Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change

Abstract

Coral communities in the Persian/Arabian Gulf (PAG) withstand unusually high salinity levels and regular summer temperature maxima of up to ∼35°C that kill conspecifics elsewhere. Due to the recent formation of the PAG and its subsequent shift to a hot climate, these corals have had only <6,000 y to adapt to these extreme conditions and can therefore inform on how coral reefs may respond to global warming. One key to coral survival in the world's warmest reefs are symbioses with a newly discovered alga, Symbiodinium thermophilum. Currently, it is unknown whether this symbiont originated elsewhere or emerged from unexpectedly fast evolution catalyzed by the extreme environment. Analyzing genetic diversity of symbiotic algae across >5,000 km of the PAG, the Gulf of Oman, and the Red Sea coastline, we show that S. thermophilum is a member of a highly diverse, ancient group of symbionts cryptically distributed outside the PAG. We argue that the adjustment to temperature extremes by PAG corals was facilitated by the positive selection of preadapted symbionts. Our findings suggest that maintaining the largest possible pool of potentially stress-tolerant genotypes by protecting existing biodiversity is crucial to promote rapid adaptation to present-day climate change, not only for coral reefs, but for ecosystems in general.Persian/Arabian Gulf | adaptation | coral | Symbiodinium | climate change

Rapid adaptive responses to climate change in corals

“…The dinoflagellate genus Symbiodinium contains enormous genetic and functional diversity 71 , and communities associated with corals vary among species, environments and host PERSPECTIVE NATURE CLIMATE CHANGE DOI: 10.1038/NCLIMATE3374 microhabitats 72 . The short generation time of Symbiodinium means that its rate of mutation is much faster than for the coral host 18 , and this, combined with its large within-host population sizes, potentially facilitates rapid responses to altered thermal environments, either through selection of existing genetic variants or through the evolution of novel adaptations 73,74 . Alternatively, the composition of host-associated Symbiodinium communities may vary temporally in response to environmental conditions or at different host lifehistory stages 75 , either through shuffling of existing symbionts 76 or through acquisition of new Symbiodinium types from the environment (that is, switching) 16 .…”

The Future of Coral Reefs Subject to Rapid Climate Change: Lessons from Natural Extreme Environments

“…Extensive research into the biology of corals surviving in the warm waters of the PAG has revealed mechanisms for survival, such as metabolic trade-offs (e.g., reduced fecundity Howells et al, 2016a), and unique physiological and genetic signatures, notably a regionally prevalent heat-specialist algal endosymbiont, Symbiodinium thermophilum Smith et al, 2017a) belonging to a highly diverse ancient group of symbionts cryptically distributed outside the PAG (Hume et al, 2016). S. thermophilum occurs in high temperature, high saline environments, and as such, the benefit of a temperature stressresistant phenotype, comes with a fitness-trade off of existing in high saline systems .…”

“…Such "specialist" restrictions carry critical implications for the ability of naturally stress-resistant corals to cope with future climate change superimposed on already extreme physicochemical conditions. As a consequence, protecting existing biodiversity by maintaining the largest possible pool of potentially stresstolerant genotypes, rather than solely the best adapted genotypes, will be crucial to provide sufficiently diverse genetic material for evolution to act on, and thus promote rapid adaptation to climate change (Hume et al, 2016).…”

Mechanisms of Thermal Tolerance in Reef-Building Corals across a Fine-Grained Environmental Mosaic: Lessons from Ofu, American Samoa

“…Although phenotypic plasticity of the coral animal is one mechanism of acclimatization to environmental stress, the dynamic symbiotic relationship with dinoflagellates of the genus Symbiodinium offers an additional pathway to elevated thermal tolerance (Berkelmans and van Oppen, 2006;Jones et al, 2008;Cooper et al, 2011;Hume et al, 2016). In Ofu, subtle differences in temperature among pools give rise to differences in Symbiodinium communities between habitats, with clade D occurring at higher frequencies in HV pool corals (Oliver and Palumbi, 2010;Palumbi et al, 2014).…”

“…As is the case with the coral host, however, adaptation and acclimatization of the symbiont represent additional pathways to rapid acclimatization and is a rapidly growing area of research (Howells et al, 2011;Baums et al, 2014;Hume et al, 2016).…”