Contribution
A short review, written after an NSF “Reintegrating Biology” meeting, which argues that coral research should treat the coral as a consortium. It adds no data. Its contributions are a definition of the coral holobiont, four methodological demands under the heading “a holistic approach requires”, and three open research questions. It is useful mainly as a compact statement of the position with its worked examples.
Key insight
A partner’s trait is not a property of the partner. Whether a Symbiodiniaceae genus is “thermally tolerant”, or whether a coral “bleached”, depends on the combination it is in and on which partner the measurement looked at. So the unit that has the phenotype is the combination, and a study that measures one partner can misattribute what it sees.
Assumptions
- Holobiont by location. The coral holobiont is the coral plus the microbiota in its body, mucus and skeleton (Introduction, after Rohwer et al. 2002). Associated animals are excluded “even if they engage in mutualisms with corals”. Margulis’s 1991 definition, a “symbiont compound of recognizable bionts”, is quoted, with the caveat that not every symbiont is part of a holobiont. No criterion of integration or dependence is used.
- Coral covers scleractinians and octocorals together.
- The cited results are taken as given. The review does not reanalyse them.
Key results
The paper’s evidence, every item cited from other work:
- Mutual benefits (Constituents section). Corals gain photosynthate and enhanced calcification from Symbiodiniaceae, and the algae take up the coral’s nitrogenous waste and are protected. Bacteria may supply carbon, nitrogen and sulfur and protect against antagonists. For archaea, viruses and fungi the roles are “reviewed” possibilities.
- Changing membership (Specificity section). Coral species keep specific Symbiodiniaceae genera and types under stress (Goulet 2006, 2007), with shuffling of proportions (Berkelmans & van Oppen 2006). Bacteria are both core and transient, and vary by geography and microhabitat. Hence the claim that “the same coral colony may represent a different holobiont at different times and/or under different environmental conditions”.
- Symbiont affects host fitness. Juvenile Acropora millepora and A. tenuis with Cladocopium grew up to three times faster than with Durusdinium (Little et al. 2004). The authors infer an effect on survivorship and on the onset of reproduction.
- Bleaching mechanism contested. Whether the host expels the algae or the algae abandon “a sinking ship” is “still debated”. In some species bleaching varies with the Symbiodiniaceae hosted, and in others it does not.
- Non-additivity (in an anemone). In Exaiptasia pallida, Florida anemone–Symbiodinium holobionts had higher oxygen flux under heat than Bermuda anemones with their native Breviolum. A laboratory pairing of Bermuda anemones with Symbiodinium gave higher flux than either natural combination at 32 and 34 °C (Goulet et al. 2005). This is the abstract’s “evidence that the holobiont properties are not necessarily the sum of its parts”.
- Two routes to one bleaching outcome. Octocoral branches at +3 °C lost Symbiodiniaceae: 26% in Eunicea tourneforti and 35% in Pseudoplexaura crucis. In P. crucis lipid also fell 19%, so symbionts per unit host lipid did not change significantly. The reading: E. tourneforti lost symbionts per host cell, while P. crucis lost host cells (McCauley et al. 2018).
- Stable consortia under perturbation. In seven Caribbean octocorals, in Acropora digitifera and A. muricata, and in six Red Sea corals, the Symbiodiniaceae and dominant bacteria were stable while bacterial abundances or mucus communities shifted.
Claims
| id | claim | strength | support |
|---|---|---|---|
| C1 | The coral should be studied as a holobiont, the coral plus the microbiota in its body, mucus and skeleton | informal argument | Introduction; Discussion |
| C2 | A colony’s holobiont can change membership over time, so the entity under study may not be constant | moderate (from cited specificity and transience studies) | Specificity section |
| C3 | Traits such as thermal tolerance should be attributed to host–symbiont combinations, not to partner taxa | moderate (one counterexample to a genus-level label) | Durusdinium discussion, citing LaJeunesse et al. 2014 |
| C4 | Holobiont properties are not necessarily the sum of partners’ properties | weak for corals: one trait (oxygen flux) in one anemone system | Goulet et al. 2005 |
| C5 | Host and symbiont measures together distinguish bleaching routes that symbiont density alone conflates | moderate: two octocoral species, one study | McCauley et al. 2018 |
| C6 | Host/symbiont terminology carries assumptions about control, and the Adaptive Bleaching Hypothesis became coral-centric through it | informal argument | Discussion, quoting Gardiner 1931 and Buddemeier & Fautin 1993 |
| C7 | Whether the coral holobiont is a unit of selection is open | question posed | Future Research Directions |
Concepts
- holobiont — after Margulis, a “symbiont compound of recognizable bionts”. For corals, the coral plus the microbiota in its body, mucus and skeleton.
- coral consortium — the paper’s synonym for the coral holobiont.
- specificity — a coral species hosting particular Symbiodiniaceae (or bacterial) taxa consistently.
- shuffling — a change in the proportions of symbiont types already present, as opposed to acquiring new ones.
- core microbiome / transient microbiota — bacteria consistently present versus those that come and go.
- Adaptive Bleaching Hypothesis (ABH) — Buddemeier and Fautin’s 1993 proposal that bleaching lets a holobiont lose ill-suited symbionts and take up better-suited ones.
Connections
- The bleaching review (LIT-712). Boilard et al. build their second stage of bleaching on the ABH and describe it in host-centred terms (“the coral host has the ability to regulate the density and diversity of their associated Symbiodiniaceae”). That is the framing this paper warns about. Neither cites the other; they appeared a month apart.
- Lloyd (LIT-160). C7 is Lloyd’s §4.6 question. On her anatomy, C4 is evidence relevant to holobionts as interactors, a combination-level character, and says nothing about holobionts as reproducers or as manifestors of adaptation.
- Wilson & Barker (LIT-168) and O’Malley & Parke (LIT-210) report the holobiont’s individuality as unsettled. This paper supplies coral cases for that dispute and does not take a side.
- Baedke (LIT-167) rejects the holobiont as organism on anti-nesting and epistemic grounds. C2, that membership changes, is an independent difficulty for treating the holobiont as one persisting thing. This paper does not draw it.
- Montévil & Mossio (LIT-582). Their tendency to closure is a proposed way to draw boundaries between interdependent organisms. The location definition used here is the kind of observer-drawn boundary that closure is meant to replace.
Bearing on the record
- It is the conceptual source for the composite-system framing of corals. It is cited, with the bleaching review, in the theory that coral bleaching is a breakdown of a regulated host–symbiont exchange reached by more than one route (THEORY-130). C5 is the evidence for “more than one route”.
- No ML instruction; nothing for the anthology.
Limitations
- A review with no data, and short: about 3,700 words of body text.
- The non-additivity evidence is not coral evidence and covers one physiological variable.
- The holobiont definition is spatial. It gives no way to decide whether a transient bacterium is a member, a question the authors raise themselves (“what is considered transient needs to be defined”).
- Unit of selection is posed, not argued.
- The octocoral inference (host-cell loss versus symbiont loss per cell) rests on lipid as a proxy for host biomass, and the review does not discuss the proxy.
Open questions
- What makes a microbe a member of the holobiont rather than a visitor? The paper asks for a definition of “transient”.
- Does the holobiont’s fitness depend on the specific consortium or only on the roles its members fill? The paper asks this; a functional-redundancy result would answer it.
- Is the non-additivity of C4 found in corals, and for traits closer to fitness than oxygen flux?