Frontloading of stress response genes enhances robustness to environmental change in chimeric corals.

BACKGROUND: Chimeras are genetically mixed entities resulting from the fusion of two or more conspecifics. This phenomenon is widely distributed in nature and documented in a variety of animal and plant phyla. In corals, chimerism initiates at early ontogenic states (larvae to young spat) and results from the fusion between two or more closely settled conspecifics. When compared to genetically homogenous colonies (non-chimeras), the literature has listed ecological and evolutionary benefits for traits at the chimeric state, further positioning coral chimerism as an evolutionary rescue instrument. However, the molecular mechanisms underlying this suggestion remain unknown. RESULTS: To address this question, we developed field monitoring and multi-omics approaches to compare the responses of chimeric and non-chimeric colonies acclimated for 1 year at 10-m depth or exposed to a stressful environmental change (translocation from 10- to 2-m depth for 48h). We showed that chimerism in the stony coral Stylophora pistillata is associated with higher survival over a 1-year period. Transcriptomic analyses showed that chimeras lose transcriptomic plasticity and constitutively express at higher level (frontload) genes responsive to stress. This frontloading may prepare the colony to face at any time environmental stresses which explain its higher robustness. CONCLUSIONS: These results show that chimeras are environmentally robust entities with an enhanced ability to cope with environmental stress. Results further document the potential usefulness of chimeras as a novel reef restoration tool to enhance coral adaptability to environmental change, and confirm that coral chimerism can be an evolutionary rescue instrument.

Morphometric and allometric rules of polyp's landscape in regular and chimeric coral colonies of the branching species Stylophora pistillata.

BACKGROUND: Most studies on architectural rules in corals have focused on the branch and the colony level, unveiling a variety of allometric rules. Working on the branching coral Stylophora pistillata, here we further extend the astogenic directives of this species at the polyp level, to reveal allometric and morphometric rules dictating polyps' arrangement. RESULTS: We identified a basic morphometric landscape as a six-polyp circlet developed around a founder polyp, with established distances between polyps (six equilateral triangles), reflecting a strong genetic-based background vs high plasticity on the population level. Testing these rules in regular and chimeric S. pistillata colonies, we revealed similar morphometric/allometric rules developed via a single astogenic pathway. In regular colonies, this pathway was driven by the presence/absence of intra-circlet budding polyps, while in chimeras, by the distances between the two founder polyps. In addition, we identified the intra-circlet budding as the origin of first branching, if BPC distances are kept <1.09 ± 0.25 mm. CONCLUSIONS: The emerged allometric/morphometric rules indicate the existence of a positional information paradigm for polyps' landscape distribution, where each polyp creates its own positional field of morphogen gradients through six inductive sites, thus forming six positional fields for the development of the archetypal "six-polyp crown".

Settling in aggregation: Spatial planning consideration for brooding coral transplants.

Aggregated larval co-settlement has been documented in myriad marine invertebrate taxa, shaping adult population structures. Still, kinship settlement patterns in brooding corals have not been studied in detail, especially under scenarios of enhanced larval assemblies. Employing two sets of ex-situ experiments, planulae staining for kinship resolution and a computer random settlement simulation, we show that larval settlement of the coral Stylophora pistillata, a brooding species in the Gulf of Aqaba/Eilat, is mostly affected by the number of larval donors, and that larvae tend to aggregate (up to 50% tissue-contacts; distances <3 mm), compared to 3% predicted in a computer simulation, all without a kinship-bias. Field surveys on juvenile colonies revealed a similar clustering pattern. Although aggregated settlement inevitably carries disadvantages such as intraspecific competition, it may be bracketed in adult colonies with benefits such as enhanced fertilization and chimerism-related ecological advantages, including augmented colony size and survivorship. These improved life-history traits of brooding coral species that aggregate could be harnessed as applied ecological engineering tools in reef restoration acts.

Spatial distribution of conspecific genotypes within chimeras of the branching coral Stylophora pistillata.

Chimerism is a coalescence of conspecific genotypes. Although common in nature, fundamental knowledge, such as the spatial distribution of the genotypes within chimeras, is lacking. Hence, we investigated the spatial distribution of conspecific genotypes within the brooding coral Stylophora pistillata, a common species throughout the Indo-Pacific and Red Sea. From eight gravid colonies, we collected planula larvae that settled in aggregates, forming 2-3 partner chimeras. Coral chimeras grew in situ for up to 25 months. Nine chimeras (8 kin, 1 non-related genotypes) were sectioned into 7-17 fragments (6-26 polyps/fragment), and genotyped using eight microsatellite loci. The discrimination power of each microsatellite-locus was evaluated with 330 'artificial chimeras,' made by mixing DNA from three different S. pistillata genotypes in pairwise combinations. In 68% of 'artificial chimeras,' the second genotype was detected if it constituted 5-30% of the chimera. Analyses of S. pistillata chimeras revealed that: (a) chimerism is a long-term state; (b) conspecifics were intermixed (not separate from one another); (c) disproportionate distribution of the conspecifics occurred; (d) cryptic chimerism (chimerism not detected via a given microsatellite) existed, alluding to the underestimation of chimerism in nature. Mixed chimerism may affect ecological/physiological outcomes for a chimera, especially in clonal organisms, and challenges the concept of individuality, affecting our understanding of the unit of selection.