Seascape genomics of common dolphins (Delphinus delphis) reveals adaptive diversity linked to regional and local oceanography

Abstract

Background High levels of standing genomic variation in wide-ranging marine species may enhance prospects for their long-term persistence. Patterns of connectivity and adaptation in such species are often thought to be influenced by spatial factors, environmental heterogeneity, and oceanographic and geomorphological features. Population-level studies that analytically integrate genome-wide data with environmental information (i.e., seascape genomics) have the potential to inform the spatial distribution of adaptive diversity in wide-ranging marine species, such as many marine mammals. We assessed genotype-environment associations (GEAs) in 214 common dolphins (Delphinus delphis) along > 3000 km of the southern coast of Australia. Results We identified 747 candidate adaptive SNPs out of a filtered panel of 17,327 SNPs, and five putatively locally-adapted populations with high levels of standing genomic variation were disclosed along environmentally heterogeneous coasts. Current velocity, sea surface temperature, salinity, and primary productivity were the key environmental variables associated with genomic variation. These environmental variables are in turn related to three main oceanographic phenomena that are likely affecting the dispersal of common dolphins: (1) regional oceanographic circulation, (2) localised and seasonal upwellings, and (3) seasonal on-shelf circulation in protected coastal habitats. Signals of selection at exonic gene regions suggest that adaptive divergence is related to important metabolic traits. Conclusion To the best of our knowledge, this represents the first seascape genomics study for common dolphins (genus Delphinus). Information from the associations between populations and their environment can assist population management in forecasting the adaptive capacity of common dolphins to climate change and other anthropogenic impacts.

Connecting the dots: applying multispecies connectivity in marine park network planning

“…Equally interesting was the very strong explanatory power of the spring advection model for the active dispersers ’ connectivity, despite its design for larval predictions. However, this was not a novel finding: strong associations have previously been found between oceanography and dolphins’ population divergence in southern Australia, with possible relevance to hydrological adaptation and feeding specialisations (Bilgmann et al 2007, Barceló et al 2022, Pratt et al 2022). It is plausible that similar factors may be contributing to structure across current-driven habitat gradients in the present study.…”

“…However, since less dispersive dolphins resident to embayment habitats are considered more likely to be impacted by extreme heatwaves (Wild et al 2019, Barceló et al 2022, the capacity for gene flow and dispersal is particularly valuable. In the present study, network analyses indicated that the strongest link between dolphin population subclusters was between Encounter (Adelaide) and Southern Spencer Gulf (Investigator Strait).…”

Cryptic marine barriers to gene flow in a vulnerable coastal species, the dugong (Dugong dugon)

“…In our study, geographical distance was identified as a more significant explanation of microsatellite genetic distance than sea‐surface temperature (which is unlikely to be limiting in most of the area studied) or seagrass distribution (knowledge of which is incomplete). This contrasts with indications that dugongs might make small‐scale movements in winter linked to sea temperatures at the high latitude limits to their range including Moreton Bay (Sheppard et al, 2006) and with a review of seascape‐genetic studies (Selkoe et al, 2016) that suggested that sea temperature could be as influential as geography in explaining regional‐scale population genetic structure of a number of marine mammal species (e.g., Amaral et al, 2012; Barceló et al, 2022; Fontaine et al, 2007; Pratt et al, 2022; Viricel & Rosel, 2014).…”

“…Environmental constraints to movements of marine wildlife that might affect population structuring may be difficult to identify not only because of the limited opportunities to observe their dispersal and behavior, but because there may be nonapparent barriers that impede gene flow compared to terrestrial systems (Selkoe et al, 2016). For marine wildlife, ecological barriers to movement may include geographic features, e.g., land masses, promontories, archipelagos, ice shelves, or bathymetric features (Viricel & Rosel, 2014), or less obvious physical impediments, including oceanographic features, e.g., currents and eddies (Briscoe et al, 2017), water velocity (Barceló et al, 2022), water depth, or sea surface temperature (Pratt et al, 2022; Sellas et al, 2005; Viricel & Rosel, 2014). In some cases, fine population structuring in highly mobile marine species with continuous distributions has been linked to social/cultural (e.g., Hoelzel et al, 2007; Whitehead, 2017) and/or ecological barriers, including distance between resource patches (e.g., Amaral et al, 2012; Ansmann et al, 2015).…”

Evolutionary history and seascape genomics of Harbour porpoises (Phocoena phocoena) across environmental gradients in the North Atlantic and adjacent waters

“…However, the role of ecological specialization on population differentiation and speciation remains poorly understood (Savolainen, Lascoux & Merila, 2013). This is particularly true for cetacean species, with only a few recent studies attempting to address the genetic basis of local adaptation (Barcelo et al, 2022;Pratt et al, 2022;de Greef et al, 2022;Louis et al, 2021;Zhou et al, 2018). Ecologically and geographical marginal environments often host populations at the edge of the species distribution and under extreme selection regimes (Johannesson & Andre, 2006).…”