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Molecular convergence and positive selection associated with the evolution of symbiont transmission mode in stony corals.

ABSTRACT: Heritable symbioses have been critical for the evolution of life. The genetic consequences of evolving a heritable symbiosis from the perspective of the symbiont are well established, but concomitant changes in the host remain unresolved. In stony corals, heritable, vertical transmission has evolved repeatedly, providing a unique opportunity to investigate the genomic basis of this complex trait. We conducted a comparative analysis of 25 coral transcriptomes to identify orthologous genes exhibiting signatures of positive selection and convergent amino acid substitutions in vertically transmitting lineages. The frequency of convergence events tends to be higher among vertically transmitting lineages, consistent with the proposed role of selection in driving the evolution of convergent transmission mode phenotypes. Of 10 774 orthologous genes, 403 exhibited at least one molecular convergence event and evidence of positive selection in at least one vertically transmitting lineage. Functional enrichments among these top candidate genes include processes previously implicated in symbiosis including endocytosis, immune response, cytoskeletal protein binding and cytoplasmic membrane-bounded vesicles. Finally, several novel candidates were identified among 100 genes showing evidence of positive selection at the particular convergence event, highlighting the value of our approach for generating new insight into host mechanisms associated with the evolution of heritable symbioses.

SUBMITTER: Dixon GB

PROVIDER: S-EPMC6501935 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Molecular convergence and positive selection associated with the evolution of symbiont transmission mode in stony corals.

Dixon Groves B GB Kenkel Carly D CD

Proceedings. Biological sciences 20190401 1901

Heritable symbioses have been critical for the evolution of life. The genetic consequences of evolving a heritable symbiosis from the perspective of the symbiont are well established, but concomitant changes in the host remain unresolved. In stony corals, heritable, vertical transmission has evolved repeatedly, providing a unique opportunity to investigate the genomic basis of this complex trait. We conducted a comparative analysis of 25 coral transcriptomes to identify orthologous genes exhibit ...[more]

PMID: 30991927

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Project description:A comprehensive understanding of coral reproduction and development is needed because corals are threatened in many ways by human activity. Major threats include the loss of their photosynthetic symbionts (Symbiodinium) caused by rising temperatures (bleaching), reduced ability to calcify caused by ocean acidification, increased storm severity associated with global climate change and an increase in predators caused by runoff from human agricultural activity. In spite of these threats, detailed descriptions of embryonic development are not available for many coral species. The current consensus is that there are two major groups of stony corals, the "complex" and the "robust". In this paper we describe the embryonic development of four "complex" species, Pseudosiderastrea tayamai, Galaxea fascicularis, Montipora hispida, and Pavona Decussata, and seven "robust" species, Oulastrea crispata, Platygyra contorta, Favites abdita, Echinophyllia aspera, Goniastrea favulus, Dipsastraea speciosa (previously Favia speciosa), and Phymastrea valenciennesi (previously Montastrea valenciennesi). Data from both histologically sectioned embryos and whole mounts are presented. One apparent difference between these two major groups is that before gastrulation the cells of the complex corals thus far described (mainly Acropora species) spread and flatten to produce the so-called prawn chip, which lacks a blastocoel. Our present broad survey of robust and complex corals reveals that prawn chip formation is not a synapomorphy of complex corals, as Pavona Decussata does not form a prawn chip and has a well-developed blastocoel. Although prawn chip formation cannot be used to separate the two clades, none of the robust corals which we surveyed has such a stage. Many robust coral embryos pass through two periods of invagination, separated by a return to a spherical shape. However, only the second of these periods is associated with endoderm formation. We have therefore termed the first invagination a pseudo-blastopore.

Project description:With marine heat waves increasing in intensity and frequency due to climate change, it is important to understand how thermal disturbances will alter coral reef ecosystems since stony corals are highly susceptible to mortality from thermally-induced, mass bleaching events. In Moorea, French Polynesia, we evaluated the response and fate of coral following a major thermal stress event in 2019 that caused a substantial amount of branching coral (predominantly Pocillopora) to bleach and die. We investigated whether Pocillopora colonies that occurred within territorial gardens protected by the farmerfish Stegastes nigricans were less susceptible to or survived bleaching better than Pocillopora on adjacent, undefended substrate. Bleaching prevalence (proportion of the sampled colonies affected) and severity (proportion of a colony's tissue that bleached), which were quantified for >1,100 colonies shortly after they bleached, did not differ between colonies within or outside of defended gardens. By contrast, the fates of 399 focal colonies followed for one year revealed that a bleached coral within a garden was a third less likely to suffer complete colony death and about twice as likely to recover to its pre-bleaching cover of living tissue compared to Pocillopora outside of a farmerfish garden. Our findings indicate that while residing in a farmerfish garden may not reduce the bleaching susceptibility of a coral to thermal stress, it does help buffer a bleached coral against severe outcomes. This oasis effect of farmerfish gardens, where survival and recovery of thermally-damaged corals are enhanced, is another mechanism that helps explain why large Pocillopora colonies are disproportionately more abundant in farmerfish territories than elsewhere in the lagoons of Moorea, despite gardens being relatively uncommon. As such, some farmerfishes may have an increasingly important role in maintaining the resilience of branching corals as the frequency and intensity of marine heat waves continue to increase.

Dataset Information

Molecular convergence and positive selection associated with the evolution of symbiont transmission mode in stony corals.

Publications

Molecular convergence and positive selection associated with the evolution of symbiont transmission mode in stony corals.

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