Shedding light: a phylotranscriptomic perspective illuminates the origin of photosymbiosis in marine bivalves

Abstract

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, longterm 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 exaptations existed in their last common ancestor, which promoted both lineages to independently establish photosymbiosis, possibly in response to the modern expansion of reef habitats.

Untangling the diversity and evolution of tentacles in scallops, oysters, and their relatives (Bivalvia: Pteriomorphia)

“…These findings add to the increasing body of evidence showing evolutionary convergences as common phenotypic outcomes among bivalves, as demonstrated for lifestyles (Morton 1990;Alejandrino et al 2011;Audino et al 2019), shell shape (Stanley 1970;Owada 2007;Serb et al 2017), chemosymbiosis (Taylor and Glover 2010), and photosymbiosis (Li et al 2020).…”

Insights into the species evolution of Calanus copepods in the northern seas revealed by de novo transcriptome sequencing

“…Recent studies have validated the use of transcriptomes in phylogenetic analyses, showing virtually identical results with phylogenies derived from whole or partial genome, regardless of the tissue origin and whether the same tissue was used across species (Cheon et al, 2020 ; Zhao et al, 2021 ). Multiple studies have already used transcriptomics for phylogenetics of various marine organisms, including dinoflagellates (Annenkova et al, 2018 ), pteropods (Peijnenburg et al, 2020 ), bivalves (Li et al, 2020 ), and crustaceans (Gan et al, 2020 ).…”

Grand Challenges in Coevolution

“…Chlorella-bearing ciliates, foraminifera, mixotrophic testate amoebae) (Hallock, 1999;Proeschold et al, 2011;Gomaa et al, 2014), and animals (e.g., reef-building corals, viridissima group of Hydra) (Stanley, 2006;Kawaida et al, 2013;van Oppen and Medina, 2020). Understanding whether the same molecular machinery is involved in establishing and maintaining photosymbiosis each time, poses interesting questions about when we should consider a trait as homologous vs. convergent (Stoecker et al, 2009;Melo Clavijo et al, 2018;Li et al, 2020). Studying similar types of symbioses across diverse organisms will lend itself not only to mechanistic discoveries, but also to advancing conceptual debates.…”

“…However, these two distantly related animal lineages both utilize the vacuolar H + -ATPase gene (VHA) to acidify their symbiont-containing environments, thereby facilitating the carbon concentrating process, and promoting algal photosynthesis (Barott et al, 2015;Armstrong et al, 2018). Vacuolar H + -ATPase is a highly conserved gene in eukaryotes (Anraku et al, 1992), and neither host lineage possesses "special" versions of VHA compared to their non-symbiotic relatives (Li et al, 2020). Therefore, adaptations to photosymbiosis appear to have occurred at the regulatory/expression level, specifically by expressing VHA in the symbiont-containing cells/tissues (Barott et al, 2015;Armstrong et al, 2018).…”