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, 121 (6), 524-536

Unexpected Mixed-Mode Transmission and Moderate Genetic Regulation of Symbiodinium Communities in a Brooding Coral

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Unexpected Mixed-Mode Transmission and Moderate Genetic Regulation of Symbiodinium Communities in a Brooding Coral

Kate M Quigley et al. Heredity (Edinb).

Abstract

Determining the extent to which Symbiodinium communities in corals are inherited versus environmentally acquired is fundamental to understanding coral resilience and to predicting coral responses to stressors like warming oceans that disrupt this critical endosymbiosis. We examined the fidelity with which Symbiodinium communities in the brooding coral Seriatopora hystrix are vertically transmitted and the extent to which communities are genetically regulated, by genotyping the symbiont communities within 60 larvae and their parents (9 maternal and 45 paternal colonies) using high-throughput sequencing of the ITS2 locus. Unexpectedly, Symbiodinium communities associated with brooded larvae were distinct from those within parent colonies, including the presence of types not detected in adults. Bayesian heritability (h2) analysis revealed that 33% of variability in larval Symbiodinium communities was genetically controlled. Results highlight flexibility in the establishment of larval symbiont communities and demonstrate that symbiont transmission is not exclusively vertical in brooding corals. Instead, we show that Symbiodinium transmission in S. hystrix involves a mixed-mode strategy, similar to many terrestrial invertebrate symbioses. Also, variation in the abundances of common Symbiodinium types among adult corals suggests that microhabitat differences influence the structure of in hospite Symbiodinium communities. Partial genetic regulation coupled with flexibility in the environmentally acquired component of Symbiodinium communities implies that corals with vertical transmission, like S. hystrix, may be more resilient to environmental change than previously thought.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1
Nonmetric multidimensional scaling (NMDS) Split Biplot, based on a Bray–Curtis distance matrix of variance-normalized OTU abundances and sequence similarity between OTUs (pairwise percent identities), illustrating differences between Symbiodinium communities associated with adult colonies and larvae of the brooding coral Seriatopora hystrix (ShA) based on parentage analysis. Ellipses encircling symbols of the corresponding color represent 95% probability regions for adults (black) and larval broods (colored), where each brood represents all larvae sharing the same dam (color-coded). Samples and OTUs have been separated to increase Biplot clarity whilst maintaining ellipse positions to facilitate comparisons of ordination space between samples and OTU positions. a Each point represents the Symbiodinium community associated with a unique coral adult or larval sample. b Each point represents an OTU colored by type level. Only 83 of the 161 OTUs are shown, representing those OTUs with the greatest taxonomic confidence (see Table S7 for full names and selection criteria). Outlining around each point represents the origin of the OTU, i.e., those found uniquely in adult (gray outline) or larval (broken gray outline) samples, or retrieved from both (black outline). Samples presented in a and OTUs presented in b share the same ordination space but were separated for clarity. c Venn diagram, illustrating the number of Symbiodinium OTU’s that were unique to larvae (dark gray text) versus adults (light gray text). The number of OTUs that were significant after p-adjustments are in parentheses. Ellipses corresponding to dams 3 and 10 are not represented, as only one larva per dam was collected and sequenced
Fig. 2
Fig. 2
Barplots of variance-normalized abundances of Symbiodinium diversity associated with a adults and b planula larvae of Seriatopora hystrix. Colors represent different Symbiodinium types. Numbers below planulae barplots represent the different broods
Fig. 3
Fig. 3
a Log2 fold change in abundances of Symbiodinium OTU’s that differed significantly between communities associated with adults versus larvae of Seriatopora hystrix (ShA). Gray-scale in the bar plot identify Symbiodinium clades. A positive change indicates the OTU is more abundant in adults. b Boxplots showing medians, quartiles, and minimum/maximum values of Symbiodinium community diversity (Leinster and Cobbold metric) in relation to individual larval relatedness. On the x-axis, 0.25 denotes half sibs, 0.5 full sibs, and 1.0 denotes larvae produced from selfing. Each larva is colored by its respective dam. c Network analysis of planula larvae showing OTUs present in 50% or more of larvae per brood. Edges have been removed for OTUs found in 100% of larvae from each brood (OTUs:1, 2, 3, 5, 8, 10, 12, 23, 105, 134, and 165). White diamonds correspond to maternal broods, where each brood sharing the same dam is color-coded. Small numbers next to each node indicate the OTU number for that Symbiodinium type. Line thickness denotes relative abundance of the Symbiodinium type per brood
Fig. 4
Fig. 4
Spatial patterns in the normalized abundance of three Symbiodinium OTU’s associated with adult colonies of Seriatopora hystrix (ShA) that differed significantly in their abundances across a portion of the 16 m × 40 m sampling area at Lizard Island. Positions of the 45 genotyped adult colonies are denoted by black circles. a C120/C120a, b D1, and c D1a. Colors represent changes in the normalized abundance of each OTU across sampling site coordinates, with yellow representing the highest abundance and blue the lowest. Sizes of the black circles represent size classes of coral colonies in cm drawn to scale of the sampling area (smallest circles are 10 cm and the largest are 30 cm)

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