Genome-wide assessment reveals opposing patterns of vertical connectivity in two depth-generalist coral species.
BackgroundCoral reefs are hotspots of biodiversity, yet processes of diversification in these ecosystems are poorly understood. The environmental heterogeneity of coral reef environments could be an important contributor to diversification, however, evidence supporting ecological speciation in corals is sparse. Here, we present data from a widespread coral species that reveals a strong association of host and symbiont lineages with specific habitats, consistent with distinct, sympatric gene pools that are maintained through ecologically-based selection.Methodology/Principal FindingsPopulations of a common brooding coral, Seriatopora hystrix, were sampled from three adjacent reef habitats (spanning a ∼30 m depth range) at three locations on the Great Barrier Reef (n = 336). The populations were assessed for genetic structure using a combination of mitochondrial (putative control region) and nuclear (three microsatellites) markers for the coral host, and the ITS2 region of the ribosomal DNA for the algal symbionts (Symbiodinium). Our results show concordant genetic partitioning of both the coral host and its symbionts across the different habitats, independent of sampling location.Conclusions/SignificanceThis study demonstrates that coral populations and their associated symbionts can be highly structured across habitats on a single reef. Coral populations from adjacent habitats were found to be genetically isolated from each other, whereas genetic similarity was maintained across similar habitat types at different locations. The most parsimonious explanation for the observed genetic partitioning across habitats is that adaptation to the local environment has caused ecological divergence of distinct genetic groups within S. hystrix.
BackgroundScleractinian corals and their algal endosymbionts (genus Symbiodinium) exhibit distinct bathymetric distributions on coral reefs. Yet, few studies have assessed the evolutionary context of these ecological distributions by exploring the genetic diversity of closely related coral species and their associated Symbiodinium over large depth ranges. Here we assess the distribution and genetic diversity of five agariciid coral species (Agaricia humilis, A. agaricites, A. lamarcki, A. grahamae, and Helioseris cucullata) and their algal endosymbionts (Symbiodinium) across a large depth gradient (2-60 m) covering shallow to mesophotic depths on a Caribbean reef.ResultsThe five agariciid species exhibited distinct depth distributions, and dominant Symbiodinium associations were found to be species-specific, with each of the agariciid species harbouring a distinct ITS2-DGGE profile (except for a shared profile between A. lamarcki and A. grahamae). Only A. lamarcki harboured different Symbiodinium types across its depth distribution (i.e. exhibited symbiont zonation). Phylogenetic analysis (atp6) of the coral hosts demonstrated a division of the Agaricia genus into two major lineages that correspond to their bathymetric distribution (“shallow”: A. humilis / A. agaricites and “deep”: A. lamarcki / A. grahamae), highlighting the role of depth-related factors in the diversification of these congeneric agariciid species. The divergence between “shallow” and “deep” host species was reflected in the relatedness of the associated Symbiodinium (with A. lamarcki and A. grahamae sharing an identical Symbiodinium profile, and A. humilis and A. agaricites harbouring a related ITS2 sequence in their Symbiodinium profiles), corroborating the notion that brooding corals and their Symbiodinium are engaged in coevolutionary processes.ConclusionsOur findings support the hypothesis that the depth-related environmental gradient on reefs has played an important role in the diversification of the genus Agaricia and their associated Symbiodinium, resulting in a genetic segregation between coral host-symbiont communities at shallow and mesophotic depths.
The composition, ecology and environmental conditions of mesophotic coral ecosystems near the lower limits of their bathymetric distributions remain poorly understood. Here we provide the first in-depth assessment of a lower mesophotic coral community (60–100 m) in the Southern Caribbean through visual submersible surveys, genotyping of coral host-endosymbiont assemblages, temperature monitoring and a growth experiment. The lower mesophotic zone harbored a specialized coral community consisting of predominantly Agaricia grahamae, Agaricia undata and a “deep-water” lineage of Madracis pharensis, with large colonies of these species observed close to their lower distribution limit of ~90 m depth. All three species associated with “deep-specialist” photosynthetic endosymbionts (Symbiodinium). Fragments of A. grahamae exhibited growth rates at 60 m similar to those observed for shallow Agaricia colonies (~2–3 cm yr−1), but showed bleaching and (partial) mortality when transplanted to 100 m. We propose that the strong reduction of temperature over depth (Δ5°C from 40 to 100 m depth) may play an important contributing role in determining lower depth limits of mesophotic coral communities in this region. Rather than a marginal extension of the reef slope, the lower mesophotic represents a specialized community, and as such warrants specific consideration from science and management.
Our rapidly warming climate is threatening coral reefs as thermal anomalies trigger mass coral bleaching events. Deep (or “mesophotic”) coral reefs are hypothesised to act as major ecological refuges from mass bleaching, but empirical assessments are limited. We evaluated the potential of mesophotic reefs within the Great Barrier Reef (GBR) and adjacent Coral Sea to act as thermal refuges by characterising long-term temperature conditions and assessing impacts during the 2016 mass bleaching event. We found that summer upwelling initially provided thermal relief at upper mesophotic depths (40 m), but then subsided resulting in anomalously warm temperatures even at depth. Bleaching impacts on the deep reefs were severe (40% bleached and 6% dead colonies at 40 m) but significantly lower than at shallower depths (60–69% bleached and 8–12% dead at 5-25 m). While we confirm that deep reefs can offer refuge from thermal stress, we highlight important caveats in terms of the transient nature of the protection and their limited ability to provide broad ecological refuge.
The role of symbiont variation in the photobiology of reef corals was addressed by investigating the links among symbiont genetic diversity, function and ecological distribution in a single host species, Madracis pharensis. Symbiont distribution was studied for two depths (10 and 25 m), two diVerent light habitats (exposed and shaded) and three host colour morphs (brown, purple and green). Two Symbiodinium genotypes were present, as deWned by nuclear internal transcribed spacer 2 ribosomal DNA (ITS2-rDNA) variation. Symbiont distribution was depthand colour morph-dependent. Type B15 occurred predominantly on the deeper reef and in green and purple colonies, while type B7 was present in shallow environments and brown colonies. DiVerent light microhabitats at Wxed depths had no eVect on symbiont presence. This ecological distribution suggests that symbiont presence is potentially driven by light spectral niches. A reciprocal depth transplantation experiment indicated steady symbiont populations under environment change. Functional parameters such as pigment composition, chlorophyll a Xuorescence and cell densities were measured for 25 m and included in multivariate analyses. Most functional variation was explained by two photobiological assemblages that relate to either symbiont identity or light microhabitat, suggesting adaptation and acclimation, respectively. Type B15 occurs with lower cell densities and larger sizes, higher cellular pigment concentrations and higher peridinin to chlorophyll a ratio than type B7. Type B7 relates to a larger xanthophyll-pool size. These unambiguous diVerences between symbionts can explain their distributional patterns, with type B15 being potentially more adapted to darker or deeper environments than B7. Symbiont cell size may play a central role in the adaptation of coral holobionts to the deeper reef. The existence of functional diVerences between B-types shows that the clade classiWcation does not necessarily correspond to functional identity. This study supports the use of ITS2 as an ecological and functionally meaningful marker in Symbiodinium.
Despite a growing interest in mesophotic coral ecosystems (MCEs), information on the photosynthetic endosymbionts (genus Symbiodinium) associated with scleractinian corals inhabiting deep reef ecosystems is sparse. Here, the deep-water Symbiodinium diversity is assessed from 10 different coral genera at a depth range of 45 to 70 m on the Great Barrier Reef (GBR), Australia. Symbiodinium identity was established using denaturing gradient gel electrophoresis (DGGE) fingerprinting of the internal transcribed spacer region 2 (ITS2) of the ribosomal DNA. Except for the novel Symbiodinium type C131 (found in Porites), all Symbiodinium types have previously been identified in shallow reef corals across the Pacific. Specimens of Seriatopora, Montipora, and Porites harboured similar symbionts as reported in shallow water (e.g. C3n, C3n-hh, C15, and C17), thus adhering to patterns of host-specificity across a wide depth range. However, several other Symbiodinium types were found to transcend previously established patterns of host-specificity at mesophotic depths. For example, 'host-specialist' types C3i and C3k (previously only reported in Acropora spp.) were found here to associate with a range of different genera (Leptoseris, Pachyseris, Fungia, and Echinophyllia). Although limited in sample size, this preliminary survey indicates that mesophotic habitats on the GBR may not represent an isolated community in terms of Symbiodinium diversity, which has significant relevance to their potential to act as refugia. Moreover, the present study identifies the need to examine symbiont diversity across broad environmental ranges (including MCEs) in order to gain an accurate understanding of symbiosis specificity and distribution range of specific coral-Symbiodinium associations. KEY WORDS: Symbiodinium · Mesophotic · Deep reefs · Coral · ITS2 · DGGE · Great Barrier ReefResale or republication not permitted without written consent of the publisher Mar Ecol Prog Ser 439: 117-126, 2011 118 zation of Symbiodinium into cladal (e.g. Rowan & Powers 1991, Baker & Rowan 1997 and subcladal types (e.g. van Oppen et al. 2001, LaJeunesse 2002 has greatly enhanced our understanding of the symbiosis. Studies of Symbiodinium diversity on broad latitudinal or longitudinal gradients have shown distinct biogeographical patterns (e.g. LaJeunesse et al. 2003, Silverstein et al. 2011), whereas more local or species-specific studies have highlighted ecological zonation, physiological diversification, and host-specificity of distinct symbionts (e.g. Rowan & Knowlton 1995, LaJeunesse et al. 2003, 2004, Iglesias-Prieto et al. 2004, Sampayo et al. 2007, Frade et al. 2008a.Community-wide shifts in symbiont diversity occur with increasing depth (LaJeunesse 2002, LaJeunesse et al. 2003, 2004, but this observation is likely to be, in part, the result of host community composition changes over depth. Nonetheless, studies focusing on single coral species show a similar pattern, and depth zonation of symbionts has been shown to occur on a cladal...
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