Coral conservation through assisted evolution

Coral reefs occupy a tiny portion of the world’s oceans (see map below) but their biodiversity is hugely disproportionate to their size. More than 450 million people from 109 countries live in close proximity to coral reefs and depend upon the ecosystem services and goods reefs provide, for example, food, tourism, and storm protection. And if their incalculable ecological and economic value isn’t enough to impress you, coral reefs are one of the most beautiful places on the planet.
Unfortunately, like many other incredible ecosystems, coral reefs, and the oceans in general, are in trouble due to a myriad of factors including overfishing, pollution, habitat destruction, ocean warming, and increased acidification (see a striking photographic time series documenting the effects of overfishing here and watch a short video about ocean decline and the problem with shifting baselines here). The map below created in 2011 by the World Resources Institute shows the global distribution of coral reefs with increasingly warmer colors indicating higher local threat levels. One thing to note is that the Great Barrier Reef is mostly blue according to 2011 standards, but recent plans by the Australian government to increase coal production and dredge 100 million tons of sea floor to increase shipping access certainly raise that risk (read more about how current industrial development is threatening the GBR here and here).

When faced with changing conditions, organisms can respond in three ways: i) individuals and populations can shift their ranges and move into more hospitable habitat, ii) individuals can acclimate to current conditions, or iii) populations can adapt. If none of these options are possible, the species is faced with local or global extinction. Corals (and other coral reef taxa) are particularly impacted by anthropogenic change because adults are sessile and dispersal only takes place in the larval phase, many species currently live at the upper limits of their physiological tolerances, leaving little room for further acclimation, and human-mediated changes to the environment are likely happening far more rapidly than populations can respond to through adaptation.
Given the rapid pace of climate change and the (generally) slow pace of evolution, researchers at the Australian Institute of Marine Science and the Hawaii Institute of Marine Biology recently outlined a conservation plan that relies on assisted evolution (i.e. artificial selection) to increase resilience in corals. The article authored by Madeleine van Oppen, James Olivera, Hollie Putnamb, and Ruth Gates is available early online at PNAS. Before I get to the details of the van Oppen et al. perspective, I’ll first give some background information about coral biology and ecology that may make them particularly amenable to assisted evolution.

The little coral polyp you see with your naked eye is actually a unit made up multiple different organisms collectively referred to as the coral holobiont. The coral itself is a cnidarian and within its tissues live bacteria, fungi, archaea, viruses, and most importantly, unicellular algal protists (commonly called zooxanthellae) from the genus Symbiodinium. Corals are heterotrophic, snagging prey that swim by with their cnidocyte-covered tentacles, but the photosynthetic zooxanthellae provide a large source of nutrition to the coral and in return receive a safe home and access to the coral’s metabolic waste (carbon dioxide, nitrogen etc).
Currently 9 clades (A-I) and 8 sub-clades (D1-D2, F2-F5, and G1-G2) of Symbiodinum have been described with variation in their geographic distribution, physiological tolerance, and host-coral association. Some corals host multiple Symbiodinium clades simultaneously and the relative abundance of clades hosted can vary temporally or spatially within a coral colony. Symbiodinium may be passed down vertically from coral parent to offspring in the egg and/or can be obtained by the coral from the environment. When conditions become inhospitable (for example, when waters become too warm), the zooxanthellae leave the coral tissue, resulting in a bleaching event. The pigments of the zooxanthellae give corals their color so when the symbionts leave, the white coral skeleton is clearly visible through the transparent coral polyp tissue. Some bleaching events pass quickly and the corals are able to take up their zooxanthellae again, but severe, prolonged events are often lethal. In the coming decades, the number and severity of bleaching events are expected to increase.

 
 
 
 
 
 
 
 
 
 
Although humans have been genetically modifying plants and animals to increase yields and promote desirable traits in commercially important species for centuries, using artificial selection to increase the resilience of natural populations for conservation efforts is rare. In their 2015 PNAS perspective van Oppen et al. propose the idea of coral conservation through assisted evolution (i.e. artificial selection). Corals have several characteristics that promote their evolvability: “(i) the common occurrence of asexual reproduction in addition to sexual reproduction—some corals brood larvae asexually and others reproduce asexually through fragmentation or colony fission: (ii) a lack of segregation of the germ cell from the somatic cell line [this means any somatic point mutation that occurs over the life of an adult coral can be passed down to its offspring]; (iii) the existence of symbiosis with a range of potentially fast-evolving microbes; and (iv) naturally occurring high levels of genetic diversity and the occurrence of interspecific hybridization in some taxa.” van Oppen et al. initiate a discussion about the risks and benefits of an assisted evolution approach and outline a plan with four approaches.
Approach 1: “stress exposure of natural stock to induce preconditioning acclimatization (i.e., within generations) and transgenerational acclimatization (i.e., between generations) through epigenetic mechanisms”
Research has shown that corals (and other organisms) exposed to a short-term, sub-lethal stressor are more likely to survive a more intense stressor in the future. van Oppen et al. propose here that we investigate approaches where corals preconditioned or hardened to mild or moderate stressors in the lab are transplanted into the field in the hopes that these individuals will be more tolerant to future stressful conditions. These hardening treatments may also induce epigenetic changes that can be passed to future generations. Finally, because the Symbiodinium clade(s) a coral hosts can shift after thermal stress, and Symbiodinium can be passed down from parent to offspring, this transfer of thermotolerant symbionts may act as a sort of transgenerational acclimation.
Approach 2: “the active modification of the community composition of coral-associated microbes (eukaryotic and prokaryotic)”
Many coral larvae are symbiont-free, motivating van Oppen et al. to suggest an approach where lab reared larvae are inoculated with particular Symbiodinium and bacterial strains that will confer stress resistance once transplanted into the field. This idea is particularly promising given its parallels with the successful manipulations of the rhizosphere in terrestrial plants. One potential limitation however, is whether lab produced coral-symbiont associations will remain stable over time.
Approach 3: “selective breeding to generate certain genotypes exhibiting desirable phenotypic traits”
Mixing gene pools within and among closely related species can introduce genetic and phenotypic variation into coral populations. A range of coral species form hybrids, some of which have higher fitness than the parentals. Coral populations have been shown to vary in thermal tolerance and gene flow between tolerant and sensitive populations may facilitate introgression of adaptive alleles among populations. Selective breeding could take place in lab-based breeding programs or through transplantation of adult colonies in the field.
Approach 4: “laboratory evolution of the algal endosymbionts (Symbiodinium spp.) of corals through mutagenesis and/or selection (i.e., evolution after the generation of variability)”
In this approach van Oppen et al. suggest using chemicals or irradiation with UV light or X-rays to induce new mutations to Symbiodinium clades with subsequent selection in the hopes of finding novel strains that confer increased resistance to environmental stress.
There are of course potential concerns with such a conservation plan. For example, the translocation of individuals among populations, the release of lab reared individuals into the field, and the introduction of genetically modified individuals may have unexpected and unintended effects on coral reef ecosystems. And while the plan of van Oppen et al. aims to improve the acclimation and adaptation of corals to increasing temperature and ocean acidification, climate change is only one problem facing coral reefs and, ultimately, tolerant populations need a place to live. Nevertheless, I have hope for coral reefs and appreciate efforts like those of van Oppen et al. that propose areas of new research and initiate important discussions about conservation strategies for coral reefs.
References
van Oppen, M. J., Oliver, J. K., Putnam, H. M., & Gates, R. D. (2015). Building coral reef resilience through assisted evolution. Proceedings of the National Academy of Sciences. DOI: 10.1073/pnas.1422301112
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Barshis, D. J., Ladner, J. T., Oliver, T. A., Seneca, F. O., Traylor-Knowles, N., & Palumbi, S. R. (2013). Genomic basis for coral resilience to climate change. Proceedings of the National Academy of Sciences, 110(4), 1387-1392. DOI: 10.1073/pnas.1210224110
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