resolved, and it is unclear whether photosymbiosis in cardiids originated once or twice.
Results: In this study, we establish a backbone phylogeny for Cardiidae utilizing RNASeq-based transcriptomic data from Tridacninae, Fraginae, and other cardiids. A variety of phylogenomic approaches were used to infer the relationship between the two groups. Our analyses found conflicting gene signals and potential rapid divergence among the lineages. Overall, results support a sister group relationship between Tridacninae and Fraginae, which diverged during the Cretaceous. Although a sister group relationship is recovered, ancestral state reconstruction using maximum likelihood-based methods reveals two independent origins of photosymbiosis, one at the base of Tridacninae and the other within a symbiotic Fraginae clade.
Conclusions: The newly revealed common ancestry between Tridacninae and Fraginae brings a possibility that certain genetic, metabolic, and/or anatomical exadaptation existed in their last common ancestor, which promoted both lineages to independently establish photosymbiosis, possibly in response to the modern expansion of reef habitats.
Keywords
Photosymbiosis, Tridacinae, Fraginae, Symbiodiniaceae, Reef habitat
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This preprint is under consideration at BMC Ecology and Evolution. A preprint is a preliminary version of a manuscript that has not completed peer review at a journal. Research Square does not conduct peer review prior to posting preprints. The posting of a preprint on this server should not be interpreted as an endorsement of its validity or suitability for dissemination as established information or for guiding clinical practice.
Learn more about In Review
Research article
Shedding light: A phylotranscriptomic perspective illuminates the origin of photosymbiosis in marine bivalves
Jingchun Li
University of Colorado Boulder
Corresponding Author
ORCiD: https://orcid.org/0000-0001-7947-0950
Badges
Prescreen
This manuscript passed our Prescreen assessment
Complete author information
Appropriate declaration statements
Potential risks to human health
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Peer Review Timeline
CURRENT STATUS: Under Review
Version 4
Posted 15 Apr, 2020
No community comments so far
Editor assigned
On 13 Apr, 2020
Submission checks complete
On 12 Apr, 2020
Editor invited
On 12 Apr, 2020
No comments provided
Editorial decision: Minor revision
On 04 Apr, 2020
Editor assigned
On 09 Mar, 2020
Submission checks complete
On 08 Mar, 2020
Editor invited
On 08 Mar, 2020
No comments provided
Editorial decision: Minor revision
On 02 Mar, 2020
Reviewer #1 agreed
On 09 Feb, 2020
Review #1 received
Received 09 Feb, 2020
Editor assigned
On 06 Feb, 2020
Reviewers invited
Invitations sent on 06 Feb, 2020
Submission checks complete
On 05 Feb, 2020
Editor invited
On 05 Feb, 2020
No comments provided
Editorial decision: Major revision
On 20 Jan, 2020
Review #2 received
Received 25 Dec, 2019
Reviewer #2 agreed
On 23 Dec, 2019
Review #1 received
Received 22 Dec, 2019
Reviewer #1 agreed
On 21 Nov, 2019
Reviewers invited
Invitations sent on 18 Nov, 2019
Editor assigned
On 28 Oct, 2019
Submission checks complete
On 10 Oct, 2019
Editor invited
On 10 Oct, 2019
First submitted
On 25 Sep, 2019
Metrics
Comments: 0
PDF Downloads: ...
HTML Views: ...
License:
This work is licensed under a CC BY 4.0 License. Read Full License
Background: Photosymbiotic associations between metazoan hosts and photosynthetic dinoflagellates are crucial to the trophic and structural integrity of many marine ecosystems, including coral reefs. Although extensive efforts have been devoted to study the short-term ecological interactions between coral hosts and their symbionts, long-term evolutionary dynamics of photosymbiosis in many marine animals are not well understood. Within Bivalvia, the second largest class of mollusks, obligate photosymbiosis is found in two marine lineages: the giant clams (subfamily Tridacninae) and the heart cockles (subfamily Fraginae), both in the family Cardiidae. Morphologically, giant clams show relatively conservative shell forms whereas photosymbiotic fragines exhibit a diverse suite of anatomical adaptations including flattened shells, leafy mantle extensions, and lens-like microstructural structures. To date, the phylogenetic relationships between these two subfamilies remain poorly resolved, and it is unclear whether photosymbiosis in cardiids originated once or twice.
Results: In this study, we establish a backbone phylogeny for Cardiidae utilizing RNASeq-based transcriptomic data from Tridacninae, Fraginae, and other cardiids. A variety of phylogenomic approaches were used to infer the relationship between the two groups. Our analyses found conflicting gene signals and potential rapid divergence among the lineages. Overall, results support a sister group relationship between Tridacninae and Fraginae, which diverged during the Cretaceous. Although a sister group relationship is recovered, ancestral state reconstruction using maximum likelihood-based methods reveals two independent origins of photosymbiosis, one at the base of Tridacninae and the other within a symbiotic Fraginae clade.
Conclusions: The newly revealed common ancestry between Tridacninae and Fraginae brings a possibility that certain genetic, metabolic, and/or anatomical exadaptation existed in their last common ancestor, which promoted both lineages to independently establish photosymbiosis, possibly in response to the modern expansion of reef habitats.
Figure 1
Figure 2
Figure 3
Figure 4