The evolution of molluscan photosymbioses: a critical appraisal

Abstract

Partnerships between animals and photosynthesizing microbes have evolved repeatedly, although their history, adaptations, and ecology remain controversial and little understood. In a critical review of 17 fossil and living clades of shell‐bearing molluscs with photosymbionts (two of them newly inferred), adaptive shell modifications and ecological aspects are discussed in the broader context of photosymbioses in other phyla. Fossil candidates have characteristics that are rare or unknown in living photosymbiotic molluscs, including cementation, porous shell microstructure, and epifaunal habits on carbonate muds. Many ancient photosymbioses may have lived in planktonically more productive environments than are typical of living tropical forms. This may be related to the late appearance (Early Eocene) of the dinoflagellate Symbiodinium, which can thrive under highly oligotrophic conditions. Living photosymbiotic molluscs represent a small and atypical sample of all the photosymbiotic clades that have evolved. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 497–511.

Characterizing Photosymbiosis Between Fraginae Bivalves and Symbiodinium Using Phylogenetics and Stable Isotopes

“…Clade C Symbiodinium is the most dominant clade in the Indo-Pacific region and can be found in diverse groups of invertebrate hosts (LaJeunesse, 2005;Pochon et al, 2006). Given that the photosymbiotic Fraginae is a relatively young clade (late Miocene, Vermeij, 2013), existing symbionts in clade C likely established associations with fragines via host expansion. It is worth noting that even though we did not identify any Fraginae-specific Symbiodinium subclades within clade C, a more variable genetic marker (e.g., ITS) may reveal a different picture.…”

“…The algae provide photosynthetic products to the host and gain shelter and inorganic nutrients in return, allowing the symbiosis to flourish in nutrient deficient habitats. Such associations have evolved in diverse marine lineages, including Foraminifera, Porifera, Cnidaria, and Mollusca (Gast and Caron, 2001;Stanley Jr, 2006;Hill et al, 2011;Vermeij, 2013). Among marine bivalves, photosymbiosis has been documented in at least four groups (Vermeij, 2013;Kirkendale and Paulay, 2017).…”

“…Such associations have evolved in diverse marine lineages, including Foraminifera, Porifera, Cnidaria, and Mollusca (Gast and Caron, 2001;Stanley Jr, 2006;Hill et al, 2011;Vermeij, 2013). Among marine bivalves, photosymbiosis has been documented in at least four groups (Vermeij, 2013;Kirkendale and Paulay, 2017). However, obligate associations are found in only two cockle (Cardiidae) subfamilies, Tridacninae (i.e., giant clams), and Fraginae (i.e., heart cockles and relatives), where the former is relatively well studied.…”

The oyster enigma variations: a hypothesis of microbial calcification

“…They also occur in some gastropods (Fissurelloidea, Neomphaloidea, and Phenacolepadidae) (Sasaki et al 2003(Sasaki et al , 2008Kiel 2004;Hesz et al 2008) and, as aesthete canal systems, in the plates of polyplacophorans (Fernandez et al 2007) and the sclerites of halkieriids (Vinther 2009). A shell cavity secondarily divided by septa or tabulae is known in putatively photosymbiotic Paleozoic productide brachiopods (Rudwick andCowen 1967, reviewed in Vermeij 2013) as well as in three groups of bivalves (Permian alatoconchids, Late Triassic wallowaconchids, and Late Cretaceous hippuritid rudists) that likely also harbored photosymbionts (reviewed in Vermeij 2013). Septa characterize all shell-bearing cephalopods, and evolved at least seven times in gastropods (Paleozoic euomphalids and macluritids, the Miocene to Recent turritellid Vermicularia, late Cretaceous to Recent vermetids, Eocene to Recent dendropomatids, the Miocene hipponicid Rothpletzia, and the Miocene Indonesian melongenid Melongena murifacta) (Yochelson 1971;Vokes 1982;Savazzi 1996;Wagner 1999;Vermeij and Raven 2009).…”

Wavelength-specific forward scattering of light by Bragg-reflective iridocytes in giant clams

“…In spite of living in nutrient-poor waters [2][3][4], the clams can grow up to 1.4 m long [5]. Such large sizes are attainable largely due to the dense cultures of endosymbiotic microalgae of the genus Symbiodinium that clams maintain within their tissues [6][7][8][9][10][11]. Like the reefbuilding corals that also host members of this algal genus, the giant clams depend on the photosynthesis of these symbionts to produce vital nutrients that support their growth in the oligotrophic and plankton-poor waters of the tropical reef, and to modulate the carbonate equilibria controlling the rapid calcification of their shells [12][13][14][15][16].…”