Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance

Abstract

Mutualisms between reef-building corals and endosymbiotic dinoflagellates are particularly sensitive to environmental stress, yet the ecosystems they construct have endured major oscillations in global climate. During the winter of 2008, an extreme cold-water event occurred in the Gulf of California that bleached corals in the genus Pocillopora harbouring a thermally 'sensitive' symbiont, designated Symbiodinium C1b-c, while colonies possessing Symbiodinium D1 were mostly unaffected. Certain bleached colonies recovered quickly while others suffered partial or complete mortality. In most colonies, no appreciable change was observed in the identity of the original symbiont, indicating that these partnerships are stable. During the initial phases of recovery, a third species of symbiont B1(Aiptasia), genetically identical to that harboured by the invasive anemone, Aiptasia sp., grew opportunistically and was visible as light-yellow patches on the branch tips of several colonies. However, this symbiont did not persist and was displaced in all cases by C1b-c several months later. Colonies with D1 were abundant at inshore habitats along the continental eastern Pacific, where seasonal turbidity is high relative to offshore islands. Environmental conditions of the central and southern coasts of Mexico were not sufficient to explain the exclusivity of D1 Pocillopora in these regions. It is possible that mass mortalities associated with major thermal disturbances during the 1997-1998 El Niño Southern Oscillation eliminated C1b-c holobionts from these locations. The differential loss of Pocillopora holobionts in response to thermal stress suggests that natural selection on existing variation can cause rapid and significant shifts in the frequency of particular coral-algal partnerships. However, coral populations may take decades to recover following episodes of severe selection, thereby raising considerable uncertainty about the long-term viability of these communities.

Figure 1.

Recent coral ‘bleaching’ and mortality in the Gulf of California caused by low-water temperatures. (a) Average monthly SSTs for the southern Gulf of California between 2003 and 2007 (black squares) relative to temperatures in 2008 (open circles). The brown and white colour shaded bar at the bottom of the graph indicates the period when colonies bleached and recovered, respectively, and arrows indicate approximate sampling times. (b) A large bleached colony of Pocillopora photographed in May 2008 is surrounded by unbleached colonies in the Gulf of California. (c) Average symbiont cell densities in colonies harbouring either Symbiodinium ‘C1b-c’ or ‘D1’ sampled in May 2008. The coloured circle above the mean value calculated for bleached colonies is the average cell density in colonies harbouring ‘C1b-c’ under normal conditions. Error bars represent 1 s.d. (d) Percentage of Pocillopora colonies harbouring either Symbiodinium ‘C1b-c’ or ‘D1’ that were healthy, bleached, partially dead or entirely dead. The numbers in parentheses above the pie graphs indicate the total number of permanently tagged colonies whose symbiont has been monitored since 2006.

Figure 2.

(a) The genetic identification of Symbiodinium in bleached and recovering colonies using ITS-DGGE rDNA fingerprinting identified three Symbiodinium spp., C1b-c, D1 and B1_Aiptasia. (b) Proportions of tagged bleached colonies with Symbiodinium C1b-c, D1 and/or B1_Aiptasia that were in the early stages of recovery (May 2008), and then four months later (September) when they had recovered completely. (c) Normal patterns of pigmentation in recovering colonies on the sides and bases of branches (grey arrows). (d) The light golden-yellow pigment observed on the apical portion of branches from several unusual colonies containing Symbiodinium B1_Aiptasia (white arrows).

Figure 3.

(a) Geographic patterns in the relative dominance of colonies with Symbiodinium D1 surveyed a decade after the 1997–1998 ENSO. Analyses of individual Pocillopora from (1) The Gulf of California (n = 201); (2) Banderas Bay (n = 179); (3) western Gulf of Tehuantepec, Oaxaca (n = 82); (4) Revillagigedo Archipelago (n = 3); (5) Clipperton Atoll (n = 21); (6) Gulf of Chiriqui (Uva Island), Panama (n = 41; Baker et al. 2004); and (7) Gulf of Panama (n = 42). Loss of live coral cover was most severe among communities of Pocillopora from central (Banderas Bay) and southern Mexico (Gulf of Tehuantepec) sites during the 1997–1998 ENSO (inset modified from Reyes-Bonilla et al. 2002). The average monthly values (±s.d.) between 2003 and 2007 of SSTs (b) and chlorophyll a concentrations (a proxy for turbidity) for each location based on satellite imaging.

Figure 4.

Conceptual representation depicting ranges in the stress responses of two host–symbiont combinations (i.e. holobionts). In the winter of 2007–2008, colonies of Pocillopora with C1b-c in the Gulf of California were more sensitive to thermal stress (e.g. cold water) than colonies with D1. Within each combination, different genotypes of host and symbiont probably influence overall physiological performance. The weakest genotypic combinations among ‘C1b-c' and ‘D1' holobionts suffered partial (grey shading) or total mortality (black). Only the most tolerant genotypic combinations might survive severe episodes of physiological stress such as the high and prolonged temperatures experienced in Banderas Bay during the 1997–1998 ENSO.