Return of the Ghosts of Dispersal Past: Historical Spread and Contemporary Gene Flow in the Blue Sea Star Linckia Laevigata

Marine animals inhabiting the Indian and Pacific oceans have some of the most extensive species ranges in the world, sometimes spanning over half the globe. These Indo-Pacific species present a challenge for study with both geographic scope and sampling density as limiting factors. Here, we augment and aggregate phylogeographic sampling of the iconic blue sea star, Linckia laevigata Linnaeus, 1758, and present one of the most geographically comprehensive genetic studies of any Indo-Pacific species to date, sequencing 392 base pairs of mitochondrial COI from 791 individuals from 38 locations spanning over 14,000 km. We first use a permutation based multiple-regression approach to simultaneously evaluate the relative influence of historical and contemporary gene flow together with putative barriers to dispersal. We then use a discrete diffusion model of phylogeography to infer the historical migration and colonization routes most likely used by L. laevigata across the Indo-Pacific. We show that estimates of genetic structure have a stronger correlation to geographic distances than to “oceanographic” distances from a biophysical model of larval dispersal, reminding us that population genetic estimates of gene flow and genetic structure are often shaped by historical processes. While the diffusion model was equivocal about the location of the mitochondrial most recent common ancestor (MRCA), we show that gene flow has generally proceeded in a step-wise manner across the Indian and Pacific oceans. We do not find support for previously described barriers at the Sunda Shelf and within Cenderwasih Bay. Rather, the strongest genetic disjunction is found to the east of Cenderwasih Bay along northern New Guinea. These results underscore the importance of comprehensive range-wide sampling in marine phylogeography

Magnificent dimensions, varied forms, and brilliant colors: The molecular ecology and evolution of the Indian and Pacific oceans

The tropical Indian and Pacific oceans form the world's largest and most speciose marine biogeographic region: the Indo-Pacific. Due to its size and political complexity, the Indo-Pacific is rarely studied as a whole, yet comprehensive studies of the region promise to teach us much about marine ecology and evolution. Molecular methods can provide substantial initial insights into the processes that create and maintain biodiversity in the region while also providing critical spatial information to managers. This special issue presents six synthetic papers that discuss the current state of molecular work in the Indo-Pacific region as well as best practices for the future. Following these synthetic papers are 15 empirical papers that extend our knowledge of the region considerably. A comprehensive understanding of the biodiversity that we stand to lose in the Indo-Pacific is going to require increased cooperation and collaboration among laboratories that study this region, as exemplified by papers in this special issue

Navigating the Currents of Seascape Genomics: How Spatial Analyses can Augment Population Genomic Studies

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 onmarine 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

Evaluation of a Single Nucleotide Polymorphism Baseline for Genetic Stock Identification of Chinook Salmon (Oncorhynchus tshawytscha) in the California Current Large Marine Ecosystem

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

High Gene Flow Due to Pelagic Larval Dispersal Among South Pacific Archipelagos in Two Amphidromous Gastropods (Neritomorpha: Neritidae)

The freshwater stream fauna of tropical oceanic islands is dominated by amphidromous species, whose larvae are transported to the ocean and develop in the plankton before recruiting back to freshwater habitat as juveniles. Because stream habitat is relatively scarce and unstable on oceanic islands, this life history would seem to favor either the retention of larvae to their natal streams, or the ability to delay metamorphosis until new habitat is encountered. To distinguish between these hypotheses, we used population genetic methods to estimate larval dispersal among five South Pacific archipelagos in two amphidromous species of Neritid gastropod (Neritina canalis and Neripteron dilatatus). Sequence data from mitochondrial COI revealed that neither species is genetically structured throughout the Western Pacific, suggesting that their larvae have a pelagic larval duration of at least eight weeks, longer than many marine species. Additionally, the two species have recently colonized isolated Central Pacific archipelagos in three independent events. Since colonization, there has been little to no gene flow between the Western and Central Pacific archipelagos in Neritina canalis, and high levels of gene flow across the same region in Neripteron dilatatus. Both species show departures from neutrality and recent dates for colonization of the Central Pacific archipelagos consistent with frequent extinction and recolonization of stream populations in this area. Similar results from other amphidromous species suggest that unstable freshwater habitats promote long-distance dispersal capabilities

Genetic Diversity, Population Structure, and Demographic History of Exploited Sea Urchin Populations (Tripneustes Gratilla) in the Philippines

The sea urchin Tripneustes gratilla is ecologically and economically important in the Indo-Pacific region. We use population genetic methods to investigate the population structure and historical demography of exploited populations in the Philippines. Sea urchins sampled in 6 localities in western Luzon and 4 outgroup sites were sequenced for mitochondrial cytochrome oxidase-1 gene (n = 282) and genotyped for seven microsatellite loci (n = 277). No significant genetic structure was found for either class of markers, indicating either extensive gene flow across the archipelago, or that populations have high genetic diversity and have not yet attained equilibrium between genetic drift and migration following large changes in demography. Interestingly, demographic inferences from the two types of markers were discordant. Mitochondrial lineages showed demographic expansion during the Pleistocene while microsatellite data indicated population decline. Estimates for the date of each event suggest that a Pleistocene expansion could have preceded a more recent population decline, but we also discuss other hypotheses for the discordant inferences.The high genetic diversity and broad distribution of haplotypes in populations that recently recovered from fishery collapse indicate that this species is very resilient over evolutionary timescales

A Coalescent Sampler Successfully Detects Biologically Meaningful Population Structure Overlooked by F‐Statistics

Assessing the geographic structure of populations has relied heavily on Sewell Wright\u27s F‐statistics and their numerous analogues for many decades. However, it is well appreciated that, due to their nonlinear relationship with gene flow, F statistics frequently fail to reject the null model of panmixia in species with relatively high levels of gene flow and large population sizes. Coalescent genealogy samplers instead allow a model‐selection approach to the characterization of population structure, thereby providing the opportunity for stronger inference. Here, we validate the use of coalescent samplers in a high gene flow context using simulations of a stepping‐stone model. In an example case study, we then re‐analyze genetic datasets from 41 marine species sampled from throughout the Hawaiian archipelago using coalescent model selection. Due to the archipelago\u27s linear nature, it is expected that most species will conform to some sort of stepping‐stone model (leading to an expected pattern of isolation by distance), but F‐statistics have only supported this inference in ~10% of these datasets. Our simulation analysis shows that a coalescent sampler can make a correct inference of stepping‐stone gene flow in nearly 100% of cases where gene flow is ≤100 migrants per generation (equivalent to FST = 0.002), while F‐statistics had mixed results. Our re‐analysis of empirical datasets found that nearly 70% of datasets with an unambiguous result fit a stepping‐stone model with varying population sizes and rates of gene flow, although 37% of datasets yielded ambiguous results. Together, our results demonstrate that coalescent samplers hold great promise for detecting weak but meaningful population structure, and defining appropriate management units

The Scope of Published Population Genetic Data for Indo-Pacific Marine Fauna and Future Research Opportunities in the Region

Marine biodiversity reaches its pinnacle in the tropical Indo-Pacific region, with high levels of both species richness and endemism, especially in coral reef habitats. While this pattern of biodiversity has been known to biogeographers for centuries, causal mechanisms remain enigmatic. Over the past 20 yrs, genetic markers have been employed by many researchers as a tool to elucidate patterns of biodiversity above and below the species level, as well as to make inferences about the underlying processes of diversification, demographic history, and dispersal. In a quantitative, comparative framework, these data can be synthesized to address questions about this bewildering diversity by treating species as “replicates.” However, the sheer size of the Indo-Pacific region means that the geographic and genetic scope of many species’ data sets are not complementary. Here, we describe data sets from 116 Indo-Pacific species (108 studies). With a mind to future synthetic investigations, we consider the strengths and omissions of currently published population genetic data for marine fauna of the Indo-Pacific region, as well as the geographic and taxonomic scope of the data, and suggest some ways forward for data collection and collation

Contrasting Demographic History and Phylogeographic Patterns in Two Indo-Pacific Gastropods

Marine species with ranges that span the Indo-Australian Archipelago (IAA) exhibit a range of phylogeographic 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 phylogeographic 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 \u3e 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 phylogeographic discordance, with N. albicilla maintaining 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 (2Ne m \u3e 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 co-distributed 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 phylogeographic structure

Comparative Phylogeography of Two Seastars and Their Ectosymbionts Within the Coral Triangle

Repeated exposure and flooding of the Sunda and Sahul shelves during Pleistocene sea level fluctuations is thought to have contributed to the isolation and diversification of sea basin populations within the Coral Triangle. This hypothesis has been tested in numerous phylogeographic studies, recovering an assortment of genetic patterns that the authors have generally attributed to differences in larval dispersal capability or adult habitat specificity. This study compares phylogeographic patterns from mitochondrial COI sequences among two co-distributed seastars that differ in their adult habitat and dispersal ability, and two seastar ectosymbionts that differ in their degree of host specificity. Of these, only the seastar Linckia laevigata displayed a classic pattern of Indian-Pacific divergence, but with only moderate genetic structure (ΦCT = 0.067). In contrast, the seastar Protoreaster nodosus exhibited strong structure (ΦCT = 0.23) between Teluk Cenderawasih and the remainder of Indonesia, a 12 pattern of regional structure that was echoed in L. laevigata (ΦCT = 0.03) as well as its obligate gastropod parasite Thyca crystallina (ΦCT = 0.04). The generalist commensal shrimp, Periclimenes soror showed little genetic structuring across the Coral Triangle. Despite species-specific phylogeographic patterns, all four species showed departures from neutrality that are consistent with massive range expansions onto the continental shelves as sea levels rose, and date within the Pleistocene epoch. Our results suggest that habitat differences may affect the manner in which species responded to Pleistocene sea level fluctuations, shaping contemporary patterns of genetic structure and diversity