Ocean circulation model predicts high genetic structure observed in a long‐lived pelagic developer

Understanding the movement of genes and individuals across marine seascapes is a long‐standing challenge in marine ecology and can inform our understanding of local adaptation, the persistence and movement of populations, and the spatial scale of effective management. Patterns of gene flow in the ocean are often inferred based on population genetic analyses coupled with knowledge of species' dispersive life histories. However, genetic structure is the result of time‐integrated processes and may not capture present‐day connectivity between populations. Here, we use a high‐resolution oceanographic circulation model to predict larval dispersal along the complex coastline of western Canada that includes the transition between two well‐studied zoogeographic provinces. We simulate dispersal in a benthic sea star with a 6–10 week pelagic larval phase and test predictions of this model against previously observed genetic structure including a strong phylogeographic break within the zoogeographical transition zone. We also test predictions with new genetic sampling in a site within the phylogeographic break. We find that the coupled genetic and circulation model predicts the high degree of genetic structure observed in this species, despite its long pelagic duration. High genetic structure on this complex coastline can thus be explained through ocean circulation patterns, which tend to retain passive larvae within 20–50 km of their parents, suggesting a necessity for close‐knit design of Marine Protected Area networks.     

Relationship between pelagic larval duration and abundance of tropical fishes on temperate coasts of Japan

The influence of pelagic larval duration (PLD) and egg type dispersal capabilities of 35 demersal and pelagic-spawning tropical fish species is examined in relation to their abundance on the temperate coasts of Japan. The PLDs of pelagic spawners were significantly longer than those of demersal spawners, and a high occurrence of pelagic spawners on the temperate coasts suggests that these fishes are more easily transported to temperate coasts than demersal spawners. For demersal spawners, the common species on the temperate coasts had significantly longer PLDs than the rare species; this suggests that PLD is a major factor influencing the distribution patterns of tropical demersal spawners on temperate coasts. Moreover, a negative correlation between PLD and the abundance of some species of pelagic and demersal spawners suggests the presence of reproductively active fishes in northern subtropical and even in temperate waters.     

Emergent patterns of population genetic structure for a coral reef community

What shapes variation in genetic structure within a community of codistributed species is a central but difficult question for the field of population genetics. With a focus on the isolated coral reef ecosystem of the Hawaiian Archipelago, we assessed how life history traits influence population genetic structure for 35 reef animals. Despite the archipelago's stepping stone configuration, isolation by distance was the least common type of genetic structure, detected in four species. Regional structuring (i.e. division of sites into genetically and spatially distinct regions) was most common, detected in 20 species and nearly in all endemics and habitat specialists. Seven species displayed chaotic (spatially unordered) structuring, and all were nonendemic generalist species. Chaotic structure also associated with relatively high global F_ST. Pelagic larval duration (PLD) was not a strong predictor of variation in population structure (R² = 0.22), but accounting for higher F_ST values of chaotic and invertebrate species, compared to regionally structured and fish species, doubled the power of PLD to explain variation in global F_ST (adjusted R² = 0.50). Multivariate correlation of eight species traits to six genetic traits highlighted dispersal ability, taxonomy (i.e. fish vs. invertebrate) and habitat specialization as strongest influences on genetics, but otherwise left much variation in genetic traits unexplained. Considering that the study design controlled for many sampling and geographical factors, the extreme interspecific variation in spatial genetic patterns observed for Hawaìi marine species may be generated by demographic variability due to species‐specific abundance and migration patterns and/or seascape and historical factors.     

Dynamic larval dispersal can mediate the response of marine metapopulations to multiple climate change impacts

Climate change is having multiple impacts on marine species characterized by sedentary adult and pelagic larval phases, from increasing adult mortality to changes in larval duration and ocean currents. Recent studies have shown impacts of climate change on species persistence through direct effects on individual survival and development, but few have considered the indirect effects mediated by ocean currents and species traits such as pelagic larval duration. We used a density-dependent and stochastic metapopulation model to predict how changes in adult mortality and dynamic connectivity can affect marine metapopulation stability. We analyzed our model with connectivity data simulated from a biophysical ocean model of the northeast Pacific coast forced under current (1998–2007) and future (2068–2077) climate scenarios in combination with scenarios of increasing adult mortality and decreasing larval duration. Our results predict that changes of ocean currents and larval duration mediated by climate change interact in complex and opposing directions to shape local mortality and metapopulation connectivity with synergistic effects on regional metapopulation stability: while species with short larval duration are most sensitive to temperature-driven reduction in larval duration, the response of species with longer larval duration are mostly mediated by changes in both the mean and variance of larval connectivity driven by ocean currents. Our results emphasize the importance of considering the spatiotemporal structure of connectivity in order to predict how the multiple effects of climate change will impact marine populations.     

Does fish larval dispersal differ between high and low latitudes?

Several factors lead to expectations that the scale of larval dispersal and population connectivity of marine animals differs with latitude. We examine this expectation for demersal shorefishes, including relevant mechanisms, assumptions and evidence. We explore latitudinal differences in (i) biological (e.g. species composition, spawning mode, pelagic larval duration, PLD), (ii) physical (e.g. water movement, habitat fragmentation), and (iii) biophysical factors (primarily temperature, which could strongly affect development, swimming ability or feeding). Latitudinal differences exist in taxonomic composition, habitat fragmentation, temperature and larval swimming, and each difference could influence larval dispersal. Nevertheless, clear evidence for latitudinal differences in larval dispersal at the level of broad faunas is lacking. For example, PLD is strongly influenced by taxon, habitat and geographical region, but no independent latitudinal trend is present in published PLD values. Any trends in larval dispersal may be obscured by a lack of appropriate information, or use of ‘off the shelf’ information that is biased with regard to the species assemblages in areas of concern. Biases may also be introduced from latitudinal differences in taxa or spawning modes as well as limited latitudinal sampling. We suggest research to make progress on the question of latitudinal trends in larval dispersal.     

Combined analyses of kinship and FST suggest potential drivers of chaotic genetic patchiness in high gene‐flow populations

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 (Φ_ST = 0.006, P = 0.001; D_{est_Chao} = 0.025) and seven nuclear microsatellites (F_ST = 0.004, P < 0.001; D_{est_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 F_ST 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‐F_16,988 = 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 (D_{est_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 F_ST and high family structure across populations can coexist, illuminating the foundations of cryptic genetic patterns and the nature of marine dispersal.     

Influence of habitat discontinuity, geographical distance, and oceanography on fine-scale population genetic structure of copper rockfish (Sebastes caurinus)

The copper rockfish is a benthic, nonmigratory, temperate rocky reef marine species with pelagic larvae and juveniles. A previous range-wide study of the population-genetic structure of copper rockfish revealed a pattern consistent with isolation-by-distance. This could arise from an intrinsically limited dispersal capability in the species or from regularly-spaced extrinsic barriers that restrict gene flow (offshore jets that advect larvae offshore and/or habitat patchiness). Tissue samples were collected along the West Coast of the contiguous USA between Neah Bay, WA and San Diego, CA, with dense sampling along Oregon. At the whole-coast scale (approximately 2200 km), significant population subdivision (F(ST) = 0.0042), and a significant correlation between genetic and geographical distance were observed based on 11 microsatellite DNA loci. Population divergence was also significant among Oregon collections (approximately 450 km, F(ST) = 0.001). Hierarchical amova identified a weak but significant 130-km habitat break as a possible barrier to gene flow within Oregon, across which we estimated that dispersal (N(e)m) is half that of the coast-wide average. However, individual-based Bayesian analyses failed to identify more than a single population along the Oregon coast. In addition, no correlation between pairwise population genetic and geographical distances was detected at this scale. The offshore jet at Cape Blanco was not a significant barrier to gene flow in this species. These findings are consistent with low larval dispersal distances calculated in previous studies on this species, support a mesoscale dispersal model, and highlight the importance of continuity of habitat and adult population size in maintaining gene flow.     

Impact of variable pelagic environments on natural larval growth and recruitment of the reef fish Thalassoma bifasciatum

New recruits of the bluehead wrasse Thalassoma bifasciatum were censused and collected from nearshore reefs of Barbados, West Indies, every 2 weeks for 20 months. Their temporal coincidence with low salinity (<34·5) water during their pelagic larval stage was determined by comparing the otolith records of new recruits with conductivity and temperature records from a current meter moored 2 km off the west coast of the island. Larval residence in a low salinity North Brazil Current (NBC) ring appeared to have a negative impact on growth. Larvae that encountered a NBC ring for at least 7 days during either the first half of the larval period exhibited slower larval growth than those that did not encounter a ring for 7 days during any part of their larval period. As a result of this slower growth, larvae that encountered low salinity waters had a longer pelagic larval duration and were larger at the time of settlement. The magnitude of settlement was not distinctly related to the presence or absence of a NBC ring, but the largest settlement event occurred at the end of the longest ring event. Early juvenile growth did not vary between fish that had encountered a ring and those that did not, so size differences at settlement were propagated through the first week of life on the reef. The potentially opposing attributes of fast and slow‐growing larvae ( e.g . fast growing larvae with shorter larval stage duration but smaller size at settlement and higher susceptibility to reef predation), and the resulting differential mortality on the reef may promote the persistence of individuals in the population with contrasting life history traits, and contribute to the lack of a relationship between larval growth and recruitment success. Positive transport related effects of rings ( i.e . enhanced retention during some ring events) may further complicate matters by outweighing the negative impact of rings on larval growth.     

Climate change and larval transport in the ocean: fractional effects from physical and physiological factors

Changes in larval import, export, and self‐seeding will affect the resilience of coral reef ecosystems. Climate change will alter the ocean currents that transport larvae and also increase sea surface temperatures (SST), hastening development, and shortening larval durations. Here, we use transport simulations to estimate future larval connectivity due to: (1) physical transport of larvae from altered circulation alone, and (2) the combined effects of altered currents plus physiological response to warming. Virtual larvae from islands throughout Micronesia were moved according to present‐day and future ocean circulation models. The Hybrid Coordinate Ocean Model (HYCOM) spanning 2004–2012 represented present‐day currents. For future currents, we altered HYCOM using analysis from the National Center for Atmospheric Research Community Earth System Model, version 1‐Biogeochemistry, Representative Concentration Pathway 8.5 experiment. Based on the NCAR model, regional SST is estimated to rise 2.74 °C which corresponds to a ~17% decline in larval duration for some taxa. This reduction was the basis for a separate set of simulations. Results predict an increase in self‐seeding in 100 years such that 62–76% of islands experienced increased self‐seeding, there was an average domainwide increase of ~1–3% points in self‐seeding, and increases of up to 25% points for several individual islands. When changed currents alone were considered, approximately half (i.e., random) of all island pairs experienced decreased connectivity but when reduced PLD was added as an effect, ~65% of connections were weakened. Orientation of archipelagos relative to currents determined the directional bias in connectivity changes. There was no universal relationship between climate change and connectivity applicable to all taxa and settings. Islands that presently export large numbers of larvae but that also maintain or enhance this role into the future should be the focus of conservation measures that promote long‐term resilience of larval supply.     

Propagule dispersal and the scales of marine community process

Benthic marine organisms are characterized by a bipartite life history in which populations of sedentary adults are connected by oceanic transport of planktonic propagules. In contrast with the terrestrial case, where ‘long distance dispersal’ (LDD) has traditionally been viewed as a process involving rare events, this creates the possibility for large numbers of offspring to travel far relative to the spatial scale of adult populations. As a result, the concept of LDD must be examined carefully when applied in a marine context. Any measure of LDD requires reference to an explicit ‘local’ scale, often defined in terms of adult population demography, habitat patchiness, or the average dispersal distance. Terms such as ‘open’ and ‘closed’ are relative, and should be used with caution, especially when compared across different taxa and systems. We use recently synthesized data on marine propagule dispersal potential and the spread of marine invasive species to draw inferences about average and maximum effective dispersal distances for marine taxa. Foremost, our results indicate that dispersal occurs at a wide range of scales in marine communities. The nonrandom distribution of these scales among community members has implications for marine community dynamics, and for the implementation of marine conservation efforts. Second, in agreement with theoretical results, our data illustrate that average and extreme dispersal scales do not necessarily covary. This further confounds simple classifications of ‘short’ and ‘long’ dispersers, because different ecological processes (e.g. range expansion vs. population replenishment) depend on different aspects of the dispersal pattern (e.g. extremes vs. average). Our findings argue for a more rigorous quantitative view of scale in the study of marine dispersal processes, where relative terms such as ‘short’ and ‘long’, ‘open’ and ‘closed’, ‘retained’ and ‘exported’ are defined only in conjunction with explicit definitions of the scale and process of interest. This shift in perspective represents an important step towards unifying theoretical and empirical studies of dispersal processes in marine and terrestrial systems.     

The relationship between dispersal ability and geographic range size

There are a variety of proposed evolutionary and ecological explanations for why some species have more extensive geographical ranges than others. One of the most common explanations is variation in species' dispersal ability. However, the purported relationship between dispersal distance and range size has been subjected to few theoretical investigations, and empirical tests reach conflicting conclusions. We attempt to reconcile the equivocal results of previous studies by reviewing and synthesizing quantitative dispersal data, examining the relationship between average dispersal ability and range size for different spatial scales, regions and taxonomic groups. We use extensive data from marine taxa whose average dispersal varies by seven orders of magnitude. Our results suggest dispersal is not a general determinant of range size, but can play an important role in some circumstances. We also review the mechanistic theories proposed to explain a positive relationship between range size and dispersal and explore their underlying rationales and supporting or refuting evidence. Despite numerous studies assuming a priori that dispersal influences range size, this is the first comprehensive conceptual evaluation of these ideas. Overall, our results indicate that although dispersal can be an important process moderating species' distributions, increased attention should be paid to other processes responsible for range size variation.     

Consequences of a poecilogonous life history for genetic structure in coastal populations of the polychaete Streblospio benedicti

In many species, alternative developmental pathways lead to the production of two distinct phenotypes, promoting the evolution of morphological novelty and diversification. Offspring type in marine invertebrates influences transport time by ocean currents, which dictate dispersal potential and gene flow, and thus has sweeping evolutionary effects on the potential for local adaptation and on rates of speciation, extinction and molecular evolution. Here, we use the polychaete Streblospio benedicti to investigate the effects of dimorphic offspring type on gene flow and genetic structure in coastal populations. We use 84 single nucleotide polymorphism (SNP) markers for this species to assay populations on the East and West Coasts of the United States. Using these markers, we found that in their native East Coast distribution, populations of S. benedicti have high‐population genetic structure, but this structure is associated primarily with geographic separation rather than developmental differences. Interestingly, very little genetic differentiation is recovered between individuals of different development types when they occur in the same or nearby populations, further supporting that this is a true case of poecilogony. In addition, we were able to demonstrate that the recently introduced (~100 ya) West Coast populations probably originated from a lecithotrophic population near Delaware.     

Consequences of variable larval dispersal pathways and resulting phenotypic mixtures to the dynamics of marine metapopulations

Larval dispersal can connect distant subpopulations, with important implications for marine population dynamics and persistence, biodiversity conservation and fisheries management. However, different dispersal pathways may affect the final phenotypes, and thus the performance and fitness of individuals that settle into subpopulations. Using otolith microchemical signatures that are indicative of ‘dispersive’ larvae (oceanic signatures) and ‘non-dispersive’ larvae (coastal signatures), we explore the population-level consequences of dispersal-induced variability in phenotypic mixtures for the common triplefin (a small reef fish). We evaluate lipid concentration and otolith microstructure and find that ‘non-dispersive’ larvae (i) have greater and less variable lipid reserves at settlement (and this variability attenuates at a slower rate), (ii) grow faster after settlement, and (iii) experience similar carry-over benefits of lipid reserves on post-settlement growth relative to ‘dispersive’ larvae. We then explore the consequences of phenotypic mixtures in a metapopulation model with two identical subpopulations replenished by variable contributions of ‘dispersive’ and ‘non-dispersive’ larvae and find that the resulting phenotypic mixtures can have profound effects on the size of the metapopulation. We show that, depending upon the patterns of connectivity, phenotypic mixtures can lead to larger metapopulations, suggesting dispersal-induced demographic heterogeneity may facilitate metapopulation persistence.     

High connectivity on a global scale in the pelagic wahoo,Acanthocybium solandri (tuna family Scombridae)

The population genetic structure and phylogeography of wahoo, Acanthocybium solandri, were investigated on a global scale with intron six of lactate dehydrogenase‐A (ldhA6, 8 locations, N = 213) and mtDNA cytochrome b (Cytb, 10 locations, N = 322). Results show extensive sharing of haplotypes across the wahoo's entire global range, and analyses were unable to detect significant structure (nuclear F_ST = 0.0125, P = 0.106; mtDNA Φ_ST < 0.0001, P = 0.634). Power analyses indicated 95% confidence in detecting nuclear F_ST ≥ 0.0389 and mtDNA Φ_ST ≥ 0.0148. These findings appear unique, as most other tunas, billfishes, and oceanic sharks exhibit significant population structure on the scale of East–West Atlantic, Atlantic vs. Indian‐Pacific, or East–West Pacific. Overall nuclear heterozygosity (H = 0.714) and mtDNA haplotype diversity (h = 0.918) are both high in wahoo, while overall mtDNA nucleotide diversity (π= 0.006) and nuclear nucleotide diversity (π=0.004) are uniformly low, indicating a recent increase in population size. Coalescence analyses yield an estimate of effective female population size (N_eF) at ~816 000, and a population bottleneck ~690 000 years ago. However, conclusions about population history from our Cytb data set are not concordant with a control region survey, a finding that will require further investigation. This is the first example of a vertebrate with a single globally distributed population, a finding we attribute to extensive dispersal at all life stages. The indications of a worldwide stock for wahoo reinforce the mandate for international cooperation on fisheries issues.     

Shifting baselines and the decline of pelagic sharks in the Gulf of Mexico

Historical abundances of many large marine vertebrates were tremendously greater than today. However, while pelagic sharks are known to have declined rapidly in the northwest Atlantic in recent years, there, as elsewhere, little is known about the former natural abundances of these species. Here, we compare initial (1950s) and recent (late‐1990s) standardized catch rates of pelagic sharks in the Gulf of Mexico, the area where methods of exploitation between these two periods were most comparable. We estimate that oceanic whitetip and silky sharks, formerly the most commonly caught shark species, have declined by over 99 and 90%, respectively. That the former prevalence of oceanic whitetip sharks in this ecosystem is unrecognized today is clear evidence of shifting baselines. Our analysis provides the missing baseline for pelagic sharks in the Gulf of Mexico that is needed for the rational management and restoration of these species.     

Sharp genetic breaks among populations of Haptosquilla pulchella (Stomatopoda) indicate limits to larval transport: patterns, causes, and consequences

To help stem the precipitous decline of coral reef ecosystems world-wide, conservation efforts are focused on establishing interconnected reserve networks to protect threatened populations. Because many coral reef organisms have a planktonic or pelagic larval dispersal phase, it is critical to understand the patterns of ecological connectivity between reserve populations that result from larval dispersal. We used genetics to infer dispersal patterns among 24 Indo-West Pacific populations of the mantis shrimp, Haptosquilla pulchella. Contrary to predictions of high dispersal facilitated by the strong currents of the Indonesian throughflow, mitochondrial DNA sequences from 393 individuals displayed striking patterns of regional genetic differentiation concordant with ocean basins isolated during periods of lowered sea level. Patterns of genetic structuring indicate that although dispersal within geographical regions with semicontiguous coastlines spanning thousands of kilometres may be common, ecologically meaningful connections can be rare among populations separated by as little as 300 km of open ocean. Strong genetic mosaics in a species with high dispersal potential highlight the utility of genetics for identifying regional patterns of genetic connectivity between marine populations and show that the assumption that ocean currents will provide ecological connectivity among marine populations must be empirically tested in the design of marine reserve networks.     

Environmental and topographic variables shape genetic structure and effective population sizes in the endangered Yosemite toad

Aim Describing the landscape variables that accurately reflect how environmental and topographic variations affect population connectivity and demography is a major goal of landscape genetics and conservation biology. However, few landscape genetics studies have quantified the relationships between landscape variables and effective population size (N_e), although N_e is a key conservation and population genetics parameter. In this study, I estimated genetic structure and effective population sizes in the Yosemite toad (Bufo canorus) and tested for associations with environmental and geographic variables. Location Yosemite National Park, California, USA. Methods I estimated F_ST, D_ps and N_e using 10 microsatellite loci amplified from 781 individuals from 24 populations. I used three landscape variables (environmental variation, topography and slope) to generate geographic distance models and a series of regression analyses to identify the variables that contributed to genetic structure in this species. I also tested for correlations between N_e and a suite of variables, including geographic and genetic isolation, habitat suitability, elevation, temperature and precipitation. Results I found substantial variation in genetic distances between populations (F_ST = 0.004–0.396, D_ps = 0.045–0.839) and in effective population sizes (N_e = 9–52). Environmental variation and slope played important roles in explaining variation in genetic distances, and precipitation variables were significantly correlated with N_e. Main conclusions These results show that environmental and topographic variables are both important for understanding population connectivity in B. canorus and provide some of the first evidence, in any species, for a link between environmental variables and effective population size.     

Population genetic structure and gene flow patterns between populations of the Antarctic icefish Chionodraco rastrospinosus

Aim A lack of genetic structure is predicted for Antarctic fish due to the duration of pelagic larval stages and the strength of the currents in the Southern Ocean, particularly the Antarctic Circumpolar Current. In this study we explored the population structure of the ocellated icefish, Chionodraco rastrospinosus, by means of analysing a total of 394 individuals collected at four geographical areas off the Antarctic Peninsula in the period 1996–2006. Location Elephant Island, southern South Shetlands, Joinville Island and South Orkneys in the Southern Ocean. Methods The spatio‐temporal genetic structure of Chionodraco rastrospinosus was explored using seven microsatellite loci. Existence and direction of gene flow across sampling locations were investigated using the isolation‐by‐migration procedure. Results Microsatellite data showed a lack of genetic structuring in the area studied, with no differences found at both the geographical or temporal level, and an eastward unidirectional gene flow among sites. This suggested a lack of genetic barriers for this species, attributable to larval dispersal following the Antarctic Circumpolar Current, which fits well with the predicted pattern for Antarctic fish. Re‐examination of genetic data of the closely related icefish Chaenocephalus aceratus, with similar larval duration but displaying genetically structured populations, indicated a weak but significant bidirectional gene flow. Main conclusions Our results point to a relationship that is more complex than expected between potential for dispersal and realized gene flow in the marine environment. In addition to ocean circulation and larval dispersal, other major life‐history traits might be driving connectivity, particularly larval retention.