Seascape genomics as a new tool to empower coral reef conservation strategies: An example on north-western Pacific Acropora digitifera

Abstract

Coral reefs are suffering a major decline due to the environmental constraints imposed by climate change. Over the last 20 years, three major coral bleaching events occurred in concomitance with anomalous heatwaves, provoking a severe loss of coral cover worldwide. The conservation strategies for preserving reefs, as they are implemented now, cannot cope with global climatic shifts. Consequently, researchers are advocating for preservation networks to be set-up to reinforce coral adaptive potential. However, the main obstacle to this implementation is that studies on coral adaption are usually hard to generalize at the scale of a reef system. Here, we study the relationships between genotype frequencies and environmental characteristics of the sea (seascape genomics), in combination with connectivity analysis, to investigate the adaptive potential of a flagship coral species of the Ryukyu Archipelago (Japan). By associating genotype frequencies with descriptors of historical environmental conditions, we discovered six genomic regions hosting polymorphisms that might promote resistance against heat stress. Remarkably, annotations of genes in these regions were consistent with molecular roles associated with heat responses. Furthermore, we combined information on genetic and spatial distances between reefs to predict connectivity at a regional scale. The combination of these results portrayed the adaptive potential of this population: we were able to identify reefs carrying potential heat stress adapted genotypes and to understand how they disperse to neighbouring reefs. This information was summarized by objective, quantifiable and mappable indices covering the whole region, which can be extremely useful for future prioritization of reefs in conservation planning. This framework is transferable to any coral species on any reef system and therefore represents a valuable tool for empowering preservation efforts dedicated to the protection of coral reefs in warming oceans.

Keywords: Acropora digitifera; Ryukyu Archipelago; climate change; conservation genomics; coral bleaching; coral reefs; local adaptation; seascape genomics.

Figure 1

Study area. The Ryukyu Archipelago extends for more than 1,000 km in the north‐western Pacific Ocean. The red circles display the 11 sites where samples were collected for the seascape genomics analysis (adapted from Shinzato et al., 2015)

Figure 2

Workflow between the steps of the approach. The starting point for the analysis is the generation of genetic data describing the genotypes observed at different sampling locations (in this example, 4 sampling sites). In the seascape genomics analysis (a), these data are combined with environmental information to uncover genotypes whose frequencies are associated with specific climatic conditions (ENV). Such genotypes are defined as potentially adaptive against the environmental condition of interest. The model describing this link is then applied to environmental data at the scale of the whole reef system (b), to predict the probability of presence of the adaptive genotypes (green: high probability; red: low probability). The genetic data are also combined with sea current information to build a connectivity model (c) describing how sea distances correspond to genetic separation between sampling sites. This model is fitted with sea distance between all the reefs of the study area to predict (d) patterns of connectivity from (outbound) and to (inbound) each reef (green: high connectivity; red: low connectivity). Finally, predictions of the presence of adaptive genotypes and connectivity patterns are combined to assess the adaptive potential across the study area (e): reefs that are connected with sites that are likely to carry the adaptive genotype will have a higher adaptive potential (green), while those that are isolated will have lower adaptive potential (red)

Figure 3

Calculation of connectivity and adaptive potential indices. The three maps display a hypothetical seascape with seven reefs (in rose) of different extent and connected by sea current flowing from left to right (large light blue arrow). On each map, a different index is calculated for the same focal reef (highlighted in red): (a) outbound connectivity index (OCI), (b) inbound connectivity index (ICI) and (c) adaptive potential index (API). The black arrows display the estimated directional genetic separation (dF_ST) for corals travelling from (a) and towards (b, c) the focal reef. The calculation of the indices requires that a threshold value for dFst is set (in this example, T(dFst)=0.002, the green border) in order to define the reefs neighbouring the focal one. OCI (a) represents the total area (in km²) of neighbouring reefs (destinations) that can be reached from the focal reef (departure). ICI (b) represents the total area of neighbouring reefs (departures) that can reach the focal reef (destination). API (c) is a special case of ICI, where the area of the neighbouring reefs is weighted by their probability of presence of adapted genotypes (PA)

Figure 4

Probability of carrying heat stress adapted genotypes ( ${\text{PA}}_{\text{heat}}$ ). The map shows the probability of presence of the genotypes expected to be linked to adaptation against heat stress across the study area and the neighbouring regions. Seven significant gene–environment associations (SGEA1, 3, 5–8 and 13, Table 1) describing the association between distinct genotypes and bleaching alert frequency were used to predict expected genotype frequencies. These expected frequencies were then averaged to compute the cumulated probability of adaptive genotypes. The dashed box highlights the position of the Ryukyu Archipelago

Figure 5

Connectivity indices. The maps show the potential connectivity to (a) and from (b) every reef of the Ryukyu Archipelago. In (a), the inbound connectivity index (ICI) represents the total area (in km²) of the reefs that are connected to the focal reef with a dF_ST < 0.02 (dF_ST towards the focal reef). Reefs with a high ICI are expected to receive recruits from a larger neighbourhood. In (b), the outbound connectivity index (OCI) displays the total area of the reefs that are connected from the focal reef with a dF_ST < 0.02 (dF_ST from the focal reef). Reefs with a high OCI are expected to disperse towards a larger neighbourhood

Figure 6

Index of adaptive potential against heat stress ( ${\text{API}}_{\text{heat}}$ ). The map displays the index of adaptive potential against heat stress (high bleaching alert frequency, BAF) for every reef of the study area. This index represents the sum of weighted areas of reefs connected to the focal reef with a pFst < 0.02 (pFst towards the focal reef). The weight applied corresponds to the probability of carrying heat stress adapted genotypes ( ${\text{PA}}_{\text{heat}}$ ). Reefs with a large API are expected to receive more heat stress adapted recruits