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

Abstract

BackgroundAggregated 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.ResultsWe 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%).ConclusionIn 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.

Internal brooding favours pre-metamorphic chimerism in a non-colonial cnidarian, the sea anemone Urticina felina

“…Fusion between allogeneic entities might confer immediate advantage to the chimera by virtue of the increment in size, especially because the latter correlates with fecundity and viability in sessile colonial invertebrates [29]. Greater fitness of multi-chimeras has been confirmed in ascidians [18,30] and corals [8,12], and molecular evidence of chimerism is reported in wild coral populations [7]. However, an important distinction exists in the type of chimeras occurring in the different taxa.…”

“…In soft corals and colonial hydroids, a window of opportunity was proposed to exist for chimerism during early ontogeny, making it possible only until the complete development of allorecognition [6,9,10]. In cnidarians, chimerism is thus believed to result from a failure to discriminate self from non-self, with few positive outcomes [6,11], except in larger colonies composed of multiple fused entities [8,12]. In ascidians, and possibly bryozoans, frequency of fusion between kin was shown to be positively correlated with relatedness of colonies [13,14].…”

The CORALZOO project: a synopsis of four years of public aquarium science

“…In CORALZOO, under controlled laboratory settings the consequences of aggregated settlement of kin larvae of S. pistillata were studied (Amar et al, 2008b). When spat came into contact, they either fused, establishing a chimera, or rejected one another.…”

To Fuse or Not to Fuse? An Evolutionary View of Self-Recognition Systems

“…Such positive relationships between size and age in maturity and fecundity rates have been reported in some lichenised fungi and corals [93][94][95][96] but see [97]. In this context, somatic fusion could represent a benefit like those suggested by the reports of an increase in fitness following somatic fusion in some fungi or colonial marine invertebrates species [98][99][100]. Interestingly, Amar et al [100] found while studying 544 colonies of a coral species over a period of one year, that growth and survival rates were higher for colonies generated by the fusion of several germ lines, whereas single-germ line colonies had the lowest survival rates.…”

“…In this context, somatic fusion could represent a benefit like those suggested by the reports of an increase in fitness following somatic fusion in some fungi or colonial marine invertebrates species [98][99][100]. Interestingly, Amar et al [100] found while studying 544 colonies of a coral species over a period of one year, that growth and survival rates were higher for colonies generated by the fusion of several germ lines, whereas single-germ line colonies had the lowest survival rates. In the colonial ascidian B. schlosseri, Carpentier et al [101] observed that chimeras showed a higher fitness than non-chimeras at high-density growth conditions.…”