From genomics to integrative species delimitation? The case study of the Indo-Pacific Pocillopora corals

Abstract

With the advent of genomics, sequencing thousands of loci from hundreds of individuals now appears feasible at reasonable costs, allowing complex phylogenies to be resolved. This is particularly relevant for cnidarians, for which insufficient data is available due to the small number of currently available markers and obscures species boundaries. Difficulties in inferring gene trees and morphological incongruences further blur the study and conservation of these organisms. Yet, can genomics alone be used to delimit species? Here, focusing on the coral genus Pocillopora, whose colonies play key roles in Indo-Pacific reef ecosystems but have challenged taxonomists for decades, we explored and discussed the usefulness of multiple criteria (genetics, morphology, biogeography and symbiosis ecology) to delimit species of this genus. Phylogenetic inferences, clustering approaches and species delimitation methods based on genome-wide single-nucleotide polymorphisms (SNP) were first used to resolve Pocillopora phylogeny and propose genomic species hypotheses from 356 colonies sampled across the Indo-Pacific (western Indian Ocean, tropical southwestern Pacific and south-east Polynesia). These species hypotheses were then compared to other lines of evidence based on genetic, morphology, biogeography and symbiont associations. Out of 21 species hypotheses delimited by genomics, 13 were strongly supported by all approaches, while six could represent either undescribed species or nominal species that have been synonymised incorrectly. Altogether, our results support (1) the obsolescence of macromorphology (i.e., overall colony and branches shape) but the relevance of micromorphology (i.e., corallite structures) to refine Pocillopora species boundaries, (2) the relevance of the mtORF (coupled with other markers in some cases) as a diagnostic marker of most species, (3) the requirement of molecular identification when species identity of colonies is absolutely necessary to interpret results, as morphology can blur species identification in the field, and (4) the need for a taxonomic revision of the genus Pocillopora. These results give new insights into the usefulness of multiple criteria for resolving Pocillopora, and more widely, scleractinian species boundaries, and will ultimately contribute to the taxonomic revision of this genus and the conservation of its species.

Keywords: Biogeography; Integrative taxonomy; Morphology; Phylogenetics; Single-nucleotide polymorphism (SNP); Symbiodiniaceae.