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Coral kin aggregations exhibit mixed allogeneic reactions and enhanced fitness during early ontogeny

BACKGROUND: Aggregated settlement of kin larvae in sessile marine invertebrates may result in a complex array of compatible and incompatible allogeneic responses within each assemblage. Each such aggregate can, therefore, be considered as a distinct self-organizing biological entity representing ada...

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Autores principales: Amar, Keren-Or, Chadwick, Nanette E, Rinkevich, Baruch
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2008
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2391163/
https://www.ncbi.nlm.nih.gov/pubmed/18447918
http://dx.doi.org/10.1186/1471-2148-8-126
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author Amar, Keren-Or
Chadwick, Nanette E
Rinkevich, Baruch
author_facet Amar, Keren-Or
Chadwick, Nanette E
Rinkevich, Baruch
author_sort Amar, Keren-Or
collection PubMed
description BACKGROUND: Aggregated settlement of kin larvae in sessile marine invertebrates may result in a complex array of compatible and incompatible allogeneic responses within each assemblage. Each such aggregate can, therefore, be considered as a distinct self-organizing biological entity representing adaptations that have evolved to maximize the potential benefits of gregarious settlement. However, only sparse information exists on the selective forces and ecological consequences of allogeneic coalescence. RESULTS: We studied the consequences of aggregated settlement of kin larvae of Stylophora pistillata (a Red Sea stony coral), under controlled laboratory settings. When spat came into contact, they either fused, establishing a chimera, or rejected one another. A one-year study on growth and survivorship of 544 settled S. pistillata genotypes revealed six types of biological entities: (1) Single genotypes (SG); (2) Bi-chimeras (BC); (3) Bi-rejecting genotypes (BR); (4) Tri-chimera entities (TC); (5) Three-rejecting genotypes (TR); and (6) Multi-partner entities (MP; consisting of 7.5 ± 2.6 partners). Analysis of allorecognition responses revealed an array of effector mechanisms: real tissue fusions, transitory fusions and six other histoincompatible reactions (borderline formation, sutures, overgrowth, bleaching, rejection, and partner death), disclosing unalike onsets of ontogeny and complex modes of appearance within each aggregate. Evaluations at the entity level revealed that MP entities were the largest, especially in the first two months (compared with SG: 571% in the first month and 162% in the seventh month). However, at the genotype level, the SG entities were the largest and the colonies with the highest-cost-per-genotype were the TR and the MP colonies. The cost was calculated as reduced average genotype size, from 27% and 12% in the first month to 67% and 64% in the seventh month, respectively. In general, MP exhibited the highest survivorship rate (85%, after one year) and SG the lowest (54%). CONCLUSION: In view of the above, we suggest that the driving force behind gregarious kin settlements in Stylophora pistillata stems from gained benefits associated with the immediate and long-term increase in total size of the MP entity, whereas survivorship rates did not draw a parallel link. Furthermore, the biological organization of MP entity exhibits, simultaneously, an intricate network of rejecting and fusible interactions in a single allogeneic intimate arena, where proposed benefits surpass costs incurred by discord among founders. Above results and documentations on gregarious settlement in other marine taxa bring us to suggest that the 'group level' of kin aggregates may serve as a ubiquitous legitimate selection entity in the evolution of a sessile mode of life in marine organisms.
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spelling pubmed-23911632008-05-22 Coral kin aggregations exhibit mixed allogeneic reactions and enhanced fitness during early ontogeny Amar, Keren-Or Chadwick, Nanette E Rinkevich, Baruch BMC Evol Biol Research Article BACKGROUND: Aggregated settlement of kin larvae in sessile marine invertebrates may result in a complex array of compatible and incompatible allogeneic responses within each assemblage. Each such aggregate can, therefore, be considered as a distinct self-organizing biological entity representing adaptations that have evolved to maximize the potential benefits of gregarious settlement. However, only sparse information exists on the selective forces and ecological consequences of allogeneic coalescence. RESULTS: We studied the consequences of aggregated settlement of kin larvae of Stylophora pistillata (a Red Sea stony coral), under controlled laboratory settings. When spat came into contact, they either fused, establishing a chimera, or rejected one another. A one-year study on growth and survivorship of 544 settled S. pistillata genotypes revealed six types of biological entities: (1) Single genotypes (SG); (2) Bi-chimeras (BC); (3) Bi-rejecting genotypes (BR); (4) Tri-chimera entities (TC); (5) Three-rejecting genotypes (TR); and (6) Multi-partner entities (MP; consisting of 7.5 ± 2.6 partners). Analysis of allorecognition responses revealed an array of effector mechanisms: real tissue fusions, transitory fusions and six other histoincompatible reactions (borderline formation, sutures, overgrowth, bleaching, rejection, and partner death), disclosing unalike onsets of ontogeny and complex modes of appearance within each aggregate. Evaluations at the entity level revealed that MP entities were the largest, especially in the first two months (compared with SG: 571% in the first month and 162% in the seventh month). However, at the genotype level, the SG entities were the largest and the colonies with the highest-cost-per-genotype were the TR and the MP colonies. The cost was calculated as reduced average genotype size, from 27% and 12% in the first month to 67% and 64% in the seventh month, respectively. In general, MP exhibited the highest survivorship rate (85%, after one year) and SG the lowest (54%). CONCLUSION: In view of the above, we suggest that the driving force behind gregarious kin settlements in Stylophora pistillata stems from gained benefits associated with the immediate and long-term increase in total size of the MP entity, whereas survivorship rates did not draw a parallel link. Furthermore, the biological organization of MP entity exhibits, simultaneously, an intricate network of rejecting and fusible interactions in a single allogeneic intimate arena, where proposed benefits surpass costs incurred by discord among founders. Above results and documentations on gregarious settlement in other marine taxa bring us to suggest that the 'group level' of kin aggregates may serve as a ubiquitous legitimate selection entity in the evolution of a sessile mode of life in marine organisms. BioMed Central 2008-04-30 /pmc/articles/PMC2391163/ /pubmed/18447918 http://dx.doi.org/10.1186/1471-2148-8-126 Text en Copyright ©2008 Amar et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Amar, Keren-Or
Chadwick, Nanette E
Rinkevich, Baruch
Coral kin aggregations exhibit mixed allogeneic reactions and enhanced fitness during early ontogeny
title Coral kin aggregations exhibit mixed allogeneic reactions and enhanced fitness during early ontogeny
title_full Coral kin aggregations exhibit mixed allogeneic reactions and enhanced fitness during early ontogeny
title_fullStr Coral kin aggregations exhibit mixed allogeneic reactions and enhanced fitness during early ontogeny
title_full_unstemmed Coral kin aggregations exhibit mixed allogeneic reactions and enhanced fitness during early ontogeny
title_short Coral kin aggregations exhibit mixed allogeneic reactions and enhanced fitness during early ontogeny
title_sort coral kin aggregations exhibit mixed allogeneic reactions and enhanced fitness during early ontogeny
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2391163/
https://www.ncbi.nlm.nih.gov/pubmed/18447918
http://dx.doi.org/10.1186/1471-2148-8-126
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