Deep connections: Divergence histories with gene flow in mesophotic Agaricia corals

Abstract

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.

Global phylogenomic assessment of Leptoseris and Agaricia reveals substantial undescribed diversity at mesophotic depths

“…This structure was consistently recovered across phylogenetic and clustering methods and often corresponded to different depths and/or geographic regions, indicating the role of both environmental and geographical (i.e., allopatric) contributors to the underlying diversification processes. Our analyses included four focal species previously assessed in population genomic studies with varying levels of intraspecific genetic structure [3, 37, 53]. Through a combined phylogenomic analysis, we were able to assess this genetic structuring in the context of interspecific variation.…”

“…For example, despite the genome-wide differentiation observed for shallow and deep A. fragilis populations in Bermuda [3], representative specimens of those populations formed a single clade here (i.e., under a phylogenomic framework), indicating that these reflect the earlier stages of the divergence continuum. In contrast, the A. lamarcki samples clearly separated into two distinct clades associated with predominantly shallower (15 m) and upper mesophotic (50 m) depths (figure 2b) despite their geographically sympatric distribution and ongoing low levels of gene flow [53], and clearly represent distinct evolutionary units. Similarly, we observed four distinct clades of A. grahamae occurring sympatrically in Curaçao and Bonaire with varying levels of divergence (figure 2b), and while not partitioned by depth, it indicates undescribed mesophotic taxa that are currently not accounted for.…”

“…Additional tissue samples were acquired from collaborators in the Hawaiian Archipelago, US Minor Outlying Islands, Gulf of Aqaba (Red Sea), San Andrés Island, Cartagena, and Santa Marta (Colombia). The Agaricia dataset includes nextRAD sequence data (n = 52) from three published datasets [3, 37, 53], and we also included Stephanocoenia intersepta (n = 3 [3]), Helioseris cucullata (n = 5), and Pachyseris speciosa (n = 3 [55]) samples to serve as outgroups (table S1).…”

“…Based on a morphological analysis of modern and fossil representatives, Stemann [79] proposed these should represent two separate genera: Agaricia and Undaria [80]. Recent differences in spatial genetic structure observed across taxa further suggest major differences in reproductive strategies between these major clades [53]. Given the major phylogenetic divergence observed in this study (figure 2b), and further corroborated by the major locus dropout between clades (figure S2), we argue that the shallower and deeper Agaricia indeed represent two genetically, morphologically, and biologically divergent groups that might require generic reassignment.…”

“…Reduced-representation genome sequencing methods (e.g., sequencing of restriction siteassociated DNA (RAD-seq) or ultra-conserved elements (UCEs)) have demonstrated their potential to overcome these issues, resulting in phylogenies that have strong support (e.g., [48][49][50][51][52]), providing a promising way forward to study the evolutionary relationships within the Agariciidae. The increased resolution of such reduced representation methods was demonstrated through recent population genomics studies of Agaricia species, revealing significant genetic structuring within all four species dominating Atlantic mesophotic communities [3,37,53,54].…”