Using neutral, selected, and hitchhiker loci to assess connectivity of marine populations in the genomic era

Abstract

Estimating the rate of exchange of individuals among populations is a central concern to evolutionary ecology and its applications to conservation and management. For instance, the efficiency of protected areas in sustaining locally endangered populations and ecosystems depends on reserve network connectivity. The population genetics theory offers a powerful framework for estimating dispersal distances and migration rates from molecular data. In the marine realm, however, decades of molecular studies have met limited success in inferring genetic connectivity, due to the frequent lack of spatial genetic structure in species exhibiting high fecundity and dispersal capabilities. This is especially true within biogeographic regions bounded by well-known hotspots of genetic differentiation. Here, we provide an overview of the current methods for estimating genetic connectivity using molecular markers and propose several directions for improving existing approaches using large population genomic datasets. We highlight several issues that limit the effectiveness of methods based on neutral markers when there is virtually no genetic differentiation among samples. We then focus on alternative methods based on markers influenced by selection. Although some of these methodologies are still underexplored, our aim was to stimulate new research to test how broadly they are applicable to nonmodel marine species. We argue that the increased ability to apply the concepts of cline analyses will improve dispersal inferences across physical and ecological barriers that reduce connectivity locally. We finally present how neutral markers hitchhiking with selected loci can also provide information about connectivity patterns within apparently well-mixed biogeographic regions. We contend that one of the most promising applications of population genomics is the use of outlier loci to delineate relevant conservation units and related eco-geographic features across which connectivity can be measured.

Population genomics of the introduced and cultivated Pacific kelp Undaria pinnatifida: Marinas—not farms—drive regional connectivity and establishment in natural rocky reefs

“…10,000 SNPs derived from ddRAD‐sequencing. As expected (Gagnaire et al., 2015), the RAD‐seq panel showed more power than the microsatellite panel for identifying fine‐grained genetic structure patterns, as well as for detecting outliers. However, overall, both marker panels revealed similar patterns.…”

Outlier analyses to test for local adaptation to breeding grounds in a migratory arctic seabird

“…These results are consistent with previous analyses of mitochondrial and microsatellite data, which also failed to detect population structure in the Atlantic Ocean (Birt‐Friesen et al., 1992; Tigano et al., 2015). Lack of population structure in marine organisms, including seabirds, is often observed due to apparent lack of barriers to gene flow and/or large population sizes (Friesen, 2015; Gagnaire et al., 2015). In some cases, the use of a high number of markers can increase resolution: In the black‐footed albatross ( Phoebastria nigripes ) for instance, genotyping of thousands of genomewide markers revealed weak but significant population structure among colonies in Japan and Hawaii, where previous results from traditional genetic markers were contradictory (Dierickx, Shultz, Sato, Hiraoka, & Edwards, 2015).…”

“…Our study highlighted the inherent limitations of outlier analyses in detecting signatures of local adaptation in natural populations, especially when the same pattern of differentiation can be driven by multiple factors such as gene flow, genetic drift, recombination rate, and demographic history. Nonetheless, we showed that if we consider the demographic histories and evolutionary scenarios of the focal species, the limitations of the methods to detect outlier loci, and all alternative hypotheses explaining differentiation patterns, outlier analyses could also be used to investigate demographic processes in populations of species that are demographically independent but not yet not genetically differentiated (Gagnaire et al., 2015). Although with five colonies we did not have enough power for more rigorous tests (e.g., genotype–environment association tests), the results from this study are promising in sight of future studies including more colonies from throughout the Atlantic.…”

Unexpected mosaic distribution of two hybridizing sibling lineages in the teleplanically dispersing snail Stramonita haemastoma suggests unusual postglacial redistribution or cryptic invasion

“…It has long been expected that species with a dispersive larval stage should be less differentiated than species with direct development (Hellberg, 1996; Johnson & Seger, 2001; Palumbi & Baker, 1994), and this has been corroborated by meta‐analyzes of the marine population genetics literature (Kelly & Palumbi, 2009; Selkoe & Toonen, 2011). However, planktonic dispersers have also long revealed pronounced genetic breaks between populations of what was recognized as a single species, and these often collocate with well documented biogeographic boundaries (Gagnaire et al., 2015; Pelc, Warner, & Gaines, 2009; Riginos et al., 2011). Marine biogeographic boundaries often coincide with oceanic fronts thought to impose a physical barrier to dispersal and with strong environmental gradients.…”