Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type

Abstract

Coral bleaching has been identified as one of the major contributors to coral reef decline, and the occurrence of different symbionts determined by broad genetic groupings (clades A-H) is commonly used to explain thermal responses of reef-building corals. By using Stylophora pistillata as a model, we monitored individual tagged colonies in situ over a two-year period and show that fine level genetic variability within clade C is correlated to differences in bleaching susceptibility. Based on denaturing gradient gel electrophoresis of the internal transcribed spacer region 2, visual bleaching assessments, symbiont densities, host protein, and pulse amplitude modulated fluorometry, we show that subcladal types C78 and C8/a are more thermally tolerant than C79 and C35/a, which suffered significant bleaching and postbleaching mortality. Although additional symbiont types were detected during bleaching in colonies harboring types C79 and C35/a, all colonies reverted back to their original symbionts postbleaching. Most importantly, the data propose that the differential mortality of hosts harboring thermally sensitive versus resistant symbionts rather than symbiont shuffling/switching within a single host is responsible for the observed symbiont composition changes of coral communities after bleaching. This study therefore highlights that the use of broad cladal designations may not be suitable to describe differences in bleaching susceptibility, and that differential mortality results in a loss of both symbiont and host genetic diversity and therefore represents an important mechanism in explaining how coral reef communities may respond to changing conditions. climate change ͉ coral reefs ͉ Symbiodinium ͉ zooxanthellae ͉ Stylophora

Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change

“…R. Soc. B 282: 20141725 particular conditions of disturbance and recovery, and that differences in these factors may explain variable reports of symbiont community stability or dynamism in the literature [8,9,[17][18][19][20][21][23][24][25][26]43]. Furthermore, these data illustrate that quantitative community metrics, rather than qualitative identification of the dominant symbiont, are necessary to evaluate symbiont shuffling responses.…”

“…In particular, recovery with heat-tolerant symbionts can increase resistance to future thermal bleaching [8], but at a potential energetic cost [13][14][15][16]. Investigations of the ABH have revealed that, although corals sometimes change their symbionts [8,9,[17][18][19][20][21], this does not always occur: sometimes corals recover with the same symbiont community they had prior to stress [22][23][24][25][26]. These conflicting reports have generated controversy surrounding the ABH and the potential role of partner-switching in coral responses to climate change.…”

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

“…The differential mortality reported by this study is consistent with evidence that most coral colonies maintain long-term stable relationships with specific Symbiodinium sp. even after bleaching (Sampayo et al 2008;Stat et al 2009;Thornhill et al 2009). Indeed, repeated temporal samplings indicate that most partnerships remain stable even when a colony is transplanted to a different habitat and/or experiences stress-induced 'bleaching' (Baker 2001;Goulet & Coffroth 2003;Goulet 2006;Thornhill et al 2006a,b;Jones et al 2008;Sampayo et al 2008).…”

“…While numerous bleaching episodes have occurred in recent decades, rarely have colonies been monitored to determine the actual importance of the resident symbiont to the coral's survival (Glynn et al 2001;Goulet et al 2008;Jones et al 2008;Sampayo et al 2008). For corals exhibiting polymorphic associations with more than one symbiont species, replacement of the dominant symbiont population by a second compatible species can occur when colonies are transplanted to a different environment (Rowan et al 1997;Baker 2001;Berkelmanns & van Oppen 2006).…”

Extensive transcriptional variation poses a challenge to thermal stress biomarker development for endangered corals

“…Due to 44 anthropogenic impacts, disease, and temperature-induced bleaching events, the 45 abundance of this prevalent species has declined by more than 80% in recent decades 46 The health of a coral colony is also tied to the identity and physiological qualities of 76 its dinoflagellate endosymbionts (Sampayo et al 2008). Mature A. cervicornis colonies 77 are typically found to associate with just one Symbiodinium species (S. 'fitti' = ITS2 type 78 A3 Caribbean ) at depths above ten meters (Thornhill et al 2006 expression biomarkers (GEBs), which capture dynamic stress responses, are promising 90 tools for coral restoration (reviewed by Louis et al 2016).…”