Evidence for adaptive morphological plasticity in the Caribbean coral, Acropora cervicornis

Abstract

Genotype-by-environment interactions (GxE) indicate that variation in organismal traits cannot be explained by fixed effects of genetics or site-specific plastic responses alone. For tropical coral reefs experiencing dramatic environmental change, identifying the contributions of genotype, environment, and GxE on coral performance will be vital for both predicting persistence and developing restoration strategies. We quantified the impacts of G, E, and GxE on the morphology and survival of the endangered coral, Acropora cervicornis, through an in situ transplant experiment exposing common garden (nursery)-raised clones of ten genotypes to nine reef sites in the Florida Keys. By fate-tracking outplants over one year with colony-level 3D photogrammetry, we uncovered significant GxE on coral size, shape, and survivorship, indicating that no universal winner exists in terms of colony performance. Rather than differences in mean trait values, we found that individual-level morphological plasticity is adaptive in that the most plastic individuals also exhibited the fastest growth and highest survival. This indicates that adaptive morphological plasticity may continue to evolve, influencing the success of A. cervicornis and resulting reef communities in a changing climate. As focal reefs are active restoration sites, the knowledge that variation in phenotype is an important predictor of performance can be directly applied to restoration planning. Taken together, these results establish A. cervicornis as a system for studying the ecoevolutionary dynamics of phenotypic plasticity that also can inform genetic- and environment-based strategies for coral restoration.

Keywords: 3D photogrammetry; GxE; fragmentation; growth; survival.

Fig. 1.

Experimental design and environmental conditions (A) Location of outplant sites (SI Appendix, Table S1) and the source restoration nursery in the lower Florida Keys, USA. Ten genets (genotypes) of A. cervicornis sourced from the lower Florida Keys (SI Appendix, Fig. S1) were outplanted in triplicate to nine reef sites in three subarrays. Sites are colored by average survival from dark blue (highest) to dark red (lowest), and the location of site-specific SERC water quality monitoring stations (56) is indicated by the white diamonds. (B) Ramets were reared in the nursery to a mean size of 8 cm and were measured just prior to outplanting in April 2018 (C) To obtain growth and morphology data, still images were captured using underwater photography, which were used to build 3D models in Agisoft Metashape, that were subsequently measured for total linear extension (TLE; example red lines), surface area (SA), volume (V), and volume of the interstitial space (V_inter; example shaded blue area) (D) Average daily temperature of each site (colored by survival rank) for the 1-y experimental period. Inset shows hourly temperatures from July through September 2018. The dashed line indicates the local bleaching threshold of 30.5°C. (E) Principal component analysis of historical SERC environmental metrics characterizing outplant reef sites (Looe Key is excluded due to missing data). PCA loadings can be found in SI Appendix, Fig. S17. (F) Results of a Bayesian negative binomial generalized linear mixed effects model testing the association of eleven uncorrelated environmental parameters on the change in V_inter. Horizontal black lines indicate 95% credible intervals of the posterior distributions. Values above (red) or below (blue) indicate significant association between the variable and the change in V_inter across sites.

Fig. 2.

Genotype, environment, and GxE patterns of survival. (A) Survival probability for genets and (B) sites over the 1-y experimental period. Genets and sites are colored by decreasing overall survival from blue to red. (C) Pairwise correlations of genet survival rank across outplant sites. Asterisks denote significant correlations (Spearman’s correlation, P < 0.05). Ellipse shape and color are proportional to the strength and direction of the correlation, respectively, between two sites. Sites are ordered according to survival as in (B).

Fig. 3.

Average size in total linear extension (TLE) for each genotype (colored by survival probability as in Fig. 2A) over time. Reef sites are also ordered by survival probability (Left to Right).

Fig. 4.

Morphological plasticity and its relationship to growth and survival. (A) Relationship between genet plasticity in final (T12) absolute size and average genet growth rate in TLE over the final 3 mo of the outplant period. Points are colored by genet mortality risk score. Line and shaded region shows line of best fit and 95% confidence interval for each relationship, respectively. (B) Principal component analysis of size-independent morphological traits: sphericity, convexity, packing (58), and SA-to-V ratio and SA-to-TLE ratio (gray vectors labeled in red). Points represent individual ramets colored by genet identity (n = 5–12 ramets per genet) by decreasing survival from blue to red. Shaded regions (colored by survival rank) frame the most extraneous ramets for each genet and outline the morphospace occupied by a genet.