Population connectivity and genetic offset in the spawning coral Acropora digitifera in Western Australia

Abstract

Anthropogenic climate change has caused widespread loss of species biodiversity and ecosystem productivity across the globe, particularly on tropical coral reefs. Predicting the future vulnerability of reef-building corals, the foundation species of coral reef ecosystems, is crucial for cost-effective conservation planning in the Anthropocene. In this study, we combine regional population genetic connectivity and seascape analyses to explore patterns of genetic offset (the mismatch of gene-environmental associations under future climate conditions) in Acropora digitifera across 12 degrees of latitude in Western Australia. Our data revealed a pattern of restricted gene flow and limited genetic connectivity among geographically distant reef systems. Environmental association analyses identified a suite of loci strongly associated with the regional temperature variation. These loci helped forecast future genetic offset in gradient forest and generalized dissimilarity models. These analyses predicted pronounced differences in the response of different reef systems in Western Australia to rising temperatures. Under the most optimistic future warming scenario (RCP 2.6), we predicted a general pattern of increasing genetic offset with latitude. Under the extreme climate scenario (RCP 8.5 in 2090-2100), coral populations at the Ningaloo World Heritage Area were predicted to experience a higher mismatch between current allele frequencies and those required to cope with local environmental change, compared to populations in the inshore Kimberley region. The study suggests complex and spatially heterogeneous patterns of climate-change vulnerability in coral populations across Western Australia, reinforcing the notion that regionally tailored conservation efforts will be most effective at managing coral reef resilience into the future.

Keywords: North-west Australia; broadcast corals; climate change; gene-environmental associations; population genetics.

FIGURE 1

Map showing the 32 sites (red circles) sampled across five reef systems; (a) Ningaloo Coast World Heritage Area, (b) Rowley Shoals, (c) inshore Kimberley, (d) Ashmore Reef, (e) Pelorus Island, GBR

FIGURE 2

Population connectivity results. (a) Neighbour‐joining tree of all sites (labels correspond to sites which can be found in Table S1) in WA (except at Lalang‐garram Marine Park reefs) and Pelorus Island (GBR), segregating offshore NW shelf populations from Pelorus Island and inshore Kimberley populations. (b) DAPC without Pelorus Island genotypes. (c) fastSTRUCTURE admixture plot using only WA genotype data (except Lalang‐garram Marine Park genotypes) with optimal K clustering (K = 4) that best describes the population structure of the SNP data (using chooseK function). Colours correspond to reef system membership: Ashmore Reef (red), Inshore Kimberley (dark green), Rowley Shoals (grey), Ningaloo World Heritage Area (blue) and Great Barrier Reef (pink)

FIGURE 3

Gradient forest analysis. (a) PCA plot showing the similarity in gene‐environmental associations within the 50 km buffer zone of the sampled sites in RGB combination (red, green and blue are assigned using PC1, PC2 and PC3 combinations) using the final GF model. In this plot, the more similar the colours, the more similar areas, that neighbour sampled sites, are in terms of genetic composition with those sample sites. Vectors represent the direction and magnitude of the five most explanatory variables (SSTrange, Tidal height, SSTmax, SSTA and Bathymetry in decreasing order). Small black circles represent site locations encircled by reefs. From left to right (green – Adele Island, black – Beagle Reef (inshore Kimberley), red – Ashmore Reef, grey – Imperieuse, Clerke and Mermaid Reef (Rowley Shoals), dark blue – Ningaloo Stations, magenta – Gnaraloo, yellow – Quobba (Ningaloo Coast World Heritage Area). The N/S arrow on the right represents the latitudinal variation in genetic similarity in the Ningaloo Coast World Heritage Area as a result of the SSTrange gradient along the coastline. (b) Line plots show the trend in cumulative importance of the five most important variables to the variable distribution. (c) Notched boxplots representing the variability in the genetic offset, represented by the Euclidean distance between present‐day and future genetic composition, across reef systems in WA under RCP 2.6 and RCP 8.5 in 2040–2050 and 2090–2100 (predicted by the gradient forest model). Red circles represent mean values while black dots represent outliers

FIGURE 4

Genetic offset raster predictions, represented by the Euclidean distance between present‐day and future genetic composition, across the four reef systems in WA under RCP 2.6 climate conditions in 2040–2050, predicted using the GF model. Ningaloo Coast World Heritage Area (a), Rowley Shoals (b), inshore Kimberley (c) and Ashmore Reef (d)