Abstract

Coral reefs are the epitome of species diversity, yet the number of described scleractinian coral species, the framework-builders of coral reefs, remains moderate by comparison. DNA sequencing studies are rapidly challenging this notion by exposing a wealth of undescribed diversity, but the evolutionary and ecological significance of this diversity remains largely unclear. Here, we present an annotated genome for one of the most ubiquitous corals in the Indo-Pacific (Pachyseris speciosa) and uncover, through a comprehensive genomic and phenotypic assessment, that it comprises morphologically indistinguishable but ecologically divergent lineages. Demographic modeling based on whole-genome resequencing indicated that morphological crypsis (across micro- and macromorphological traits) was due to ancient morphological stasis rather than recent divergence. Although the lineages occur sympatrically across shallow and mesophotic habitats, extensive genotyping using a rapid molecular assay revealed differentiation of their ecological distributions. Leveraging "common garden" conditions facilitated by the overlapping distributions, we assessed physiological and quantitative skeletal traits and demonstrated concurrent phenotypic differentiation. Lastly, spawning observations of genotyped colonies highlighted the potential role of temporal reproductive isolation in the limited admixture, with consistent genomic signatures in genes related to morphogenesis and reproduction. Overall, our findings demonstrate the presence of ecologically and phenotypically divergent coral species without substantial morphological differentiation and provide new leads into the potential mechanisms facilitating such divergence. More broadly, they indicate that our current taxonomic framework for reef-building corals may be scratching the surface of the ecologically relevant diversity on coral reefs, consequently limiting our ability to protect or restore this diversity effectively.

Highlights

  • Tropical coral reefs are known for their high levels of biodiversity, harboring hundreds of thousands of macroscopic and an unknown number of microscopic species.[1]

  • Tens of thousands of multicellular species have been described in association with tropical coral reefs, yet this is estimated to represent

  • Reef-building corals (Scleractinia) have been considered to contribute relatively little to this estimated discrepancy, with the taxonomy considered to be relatively complete compared to other lessstudied coral reef taxa.[1]

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Summary

Introduction

Tropical coral reefs are known for their high levels of biodiversity, harboring hundreds of thousands of macroscopic and an unknown number of microscopic species.[1]. Molecular approaches have helped resolve some of these difficulties by differentiating morphological plasticity from actual species traits,[11,12] confirming species separation in the context of subtle morphological differences,[13,14,15] and clarifying deeper evolutionary relationships within the order.[9,10] molecular studies have uncovered a wealth of undescribed diversity within taxonomic species that cannot be readily explained.[11,16,17,18,19,20,21,22,23,24]

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