Largely understudied, mesophotic coral ecosystems lie below shallow reefs (at >30 m depth) and comprise ecologically distinct communities. Brooding reproductive modes appear to predominate among mesophotic‐specialist corals and may limit genetic connectivity among populations. Using reduced representation genomic sequencing, we assessed spatial population genetic structure at 50 m depth in an ecologically important mesophotic‐specialist species Agaricia grahamae, among locations in the Southern Caribbean. We also tested for hybridisation with the closely related (but depth‐generalist) species Agaricia lamarcki, within their sympatric depth zone (50 m). In contrast to our expectations, no spatial genetic structure was detected between the reefs of Curaçao and Bonaire (~40 km apart) within A. grahamae. However, cryptic taxa were discovered within both taxonomic species, with those in A. lamarcki (incompletely) partitioned by depth and those in A. grahamae occurring sympatrically (at the same depth). Hybrid analyses and demographic modelling identified contemporary and historical gene flow among cryptic taxa, both within and between A. grahamae and A. lamarcki. These results (1) indicate that spatial connectivity and subsequent replenishment may be possible between islands of moderate geographic distances for A. grahamae, an ecologically important mesophotic species, (2) that cryptic taxa occur in the mesophotic zone and environmental selection along shallow to mesophotic depth gradients may drive divergence in depth‐generalists such as A. lamarcki, and (3) highlight that gene flow links taxa within this relativity diverse Caribbean genus.

Coral reefs across the world are undergoing rapid deterioration, and understanding the ecological and evolutionary processes that govern these ecosystems is critical to our ability to protect them. Molecular ecological studies have been instrumental in advancing such understanding, and while initially focused primarily on broad-scale patterns, they have gradually uncovered the prevalence of local genetic structuring. Genome-wide sequencing approaches have provided new opportunities to understand both neutral and adaptive contributions to this largely unexplained diversity, but fine-scale assessments have been hampered by challenges associated with aquatic environments, in terms of (geo)referencing, seafloor characterization, and in situ phenotyping. Here, we discuss the potential of “reefscape genomics,” leveraging recent advances in underwater imaging to enable spatially explicit genomic studies on coral reefs. More specifically, we consider how (close-range) photogrammetry approaches enable (1) fine-scale spatial mapping of benthic target organisms, (2) repeatable characterization of the abiotic and biotic reefscape, and (3) simultaneous in situ mass-phenotyping. The spatially explicit consideration of genomic data –combined with detailed environmental and phenotypic characterization– opens up the opportunity for fine-scale landscape genomic approaches on coral reefs (and other marine ecosystems). Such approaches enable assessment of the spatio-temporal drivers and adaptive potential of the extensive genetic structuring and cryptic diversity encountered in benthic invertebrates, such as reef-building corals. Considering the threats that coral reefs are facing worldwide, we believe that reefscape genomics represents a promising advancement of our molecular ecological toolkit to help inform how we can most effectively conserve and restore coral reef ecosystems into the future.

Background Mesophotic coral communities are increasingly gaining attention for the unique biological diversity they host, exemplified by the numerous mesophotic fish species that continue to be discovered. In contrast, many of the photosynthetic scleractinian corals observed at mesophotic depths are assumed to be depth-generalists, with very few species characterised as mesophotic-specialists. This presumed lack of a specialised community remains largely untested, as phylogenetic studies on corals have rarely included mesophotic samples and have long suffered from resolution issues associated with traditional sequence markers. Results Here, we used reduced-representation genome sequencing to conduct a phylogenomic assessment of the two dominant mesophotic genera of plating corals in the Indo-Pacific and Western Atlantic, respectively, Leptoseris and Agaricia. While these genome-wide phylogenies broadly corroborated the morphological taxonomy, they also exposed deep divergences within the two genera and undescribed diversity across the current taxonomic species. Five of the eight focal species consisted of at least two sympatric and genetically distinct lineages, which were consistently detected across different methods. Conclusions The repeated observation of genetically divergent lineages associated with mesophotic depths highlights that there may be many more mesophotic-specialist coral species than currently acknowledged and that an urgent assessment of this largely unstudied biological diversity is warranted.