Marine Invertebrate Larvae Associated with Symbiodinium: A Mutualism from the Start?

Abstract

Symbiodinium are dinoflagellate photosynthetic algae that associate with a diverse array of marine invertebrates, and these relationships are comprehensively documented for adult animal hosts. Conversely, comparatively little is known about the associations during larval development of animal hosts, although four different metazoan phyla (Porifera, Cnidaria, Acoelomorpha, and Mollusca) produce larvae associated with Symbiodinium. These phyla represent considerable diversities in larval forms, manner of symbiont acquisition, and requirements on the presence of symbionts for successful metamorphosis. Importantly, the different requirements are conveyed by specific symbiont types that are selected by the host animal larvae. Nevertheless, it remains to be determined whether these associations during larval stages already represent mutualistic interactions, as evident from the relationship of Symbiodinium with their adult animal hosts. For instance, molecular studies suggest that the host larval transcriptome is nearly unaltered after symbiont acquisition. Even so, a symbiosis-specific gene has been identified in Symbiodinium that is expressed in larval host stages, and similar genes are currently being described for host organisms. However, some reports suggest that the metabolic exchange between host larvae and Symbiodinium may not cover the energetic requirements of the host. Here, we review current studies to summarize what is known about the association between metazoan larvae and Symbiodinium. In particular, our aim was to gather in how far the mutualistic relationship present between adult animals hosts and Symbiodinium is already laid out at the time of symbiont acquisition by host larvae. We conclude that the mutualistic relationship between animal hosts and algal symbionts in many cases is not set up during larval development. Furthermore, symbiont identity may influence whether a mutualism can be established during host larval stages.

Acquisition of obligate mutualist symbionts during the larval stage is not beneficial for a coral host

“…The incorporation of the photosymbiont into host cells and continued maintenance of the association involves both the symbiont (Hill & Hill, ; Sachs, Essenberg, & Turcotte, ; Sachs & Wilcox, ) and the host (Baird, Bhagooli, Ralph, & Takahashi, ; Barott, Venn, Perez, Tambutté, & Tresguerres, ; Paxton, Davy, & Weis, ), whereby mixed symbiont communities are winnowed to one or a few dominant Symbiodiniaceae species, either through host selection mechanisms or competition among Symbiodiniaceae species (Bay et al, ; Coffroth et al, ; Dunn & Weis, ; Poland & Coffroth, ; Rodriguez‐Lanetty, Wood‐Charlson, Hollingsworth, Krupp, & Weis, ). The symbiont winnowing process can take much longer than the initial acquisition period (Mies et al, ; Poland & Coffroth, ). For example, metamorphosed recruits of a soft coral continue altering their symbiont communities over the course of multiple years, eventually harbouring communities similar to those found in their parents (Poland & Coffroth, ).…”

“…These disadvantages suggest that delaying photosymbiont acquisition provides benefits to larvae of HA coral species, perhaps explaining the incongruence between theory and natural history. While the consequences of larval acquisition in HA species have been examined (e.g., Yakovleva et al, 2009, Nesa et al, 2012, Suzuki et al, 2013, we lack a complete assessment of the physiological, behavioural and ecological costs and benefits of HA (Mies, Sumida, Rädecker, & Voolstra, 2017).…”

Feeding increases the number of offspring but decreases parental investment of Red Sea coral Stylophora pistillata

“…These authors concluded that while minimal translocation was observed, this was in quantities which would negligibly contribute to larval energetic demands (Kopp et al, 2016). Despite demonstrations of increased lipid utilization and decreased survival in darkness (Harii, Yamamoto, & Hoegh-Guldberg, 2010), and changes in symbiont transcriptome upon larval infection (Mohamed et al, 2019), these data do not prove translocation per se and therefore a recent review of the topic concluded that during the larval phase a "mutualistic relationship cannot be unequivocally confirmed" (Mies, Sumida, Rädecker, & Voolstra, 2017). Additionally, there were no isotopic signatures of feeding found in planulae of Red Sea coral Stylophora pistillata ).…”

Polymorphic adaptations in metazoans to establish and maintain photosymbioses

“…Acquiring symbionts horizontally always includes an aposymbiotic life stage present in all photosymbiotic animal lineages, which is usually the larval phase before metamorphosis into juveniles (e.g. Belda‐Baillie et al, ; Weis et al, ; Harrison, ; Pelletreau et al, ; Mies et al, ). Juveniles then successfully take up the symbiont from their environment, but there seems to be little co‐evolution of species with horizontal transmission and their symbiont partners (van Oppen et al, ; Bright & Bulgheresi, ).…”