Seascape genetics, a term coined in 2006, is a fast growing area of population genetics that draws on ecology, oceanography and geography to address challenges in basic understanding of marine connectivity and applications to management. We provide an accessible overview of the latest developments in seascape genetics that merge exciting new ideas from the field of marine population connectivity with statistical and technical advances in population genetics. After summarizing the historical context leading to the emergence of seascape genetics, we detail questions and methodological approaches that are evolving the discipline, highlight applications to conservation and management, and conclude with a summary of the field's transition to seascape ge-nomics. From 100 seascape genetic studies, we assess trends in taxonomic and geographic coverage, sampling and statistical design, and dominant seascape drivers. Notably, temperature, oceanography and geography show equal prevalence of influence on spatial genetic patterns, and tests of over 20 other seascape factors suggest that a variety of forces impact connec-tivity at distinct spatio-temporal scales. A new level of rigor in statistical analysis is critical for disentangling multiple drivers and spurious effects. Coupled with GIS data and genomic scale sequencing methods, this rigor is taking seascape genetics beyond an initial focus on identifying correlations to hypothesis-driven insights into patterns and processes of population An underwater seascape from the top of Steve's Bommie in the Great Barrier Reef, Australia. Photo by Jonathan B. Puritz OPEN PEN ACCESS CCESS connectivity and adaptation. The latest studies are illuminating differences between demographic, functional and neutral genetic connectivity, and informing applications to marine reserve design, fisheries science and strategies to assess resilience to climate change and other anthropogenic impacts.
Extreme concentration of marine biodiversity and exploitation of marine resources in the Coral Triangle pose challenges to biogeographers and resource managers. Comparative phylogeography provides a powerful tool to test biogeographic hypotheses evoked to explain species richness in the Coral Triangle. It can also be used to delineate management units for marine resources. After about a decade of phylogeographical studies, patterns for the Coral Triangle are emerging. Broad connectivity in some species support the notion that larvae have maintained gene flow among distant populations for long periods. Other phylogeographic patterns suggest vicariant events resulting from Pleistocene sea level fluctuations, which have, at least occasionally, resulted in speciation. Divergence dates ranging back to the Miocene suggest that changing land configurations may have precipitated an explosion of species diversification. A synthesis of the marine phylogeographic studies reveals repeated patterns that corroborate hypothesized biogeographic processes and suggest improved management schemes for marine resources.
Marine species with ranges that span the Indo-Australian Archipelago (IAA) exhibit a range of phylogeographical patterns, most of which are interpreted in the context of vicariance between Indian and Pacific Ocean populations during Pliocene and Pleistocene low sea-level stands. However, patterns often vary among ecologically similar taxa, sometimes even within genera. This study compares phylogeographical patterns in two species of highly dispersive neritid gastropod, Nerita albicilla and Nerita plicata, with nearly sympatric ranges that span the Indo-Pacific. Mitochondrial COI sequences from >1000 individuals from 97 sites reveal similar phylogenies in both species (two divergent clades differing by 3.2% and 2.3%, for N. albicilla and N. plicata, respectively). However, despite ecological similarity and congeneric status, the two species exhibit phylogeographical discordance. N. albicilla has maintained reciprocal monophyly of Indian and Pacific Ocean populations, while N. plicata is panmictic between oceans, but displays a genetic cline in the Central Pacific. Although this difference might be explained by qualitatively different demographic histories, parameter estimates from three coalescent models indicate that both species have high levels of gene flow between demes (2Nem>75), and share a common history of population expansion that is likely associated with cyclical flooding of continental shelves and island lagoons following low sea-level stands. Results indicate that ecologically similar, codistributed species may respond very differently to shared environmental processes, suggesting that relatively minor differences in traits such as pelagic larval duration or microhabitat association may profoundly impact phylogeographical structure.
Population genomic approaches are making rapid inroads in the study of non-model organisms, including marine taxa. To date, these marine studies have predominantly focused on rudimentary metrics describing the spatial and environmental context of their study region (e.g., geographical distance, average sea surface temperature, average salinity). We contend that a more nuanced and considered approach to quantifying seascape dynamics and patterns can strengthen population genomic investigations and help identify spatial, temporal, and environmental factors associated with differing selective regimes or demographic histories. Nevertheless, approaches for quantifying marine landscapes are complicated. Characteristic features of the marine environment, including pelagic living in flowing water (experienced by most marine taxa at some point in their life cycle), require a well-designed spatial-temporal sampling strategy and analysis. Many genetic summary statistics used to describe populations may be inappropriate for marine species with large population sizes, large species ranges, stochastic recruitment, and asymmetrical gene flow. Finally, statistical approaches for testing associations between seascapes and population genomic patterns are still maturing with no single approach able to capture all relevant considerations. None of these issues are completely unique to marine systems and therefore similar issues and solutions will be shared for many organisms regardless of habitat. Here, we outline goals and spatial approaches for landscape genomics with an emphasis on marine systems and review the growing empirical literature on seascape genomics. We review established tools and approaches and highlight promising new strategies to overcome select issues including a strategy to spatially optimize sampling. Despite the many challenges, we argue that marine systems may be especially well suited for identifying candidate genomic regions under environmentally mediated selection and that seascape genomic approaches are especially useful for identifying robust locus-by-environment associations.
ABSTRACT.-Targeted conservation and management programs are crucial for mitigating anthropogenic threats to declining biodiversity. Although evolutionary processes underpin extant patterns of biodiversity, it is uncommon for resource managers to explicitly consider genetic data in conservation prioritization. Genetic information is inherently relevant to management because it describes genetic diversity, population connectedness, and evolutionary history; thereby typifying their behavioral traits, physiological climate tolerance, evolutionary potential, and dispersal ability. Incorporating genetic information into spatial conservation prioritization starts with reconciling the terminology and techniques used in genetics and conservation science. Genetic data vary widely in analyses and their interpretations can be challenging even for experienced geneticists. Therefore, identifying objectives, decision rules, and implementations in decision support tools specifically for management using genetic data is challenging. Here, we outline a framework for eight genetic system characteristics, their measurement, and how they could be incorporated in spatial conservation prioritization for two contrasting objectives: biodiversity preservation vs maintaining ecological function and sustainable use. We illustrate this framework with an example using data from Tridacna crocea (Lamarck, 1819) (boring giant clam) in the Coral Triangle. We find that many reefs highlighted as conservation priorities with genetic data based on genetic subregions, genetic diversity, genetic distinctness, and connectivity are not prioritized using standard practices. Moreover, different characteristics calculated from the same samples resulted in different spatial conservation priorities. Our results highlight that omitting genetic information from conservation decisions may fail to adequately represent processes regulating biodiversity, but that conservation objectives related to the choice of genetic system characteristics require careful consideration.
Abstract-Chinook Salmon (Oncorhynchus tshawytscha) is an economically and ecologically important species, and populations from the west coast of North America are a major component of fisheries in the North Pacific Ocean. The anadromous life history strategy of this species generates populations (or stocks) that typically are differentiated from neighboring populations. In many cases, it is desirable to discern the stock of origin of an individual fish or the stock composition of a mixed sample to monitor the stock-specific effects of anthropogenic impacts and alter management strategies accordingly. Genetic stock identification (GSI) provides such discrimination, and we describe here a novel GSI baseline composed of genotypes from more than 8000 individual fish from 69 distinct populations at 96 single nucleotide polymorphism (SNP) loci. The populations included in this baseline represent the likely sources for more than 99% of the salmon encountered in ocean fisheries of California and Oregon. This new genetic baseline permits GSI with the use of rapid and cost-effective SNP genotyping, and power analyses indicate that it provides very accurate identification of important stocks of Chinook Salmon. In an ocean fishery sample, GSI assignments of more than 1000 fish, with our baseline, were highly concordant (98.95%) at the reporting unit level with information from the physical tags recovered from the same fish. This SNP baseline represents an important advance in the technologies available to managers and researchers of this species.
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