A decade of seascape genetics: contributions to basic and applied marine connectivity

Abstract

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.

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

“…Larval dispersal is a key ecological process driving population source–sink dynamics and gene flow (Selkoe et al., 2016). Specifically, gene flow and demographic connectivity maintain genetic diversity (Baguette, Blanchet, Legrand, Stevens, & Turlure, 2013), thus promoting population resilience after disturbance (Baguette et al., 2013; Hughes & Stachowicz, 2004).…”

“…Yet, in marine landscapes (i.e., seascapes), dispersal of most organisms occurs during the pelagic larval stage and depends on oceanic currents that can transport propagules over large distances (White et al., 2010). Larval dispersal is then expected to influence seascape genetic variations, and the resulting genetic patterns often differ from the classical theory of isolation by distance (Selkoe et al., 2016). Hence, a comprehensive assessment of the drivers of spatial genetic variation in marine populations needs to include in a same framework environmental heterogeneity, geographic isolation, and larval dispersal (D'Aloia, Bogdanowicz, Harrison, & Buston, 2014; Selkoe et al., 2016).…”

“…Larval dispersal is then expected to influence seascape genetic variations, and the resulting genetic patterns often differ from the classical theory of isolation by distance (Selkoe et al., 2016). Hence, a comprehensive assessment of the drivers of spatial genetic variation in marine populations needs to include in a same framework environmental heterogeneity, geographic isolation, and larval dispersal (D'Aloia, Bogdanowicz, Harrison, & Buston, 2014; Selkoe et al., 2016). To this aim, large‐scale datasets and novel analytical methods are required (Manel & Holderegger, 2013).…”

“…Historical events such as demographic fluctuations and colonization are also expected to influence spatial genetic variation (Lowe & Allendorf, 2010). It is now well established that several processes structure genetic variation, but there is still much to be learned about the drivers of seascape genetic patterns (Selkoe et al., 2016). In particular, the relative importance and the spatial scale associated with these drivers are rarely discussed in seascape studies (Riginos, Crandall, Liggins, Bongaerts, & Treml, 2016).…”

Ancient DNA reveals the Arctic origin of Viking Age cod from Haithabu, Germany

“…In particular, the genome-wide analysis of 1,000s or more single nucleotide polymorphisms (SNPs) allows the determination of an individual's geographic origin with accuracy and precision, even when limited genetic differentiation exists among regions (20)(21)(22). Since low levels of genetic differentiation are typical for marine species with high dispersal capabilities like Atlantic cod (23,24), such genome-wide approaches are essential to increase the assignment power of modern (22) and ancient samples of these species (25). So far, however, aDNA studies using genome-wide approaches are lacking for marine fishes.…”