Marine species frequently show weak and/or complex genetic structuring that is commonly dismissed as 'chaotic' genetic patchiness and ecologically uninformative. Here, using three datasets that individually feature weak chaotic patchiness, we demonstrate that combining inferences across species and incorporating environmental data can greatly improve the predictive value of marine population genetics studies on small spatial scales. Significant correlations in genetic patterns of microsatellite markers among three species, kelp bass Paralabrax clathratus, Kellet's whelk Kelletia kelletii and California spiny lobster Panulirus interruptus, in the Southern California Bight suggest that slight differences in diversity and pairwise differentiation across sampling sites are not simply noise or chaotic patchiness, but are ecologically meaningful. To test whether interspecies correlations potentially result from shared environmental drivers of genetic patterns, we assembled data on kelp bed size, sea surface temperature and estimates of site-to-site migration probability derived from a high resolution multi-year ocean circulation model. These data served as predictor variables in linear models of genetic diversity and linear mixed models of genetic differentiation that were assessed with information-theoretic model selection. Kelp was the most informative predictor of genetics for all three species, but ocean circulation also played a minor role for kelp bass. The shared patterns suggest a single spatial marine management strategy may effectively protect genetic diversity of multiple species. This study demonstrates the power of environmental and ecological data to shed light on weak genetic patterns and highlights the need for future focus on a mechanistic understanding of the links between oceanography, ecology and genetic structure.
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.
Understanding how geography, oceanography, and climate have ultimately shaped marine biodiversity requires aligning the distributions of genetic diversity across multiple taxa. Here, we examine phylogeographic partitions in the sea against a backdrop of biogeographic provinces defined by taxonomy, endemism, and species composition. The taxonomic identities used to define biogeographic provinces are routinely accompanied by diagnostic genetic differences between sister species, indicating interspecific concordance between biogeography and phylogeography. In cases where individual species are distributed across two or more biogeographic provinces, shifts in genotype frequencies often align with biogeographic boundaries, providing intraspecific concordance between biogeography and phylogeography. Here, we provide examples of comparative phylogeography from (i) tropical seas that host the highest marine biodiversity, (ii) temperate seas with high productivity but volatile coastlines, (iii) migratory marine fauna, and (iv) plankton that are the most abundant eukaryotes on earth. Tropical and temperate zones both show impacts of glacial cycles, the former primarily through changing sea levels, and the latter through coastal habitat disruption. The general concordance between biogeography and phylogeography indicates that the population-level genetic divergences observed between provinces are a starting point for macroevolutionary divergences between species. However, isolation between provinces does not account for all marine biodiversity; the remainder arises through alternative pathways, such as ecological speciation and parapatric (semiisolated) divergences within provinces and biodiversity hotspots.biogeography | coral reefs | evolution | marine biodiversity | speciation P hylogeography has roots in biogeography, wherein geographic provinces are identified by concordant shifts in species composition. If the partitions defined by taxonomy are regarded as first-order approximations of evolutionary genetic separations, then continuity between biogeography and phylogeography is apparent. Marine biogeography, the study of species' distributions and evolutionary processes in the sea, began in the mid19th century based on taxonomic distinctions. Dana (1) divided the surface waters of the world into several temperature zones based on the distributions of corals and crustaceans. Woodward (2) identified a series of marine provinces based on the distributions of mollusks. Forbes (3) made three enduring observations: (i) each biogeographic province is a center of origin for new species, (ii) these new species tend to migrate outward from the center of origin, and (iii) provinces, like species, must be traced back to their historical origins to be understood. These three fundamental contributions appeared in the same decade in which Darwin and Wallace (4) and Darwin (5) identified geography and natural selection as agents of evolutionary change.It is remarkable that five essential publications in the 1850s (1-5) set the stage ...
We combine kinship estimates with traditional F-statistics to explain contemporary drivers of population genetic differentiation despite high gene flow. We investigate range-wide population genetic structure of the California spiny (or red rock) lobster (Panulirus interruptus) and find slight, but significant global population differentiation in mtDNA (ΦST = 0.006, P = 0.001; Dest_Chao = 0.025) and seven nuclear microsatellites (FST = 0.004, P < 0.001; Dest_Chao = 0.03), despite the species’ 240- to 330-day pelagic larval duration. Significant population structure does not correlate with distance between sampling locations, and pairwise FST between adjacent sites often exceeds that among geographically distant locations. This result would typically be interpreted as unexplainable, chaotic genetic patchiness. However, kinship levels differ significantly among sites (pseudo-F16,988 = 1.39, P = 0.001), and ten of 17 sample sites have significantly greater numbers of kin than expected by chance (P < 0.05). Moreover, a higher proportion of kin within sites strongly correlates with greater genetic differentiation among sites (Dest_Chao, R2 = 0.66, P < 0.005). Sites with elevated mean kinship were geographically proximate to regions of high upwelling intensity (R2 = 0.41, P = 0.0009). These results indicate that P. interruptus does not maintain a single homogenous population, despite extreme dispersal potential. Instead, these lobsters appear to either have substantial localized recruitment or maintain planktonic larval cohesiveness whereby siblings more likely settle together than disperse across sites. More broadly, our results contribute to a growing number of studies showing that low FST and high family structure across populations can coexist, illuminating the foundations of cryptic genetic patterns and the nature of marine dispersal.
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