Chimerism and allorecognition in the broadcast spawning coral Acropora millepora on the Great Barrier Reef

Puill-Stephan, Eneour (2010) Chimerism and allorecognition in the broadcast spawning coral Acropora millepora on the Great Barrier Reef. PhD thesis, James Cook University.

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Abstract

The ability to differentiate between self and non-self is a key feature of all living organisms and provides the first line of defense against invading pathogens, however, the allorecognition systems of many marine invertebrates allow fusion of two or more genetically distinct individuals, resulting in the formation of genetic chimeras. In scleractinian corals, fusion among allogeneic juveniles is known to occur following aggregated larval settlement in some brooding species, but no studies have investigated chimerism in juveniles of broadcast spawning corals or in adult populations of any coral species.

Accordingly, the potential of the broadcast spawning coral species, Acropora millepora, to form chimeras during early life stages was explored under experimental conditions, and the persistence of chimeras deployed in the field monitored for 23 months post-settlement. Larvae settled in aggregations in high numbers with 47% of juveniles originating from aggregated settlement. Genotyping at 9 microsatellite loci revealed that 50% of juveniles tested were chimeras. Therefore, Acropora millepora shows high potential for chimera formation following gregarious larval settlement. Relatedness analysis highlighted that the majority of chimeric colonies were either full or half sibling associations. Fusion at settlement confered greater size for chimeras (~three-fold greater) compared to solitary juveniles through to at least three months. Consequently, chimerism is likely to be an important strategy for maximizing survival of vulnerable early life history stages of corals.

To determine if the lack of a mature allorecognition system might facilitate chimera formation, I compared the development of allorecognition in full sibling, half sibling and non-sibling contact reactions between newly settled juveniles of Acropora millepora. In the first two months post-settlement, fusions among juveniles of all kinship levels indicate that A. millepora juveniles lack a mature allorecognition system in early life history stages. Relatedness governed the rate of allorecognition maturation, with all contact reactions between non-siblings rejecting by 3 months, while it took at least 5 months for all contact reactions between half siblings to reject and longer than 13 months for full siblings. The comparatively slow maturation of allorecognition in spawning corals (more than 13 months) compared to brooders (4 months) constitutes a significant difference in their life history strategies, and may contribute to flexibility in Symbiodinium uptake in the early ontogeny of broadcast spawning corals.

Differential expression of putative immune response genes (apextrin, complement C3, and two CELIII type lectin genes) was monitored in Acropora millepora juveniles for six months post-settlement, to explore the molecular basis of allorecognition maturation. Using quantitative real-time PCR (qPCR), I found that expression of the lectin gene A036-E7 peaked and was significantly greater in the fourth month than at any other time for the majority of coral juveniles sampled. Complement C3 and apextrin were also highly expressed concurrently with A036-E7, suggesting that there may be a number of genes co-expressed and influencing the immune system of corals during development. Increased expression levels of one lectin gene may be linked to allorecognition maturation, or alternatively may represent a response to non-self recognition challenges. Although my data are preliminary, they confirm, as highlighted by recent studies of A. millepora, the crucial role lectins may play in the allorecognition and innate immunity of corals.

The extent of chimerism was explored within two wild populations of a common coral, Acropora millepora, on the Great Barrier Reef, Australia, by using up to 12 polymorphic DNA microsatellite loci. At least 2% and 5% of Magnetic Island and Pelorus Island populations of A. millepora, respectively, were found to be chimeras (3% overall), based on conservative estimates. These values are likely to be vast underestimates of the true extent of chimerism in wild populations, as the sampling protocol was restricted to a maximum of eight branches per colony, whereas most colonies consist of hundreds of branches. Genotypes within chimeric corals showed high relatedness, indicating that genetic similarity is a prerequisite for long-term acceptance of non-self genotypes within coral colonies. Detection of chimeras in wild populations of Acorpora millepora validates results of experimental studies showing fusion and chimera persistence in juveniles.

Taken together, the high potential for chimera formation following aggregated larval settlement found in experimental studies and the occurrence of chimerism in wild populations of A. millepora suggest that chimerism is likely to be an important strategy in the early life cycle of broadcast spawning corals and may be more widespread in corals than previously thought. Chimerism and associated increased genetic diversity within colonies are likely to have important implications for the resilience of reef corals, potentially enhancing their capacity to compete for space and respond to environmental stressors and pathogen infection.

Item ID: 18999
Item Type: Thesis (PhD)
Keywords: chimerism, allorecognition, broadcast spawning corals, Great Barrier Reef, Acropora millepora, genetics, coral reefs, coral reef colonies, ecological connectivity, larval recruitment, biological resilience, life histories, gene expression, larval settlement, relatedness, ecological persistence, coral larvae, allorecognition maturation
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 5: Puill-Stephan, E., Willis, B.L., van Herwerden, L., and van Oppen, M.J.H. (2009) Chimerism in wild adult populations of the broadcast spawning coral Acropora millepora on the Great Barrier Reef. PLoS ONE 4(11): e7751. doi: 10.1371/journal.pone.0007751

Date Deposited: 28 Nov 2011 23:08
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 34%
06 BIOLOGICAL SCIENCES > 0608 Zoology > 060808 Invertebrate Biology @ 33%
06 BIOLOGICAL SCIENCES > 0604 Genetics > 060411 Population, Ecological and Evolutionary Genetics @ 33%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 34%
96 ENVIRONMENT > 9605 Ecosystem Assessment and Management > 960506 Ecosystem Assessment and Management of Fresh, Ground and Surface Water Environments @ 33%
97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 33%
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