Seascape genomics reveals adaptive divergence in a connected and commercially important mollusc, the greenlip abalone (Haliotis laevigata), along a longitudinal environmental gradient

Abstract

Populations of broadcast spawning marine organisms often have large sizes and are exposed to reduced genetic drift. Under such scenarios, strong selection associated with spatial environmental heterogeneity is expected to drive localized adaptive divergence, even in the face of connectivity. We tested this hypothesis using a seascape genomics approach in the commercially important greenlip abalone (Haliotis laevigata). We assessed how its population structure has been influenced by environmental heterogeneity along a zonal coastal boundary in southern Australia linked by strong oceanographic connectivity. Our data sets include 9,109 filtered SNPs for 371 abalones from 13 localities and environmental mapping across ~800 km. Genotype-environment association analyses and outlier tests defined 8,786 putatively neutral and 323 candidate adaptive loci. From a neutral perspective, the species is better represented by a metapopulation with very low differentiation (global F = 0.0081) and weak isolation by distance following a stepping-stone model. For the candidate adaptive loci, however, model-based and model-free approaches indicated five divergent population clusters. After controlling for spatial distance, the distribution of putatively adaptive variation was strongly correlated to selection linked to minimum sea surface temperature and oxygen concentration. Around 80 candidates were annotated to genes with functions related to high temperature and/or low oxygen tolerance, including genes that influence the resilience of abalone species found in other biogeographic regions. Our study includes a documented example about the uptake of genomic information in fisheries management and supports the hypothesis of adaptive divergence due to coastal environmental heterogeneity in a connected metapopulation of a broadcast spawner.

Geographic isolation and larval dispersal shape seascape genetic patterns differently according to spatial scale

“…Sandoval‐Castillo et al. (2018) provided an example of marine genomic and connectivity information being directly used by a government for management and conservation purposes.…”

“…A recent study based on SNPs genotyping of the greenlip abalone ( Haliotis laevigata ) showed that its adaptive genetic structure along southern Australian coast has been influenced by environmental heterogeneity. This pattern probably results from adaptation to minimum sea surface temperature and oxygen concentration (Sandoval‐Castillo, Robinson, Hart, Strain, & Beheregaray, 2018). In marine fishes, Schunter et al.…”

Oxygen concentration drives local adaptation in the greenlip abalone (Haliotis laevigata)

“…For their genetic analyses, Sandoval‐Castillo et al. () compared 349 samples from 13 field sites using a ddRAD approach. A total of 9,109 SNPs were identified: 8,786 were considered as putatively neutral markers, while 323 SNPs were recognized by at least two different analytical approaches to be under selection (candidate adaptive genes).…”

“…The candidate genes identified by Sandoval‐Castillo et al. () are a great starting point for more detailed investigations of the mechanisms of oxygen level adaptation. Understanding these mechanisms would help us to understand and estimate the consequences of climate change on the diversity, distribution and abundances of marine species and ecosystems.…”

“…Therefore, the work of Sandoval‐Castillo et al. () exemplifies a case study that bridges the gap between collection and application of genomic data, a topic of considerable debate in the literature (Garner et al., ).…”