Distinct interspecific and intraspecific vulnerability of coastal species to global change.

Characterising and predicting species responses to anthropogenic global change is one of the key challenges in contemporary ecology and conservation. The sensitivity of marine species to climate change is increasingly being described with forecasted species distributions, yet these rarely account for population level processes such as genomic variation and local adaptation. This study compares inter- and intraspecific patterns of biological composition to determine how vulnerability to climate change, and its environmental drivers, vary across species and populations. We compare species trajectories for three ecologically important southern African marine invertebrates at two time points in the future, both at the species level, with correlative species distribution models, and at the population level, with gradient forest models. Reported range shifts are species-specific and include both predicted range gains and losses. Forecasted species responses to climate change are strongly influenced by changes in a suite of environmental variables, from sea surface salinity and sea surface temperature, to minimum air temperature. Our results further suggest a mismatch between future habitat suitability (where species can remain in their ecological niche) and genomic vulnerability (where populations retain their genomic composition), highlighting the inter- and intraspecific variability in species' sensitivity to global change. Overall, this study demonstrates the importance of considering species and population level climatic vulnerability when proactively managing coastal marine ecosystems in the Anthropocene.

Multi-model seascape genomics identifies distinct environmental drivers of selection among sympatric marine species.

BACKGROUND: As global change and anthropogenic pressures continue to increase, conservation and management increasingly needs to consider species' potential to adapt to novel environmental conditions. Therefore, it is imperative to characterise the main selective forces acting on ecosystems, and how these may influence the evolutionary potential of populations and species. Using a multi-model seascape genomics approach, we compare putative environmental drivers of selection in three sympatric southern African marine invertebrates with contrasting ecology and life histories: Cape urchin (Parechinus angulosus), Common shore crab (Cyclograpsus punctatus), and Granular limpet (Scutellastra granularis). RESULTS: Using pooled (Pool-seq), restriction-site associated DNA sequencing (RAD-seq), and seven outlier detection methods, we characterise genomic variation between populations along a strong biogeographical gradient. Of the three species, only S. granularis showed significant isolation-by-distance, and isolation-by-environment driven by sea surface temperatures (SST). In contrast, sea surface salinity (SSS) and range in air temperature correlated more strongly with genomic variation in C. punctatus and P. angulosus. Differences were also found in genomic structuring between the three species, with outlier loci contributing to two clusters in the East and West Coasts for S. granularis and P. angulosus, but not for C. punctatus. CONCLUSION: The findings illustrate distinct evolutionary potential across species, suggesting that species-specific habitat requirements and responses to environmental stresses may be better predictors of evolutionary patterns than the strong environmental gradients within the region. We also found large discrepancies between outlier detection methodologies, and thus offer a novel multi-model approach to identifying the principal environmental selection forces acting on species. Overall, this work highlights how adding a comparative approach to seascape genomics (both with multiple models and species) can elucidate the intricate evolutionary responses of ecosystems to global change.

Complex signatures of genomic variation of two non-model marine species in a homogeneous environment.

BACKGROUND: Genomic tools are increasingly being used on non-model organisms to provide insights into population structure and variability, including signals of selection. However, most studies are carried out in regions with distinct environmental gradients or across large geographical areas, in which local adaptation is expected to occur. Therefore, the focus of this study is to characterize genomic variation and selective signals over short geographic areas within a largely homogeneous region. To assess adaptive signals between microhabitats within the rocky shore, we compared genomic variation between the Cape urchin (Parechinus angulosus), which is a low to mid-shore species, and the Granular limpet (Scutellastra granularis), a high shore specialist. RESULTS: Using pooled restriction site associated DNA (RAD) sequencing, we described patterns of genomic variation and identified outlier loci in both species. We found relatively low numbers of outlier SNPs within each species, and identified outlier genes associated with different selective pressures than those previously identified in studies conducted over larger environmental gradients. The number of population-specific outlier loci differed between species, likely owing to differential selective pressures within the intertidal environment. Interestingly, the outlier loci were highly differentiated within the two northernmost populations for both species, suggesting that unique evolutionary forces are acting on marine invertebrates within this region. CONCLUSIONS: Our study provides a background for comparative genomic studies focused on non-model species, as well as a baseline for the adaptive potential of marine invertebrates along the South African west coast. We also discuss the caveats associated with Pool-seq and potential biases of sequencing coverage on downstream genomic metrics. The findings provide evidence of species-specific selective pressures within a homogeneous environment, and suggest that selective forces acting on small scales are just as crucial to acknowledge as those acting on larger scales. As a whole, our findings imply that future population genomic studies should expand from focusing on model organisms and/or studying heterogeneous regions to better understand the evolutionary processes shaping current and future biodiversity patterns, particularly when used in a comparative phylogeographic context.

Multispecies genetic objectives in spatial conservation planning.

Growing threats to biodiversity and global alteration of habitats and species distributions make it increasingly necessary to consider evolutionary patterns in conservation decision making. Yet, there is no clear-cut guidance on how genetic features can be incorporated into conservation-planning processes, despite multiple molecular markers and several genetic metrics for each marker type to choose from. Genetic patterns differ between species, but the potential tradeoffs among genetic objectives for multiple species in conservation planning are currently understudied. We compared spatial conservation prioritizations derived from 2 metrics of genetic diversity (nucleotide and haplotype diversity) and 2 metrics of genetic isolation (private haplotypes and local genetic differentiation) in mitochondrial DNA of 5 marine species. We compared outcomes of conservation plans based only on habitat representation with plans based on genetic data and habitat representation. Fewer priority areas were selected for conservation plans based solely on habitat representation than on plans that included habitat and genetic data. All 4 genetic metrics selected approximately similar conservation-priority areas, which is likely a result of prioritizing genetic patterns across a genetically diverse array of species. Largely, our results suggest that multispecies genetic conservation objectives are vital to creating protected-area networks that appropriately preserve community-level evolutionary patterns.

Molecular ecology meets systematic conservation planning.

Integrative and proactive conservation approaches are critical to the long-term persistence of biodiversity. Molecular data can provide important information on evolutionary processes necessary for conserving multiple levels of biodiversity (genes, populations, species, and ecosystems). However, molecular data are rarely used to guide spatial conservation decision-making. Here, we bridge the fields of molecular ecology (ME) and systematic conservation planning (SCP) (the 'why') to build a foundation for the inclusion of molecular data into spatial conservation planning tools (the 'how'), and provide a practical guide for implementing this integrative approach for both conservation planners and molecular ecologists. The proposed framework enhances interdisciplinary capacity, which is crucial to achieving the ambitious global conservation goals envisioned for the next decade.

Management and conservation implications of cryptic population substructure for two commercially exploited fishes (Merluccius spp.) in southern Africa.

Genomic information can aid in the establishment of sustainable management plans for commercially exploited marine fishes, aiding in the long-term conservation of these resources. The southern African hakes (Merluccius capensis and M. paradoxus) are commercially valuable demersal fishes with similar distribution ranges but exhibiting contrasting life histories. Using a comparative framework based on Pool-Seq genome-wide SNP data, we investigated whether the evolutionary processes that shaped extant patterns of diversity and divergence are shared among these two congeneric fishes, or unique to each one. Our findings revealed that M. capensis and M. paradoxus show similar levels of genome-wide diversity, despite different census sizes and life-history features. In addition, M. capensis shows three highly structured geographic populations across the Benguela Current region (one in the northern Benguela and two in the southern Benguela), with no consistent genome-environment associations detected. In contrast, although population structure and outlier analyses suggested panmixia for M. paradoxus, reconstruction of its demographic history suggested the presence of an Atlantic-Indian Ocean subtle substructuring pattern. Therefore, it appears that M. paradoxus might be composed by two highly connected populations, one in the Atlantic and one in the southwest Indian Ocean. The reported similar low levels of genomic diversity, as well as newly discovered genetically distinct populations in both hake species can thus assist in informing and improving conservation and management plans for the commercially important southern African Merluccius.