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.

Keywords: Scleractinia; cryptic species; isolation with migration; mesophotic; population genetics; spatial connectivity.

FIGURE 1

Sampling locations for collected samples of Agaricia grahamae and A. lamarcki. Samples were collected from Curaçao and Bonaire located in the Southern Carribean, outgroup samples are from San Andrés (top left). Samples of A. grahamae were collected from five sites in Curaçao and three sites in Bonaire and A. lamarcki were collected in four sites in Curaçao: CK, CR, CS and CE (bottom left). Photograph of the two study species (right)

FIGURE 2

ADMIXTURE, NJ‐Tree and PCA results show genetic distinction between species and further substructure within each species. (a) Ancestry proportions with ADMIXTURE analysis of 161 individuals using 1465 unlinked and neutral SNPs (119 Agaricia grahamae and 42 A. lamarcki) for K = 2–4. Each bar on the x‐axis represents an individual and the y‐axis is the proportion of ancestry. Genetic clusters are represented by colours. (b) Neighbour joining tree of the same individuals with 4306 neutral SNPs using genetic distance. Grey individuals represent outliers. (c) PCA of the same individuals using 4306 neutral SNPs displaying PC1 and 2. * indicates the putative hybrid between nominal species

FIGURE 3

ADMIXTURE and PCA results show genetic structure within A. grahamae, these genetic groups occur sympatrically at most sites within Curaçao and Bonaire. (a) Ancestry proportions with ADMIXTURE analysis of 118 individuals using 813 neutral and unlinked SNPs (K = 2–4) for the 10% missing data set. (b) Map of Curaçao and Bonaire indicating the proportion of each cluster at each site. (c) PCA results using SNPs. Site codes consist one letter for region, one letter for site and numbers for depth sampled at, except for SA which combines all sites from outgroup, San Andrés. * indicates the previously found putative hybrid between A. grahamae and A. lamarcki

FIGURE 4

ADMIXTURE and PCA results show genetic substructure within Agaricia lamarcki. Samples were collected from two depth profiles at three sites within Curaçao and one depth in at one site. (a) Ancestry proportions with ADMIXTURE analysis of 41 individuals using 1328 unlinked and neutral SNPs for K = 2. Each bar on the x‐axis represents an individual and the y‐axis is the proportion of ancestry. Genetic clusters are represented by colours. (b) Map of the study sites within Curaçao, pie charts represents the proportion of each genetic cluster found at each site. (c) PCA of the same individuals using 2515 neutral SNPs

FIGURE 5

Demographic analysis for cryptic taxa within species and between species show that divergence with migration is more likely than divergence in isolation. (a) The folded joint allele frequency spectrum (Data), (b) two simulated JAFS from each model (divergence in isolation and divergence with migration) (Model), and (c) their standardised residuals (Model ‐ Data SNPs) are shown for (left panel) A. grahamae taxa (AG1 and AG2) and (right panel) between species (AG2 and AL1). Haplotypes from each population are represented on the x‐ and y‐axes of the JAFS and the colour scale represents the SNP counts corresponding to all haplotype frequency combinations between pairs of populations