Seven photosymbiotic lineages are currently known in the Bivalvia, but obligate associations are limited to tropical representatives of the Cardiidae, which also exhibit a suite of behavioral, anatomical and microstructural adaptations. – Kirkendale & Paulay, 2017

Background:

Little known to most, the giant clams are not the only photosymbiotic clams! The other group of clams that host photosymbionts is the fragines (or heart cockles). Although the giant clams were initially placed in a separate family (Tridacnidae), they are now phylogenetically recognised as highly modified cardiids (Herrera et al., 2015). And their closest relatives are the fragines!

Given this newfound relationship, I have wondered – which group picked up photosymbiosis first? Did they evolved separately or co-evolved? Let’s find out!

The family members of photosymbiotic cockles

Cardiids are the only extant bivalves known to be involved in obligate photosymbiosis (Kirkendale & Paulay, 2017). Within the family of Cardiids, the Tridacninae and Fraginae exhibit photosymbiosis, but both subfamilies show very different morphological responses to a similar selective pressure of capturing light for photosynthesis.

Photosymbiotic shells
Members of the Cardiidae family that are in symbiosis with microalgae. Photo credits: Neo Mei Lin.

Giant clams were the first photosymbiotic bivalves documented (Yonge, 1936). All the members of Tridacninae (Tridacna and Hippopus) host zooxanthellae, and this mutualistic relationship with photosymbionts has been said to explain how they attain their great sizes. Contrary, only a subset of members of Fraginae exhibit photosymbiosis, namely those of genera Corculum, Lunulicardia, and Fragum.

Most of the known photosymbiotic taxa such as stony corals and shell-less sea slugs have exposed soft tissues and large surface areas that assist in light capture by photosymbionts. Yet, these hard and opaque shelled bivalves are able to facilitate photosymbiosis, even though their bodies are not ‘adapted’ for the process. Given these constraints, how do they allow for light capture? Here’s a summary of how they do it!

Adaptations for photosymbiotic lifestyle – Functional morphology:

Generally, the risk of predation is high for these photosymbiotic bivalves due to their epibiotic and shallow infaunal habits, but are often minimise through escape to safe places, crypsis, or gigantism. On one hand, the giant clams have responded with a similar suite of morphological adaptations to photosymbiosis. On the other hand, the heart cockles displayed multiple morphological solutions to the problem of light capture.

Tridacna spp. and Hippopus spp.

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  • Unlike the other cardiids that are partially or entirely buried in the sediments, the giant clams are epibenthic in habit, i.e. they live on the surface of seabed. Thus, allowing for light capture.
  • The anatomical body plan of tridacnines is highly modified compared to a typical cardiid (see Figure 4 below). For example, the posterior mantle tissue (where photosymbionts reside) is greatly enlarged and exposed upward to the light between the widely gaping valves.
  • Modified hypertrophied mantle extends laterally over the valve margin (in Tridacna), increasing the surface area for light capture.
  • Photosymbionts are located in a specialised tubule system, separated from the surrounding haemocoel.
Screenshot 2019-06-07 at 6.16.53 PM
Anatomical organisation between a typical cardiid and Tridacna. Extracted from Kirkendale & Paulay, 2017.

Corculum spp.

Heart cockle-TPTengah2012_THantu2013
Heart cockles (Corculum spp.)
  • The Corculum shells are strictly epifaunal, hence lies posterior side up and often extremely cryptic.
  • Their shells are thin (i.e. translucency) and greatly flattened – this shape greatly enhances the surface area for light capture. A reduction in shell pigmentation also facilitates light penetration.
  • Presence of well-developed ‘window’  and condensing-lens microstructures that are translucent permitting light penetration.

Fragum spp.

Strawberry cockle-TPDarat2010
Strawberry cockle (Fragum unedo)
  • This Fragum unedo is not completely epifaunal, but buries itself in the sediments only revealing its valve gape.
  • Exposure of symbionts by posterior valve gaping and limited extension of its mantle over the valve margin (in Fragum).
  • Photosymbionts are located in a specialised tubule system, separated from the surrounding haemocoel.

So… what’s the origin of photosymbiosis in cardiids?

Based on their phylogenetic relationships, photosymbiosis appears to have derived from two separate ancestral origins: in the Tridacnine and Fraginae. It should be noted that within the fragines, photosymbiosis is restricted to only one clade (FragumLunulicardiaCorculum). Therefore, this suggests either independent origin in Tridacninae and FragumLunulicardiaCorculum, or loss of photosymbiosis trait along the lineage, depending on the relationship of Fraginae and Tridacninae.

Another possibility is a single lineage of photosymbiosis if fragines and tridacnines were found to be sister lineages. But the relationship between these subfamilies remains unclear, as the giant clams were found to be more closely related to the azooxanthellate cardiids than to Fragum or Corculum (Herrera et al., 2015).

Despite this disparate phylogenetic placement, Kirkendale & Paulay (2017) remarked that both groups share a common anatomical structure – the complex zooxanthellal tubular system housing photosymbionts that is found in the mantle, gills and foot (in this case, the Corculum). Again, this means either this tubule structure had evolved convergently or photosymbiosis was lost in multiple lineages between the tridacnines and the FragumLunulicardiaCorculum clade.

Alas, evidence from fossil records for photosymbiosis in extinct bivalves is limited and ambiguous. The lack of unique photosymbiotic characters also makes it difficult to establish if any of the fossil bivalves could have been photosymbiotic. At present, more research is proposed for identifying photosymbiont lineages in bivalves beyond the currently known ones, so as to push ahead understanding the evolutionary history of photosymbiosis in bivalves.

Further readings:

  • Herrera ND, JJ ter Poorten, R Bieler, PM Mikkelsen, EE Strong, D Jablonski & SJ Steppan (2015) Molecular phylogenetics and historical biogeography amid shifting continents in the cockles and giant clams (Bivalvia: Cardiidae). Molecular Phylogenetics and Evolution 93: 94-106.
  • Kirkendale L (2009) Their Day in the Sun: molecular phylogenetics and origin of photosymbiosis in the ‘other’ group of photosymbiotic marine bivalves (Cardiidae: Fraginae). Biological Journal of the Linnean Society 97: 448-465.
  • Kirkendale L & G Paulay (2017) Part N, Revised, Volume 1, Chapter 9: Photosymbiosis in Bivalvia. Treatise Online 89: 1-31.
  • Li J, M Volsteadt, L Kirkendale & CM Cavanaugh (2018) Characterizing photosymbiosis between Fraginae bivalves and Symbiodinium using phylogenetics and stable isotopes. Frontiers in Ecology and Evolution 6: 45.
  • Yonge CM (1936) Mode of life, feeding, digestion and symbiosis with zooxanthellae in the Tridacnidae. Scientific Reports, Great Barrier Reef Expedition 1928-29. Volume 1, pp. 283-321.
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