Spatially varying selection between habitats drives physiological shifts and local adaptation in a broadcast spawning coral on a remote atoll in Western Australia.

At the Rowley Shoals in Western Australia, the prominent reef flat becomes exposed on low tide and the stagnant water in the shallow atoll lagoons heats up, creating a natural laboratory for characterizing the mechanisms of coral resilience to climate change. To explore these mechanisms in the reef coral Acropora tenuis, we collected samples from lagoon and reef slope habitats and combined whole-genome sequencing, ITS2 metabarcoding, experimental heat stress, and transcriptomics. Despite high gene flow across the atoll, we identified clear shifts in allele frequencies between habitats at relatively small linked genomic islands. Common garden heat stress assays showed corals from the lagoon to be more resistant to bleaching, and RNA sequencing revealed marked differences in baseline levels of gene expression between habitats. Our results provide new insight into the complex mechanisms of coral resilience to climate change and highlight the potential for spatially varying selection across complex coral reef seascapes to drive pronounced ecological divergence in climate-related traits.

Individual haplotyping of whale sharks from seawater environmental DNA.

Population genetic data can provide valuable information on the demography of a species. For rare and elusive marine megafauna, samples for generating the data are traditionally obtained from tissue biopsies, which can be logistically difficult and expensive to collect and require invasive sampling techniques. Analysis of environmental DNA (eDNA) offers an alternative, minimally invasive approach to provide important genetic information. Although eDNA approaches have been studied extensively for species detection and biodiversity monitoring in metabarcoding studies, the potential for the technique to address population-level questions remains largely unexplored. Here, we applied "eDNA haplotyping" to obtain estimates of the intraspecific genetic diversity of a whale shark (Rhincodon typus) aggregation at Ningaloo reef, Australia. Over 2 weeks, we collected seawater samples directly behind individual sharks prior to taking a tissue biopsy sample from the same animal. Our data showed a 100% match between mtDNA sequences recovered in the eDNA and tissue sample for all 28 individuals sampled. In the seawater samples, >97% of all reads were assigned to six dominant haplotypes, and a clear dominant signal (~99% of sample reads) was recovered in each sample. Our study demonstrates accurate individual-level haplotyping from seawater eDNA. When DNA from one individual clearly dominates each eDNA sample, it provides many of the same opportunities for population genetic analyses as a tissue sample, potentially removing the need for tissue sampling. Our results show that eDNA approaches for population-level analyses have the potential to supply critical demographic data for the conservation and management of marine megafauna.

Stress-resistant corals may not acclimatize to ocean warming but maintain heat tolerance under cooler temperatures.

Naturally heat-resistant coral populations hold significant potential for facilitating coral reef survival under rapid climate change. However, it remains poorly understood whether they can acclimatize to ocean warming when superimposed on their already thermally-extreme habitats. Furthermore, it is unknown whether they can maintain their heat tolerance upon larval dispersal or translocation to cooler reefs. We test this in a long-term mesocosm experiment using stress-resistant corals from thermally-extreme reefs in NW Australia. We show that these corals have a remarkable ability to maintain their heat tolerance and health despite acclimation to 3-6 °C cooler, more stable temperatures over 9 months. However, they are unable to increase their bleaching thresholds after 6-months acclimation to + 1 °C warming. This apparent rigidity in the thermal thresholds of even stress-resistant corals highlights the increasing vulnerability of corals to ocean warming, but provides a rationale for human-assisted migration to restore cooler, degraded reefs with corals from thermally-extreme reefs.