Rampant asexual reproduction and limited dispersal in a mangrove population of the coral Porites divaricata.

Corals are critical to marine biodiversity. Reproduction and dispersal are key to their resilience, but rarely quantified in nature. Exploiting a unique system-a fully censused, longitudinally characterized, semi-isolated population inhabiting mangroves-we used 2bRAD sequencing to demonstrate that rampant asexual reproduction most likely via parthenogenesis and limited dispersal enable the persistence of a natural population of thin-finger coral (Porites divaricata). Unlike previous studies on coral dispersal, knowledge of colony age and location enabled us to identify plausible parent-offspring relationships within multiple clonal lineages and develop tightly constrained estimates of larval dispersal; the best-fitting model indicates dispersal is largely limited to a few metres from parent colonies. Our results explain why this species is adept at colonizing mangroves but suggest limited genetic diversity in mangrove populations and limited connectivity between mangroves and nearby reefs. As P. divaricata is gonochoristic, and parthenogenesis would be restricted to females (whereas fragmentation, which is presumably common in reef and seagrass habitats, is not), mangrove populations likely exhibit skewed sex ratios. These findings suggest that coral reproductive diversity can lead to distinctly different demographic outcomes in different habitats. Thus, coral conservation will require the protection of the entire coral habitat mosaic, and not just reefs.

Isolation-by-distance and genetic parentage analysis provide similar larval dispersal estimates.

Larval exchange among marine populations is a vital driver of population dynamics and has the potential to inform conservation actions, but accurately measuring dispersal remains challenging. Consequently, empirical dispersal kernels have been measured for only a few marine species. Here, we obtained indirect dispersal estimates using an isolation-by-distance (IBD) model in the coral reef fish Elacatinus lori and assessed the accuracy of these estimates by comparing them to direct measurements of dispersal from genetic parentage analysis. Specifically, drawing on the IBD slope and effective population density, we indirectly estimated sigma (σ), the spread of a dispersal distribution. While the spread of the directly measured distribution was σ = 3.93 km (95% CI: 3.29-4.71 km), the spread of the IBD distribution was σ = 4.10 km (95% CI: 3.23-5.03) and σ = 2.90 km (95% CI: 2.26-3.59), assuming a random or monogamous mating system, respectively. Parameterizing Laplace dispersal kernels with these values of σ yielded patterns that were remarkably similar to a kernel fit to the direct parentage data. We also found that, like many marine fishes, E. lori has a large effective population size. However, uncertainty in effective size did not ultimately have a strong effect on the IBD-based dispersal estimates. Taken together, these findings illustrate that accurate dispersal estimates can be produced by indirect IBD methods and suggest that this more feasible approach to estimating dispersal may be broadly applicable to the study of marine larval dispersal.

Incorporating putatively neutral and adaptive genomic data into marine conservation planning.

The availability of genomic data for an increasing number of species makes it possible to incorporate evolutionary processes into conservation plans. Recent studies show how genetic data can inform spatial conservation prioritization (SCP), but they focus on metrics of diversity and distinctness derived primarily from neutral genetic data sets. Identifying adaptive genetic markers can provide important information regarding the capacity for populations to adapt to environmental change. Yet, the effect of including metrics based on adaptive genomic data into SCP in comparison to more widely used neutral genetic metrics has not been explored. We used existing genomic data on a commercially exploited species, the giant California sea cucumber (Parastichopus californicus), to perform SCP for the coastal region of British Columbia (BC), Canada. Using a RAD-seq data set for 717 P. californicus individuals across 24 sampling locations, we identified putatively adaptive (i.e., candidate) single nucleotide polymorphisms (SNPs) based on genotype-environment associations with seafloor temperature. We calculated various metrics for both neutral and candidate SNPs and compared SCP outcomes with independent metrics and combinations of metrics. Priority areas varied depending on whether neutral or candidate SNPs were used and on the specific metric used. For example, targeting sites with a high frequency of warm-temperature-associated alleles to support persistence under future warming prioritized areas in the southern coastal region. In contrast, targeting sites with high expected heterozygosity at candidate loci to support persistence under future environmental uncertainty prioritized areas in the north. When combining metrics, all scenarios generated intermediate solutions, protecting sites that span latitudinal and thermal gradients. Our results demonstrate that distinguishing between neutral and adaptive markers can affect conservation solutions and emphasize the importance of defining objectives when choosing among various genomic metrics for SCP.

Incorporación de Datos Genómicos Putativamente Neutros y Adaptativos dentro de la Planeación de la Conservación Marina Resumen La disponibilidad de los datos genómicos para un número creciente de especies posibilita la incorporación de los procesos evolutivos dentro de los planes de conservación. Los estudios recientes muestran cómo los datos genéticos pueden informar a la priorización de la conservación espacial (PCE) pero tienden a enfocarse más en las medidas de la diversidad y la distinción derivadas principalmente de los conjuntos de datos genéticos neutrales. La identificación de los marcadores genéticos adaptativos puede proporcionar información importante con respecto a la capacidad de las poblaciones para adaptarse al cambio ambiental. Aun así, no se ha explorado el efecto de la inclusión de las medidas basadas en los datos genéticos adaptativos dentro de la PCE y cómo se comparan con las medidas genéticas neutrales de uso más amplio. Usamos datos genómicos existentes sobre una especie de explotación comercial, el pepino de mar gigante de California (Parastichopus californicus), para realizar la PCE para la región costera de la Columbia Británica (BC) en Canadá. Usamos un conjunto de datos RAD-seq para 717 individuos de la especie P. californicus en 24 localidades de muestreo para identificar los polimorfismos de un solo nucleótido (PSNs) putativamente adaptativos (es decir, candidatos) con base en las asociaciones genotipo-ambiente manifestadas con la temperatura del fondo marino. Calculamos varias medidas para los PSNs neutrales y los PSNs candidatos y comparamos los resultados de la PCE con medidas independientes y con combinaciones de medidas. Las áreas prioritarias variaron dependiendo de si se usaron los SNP neutrales o los candidatos y de la medida específica que se utilizó. Por ejemplo, enfocarse en sitios con una frecuencia alta de alelos asociados con agua cálida para fortalecer la persistencia frente al futuro calentamiento prioriza las áreas en la región del sur de la costa. Al contrario, enfocarse en sitios con una alta heterocigosidad esperada en los loci de los candidatos para fortalecer la persistencia frente a la incertidumbre ambiental prioriza las áreas en la parte norte de la costa. Cuando combinamos las medidas, todos los escenarios generaron soluciones intermedias, protegiendo así los sitios que abarcan gradientes latitudinales y gradientes térmicos. Nuestros resultados demuestran que la distinción entre los marcadores neutrales y los adaptativos puede afectar las soluciones de conservación y también enfatizan la importancia de la definición de los objetivos cuando se elige entre varias medidas genómicas para la PCE.

Unraveling hierarchical genetic structure in a marine metapopulation: A comparison of three high-throughput genotyping approaches.

Marine metapopulations often exhibit subtle population structure that can be difficult to detect. Given recent advances in high-throughput sequencing, an emerging question is whether various genotyping approaches, in concert with improved sampling designs, will substantially improve our understanding of genetic structure in the sea. To address this question, we explored hierarchical patterns of structure in the coral reef fish Elacatinus lori using a high-resolution approach with respect to both genetic and geographic sampling. Previously, we identified three putative E. lori populations within Belize using traditional genetic markers and sparse geographic sampling: barrier reef and Turneffe Atoll; Glover's Atoll; and Lighthouse Atoll. Here, we systematically sampled individuals at ~10 km intervals throughout these reefs (1,129 individuals from 35 sites) and sequenced all individuals at three sets of markers: 2,418 SNPs; 89 microsatellites; and 57 nonrepetitive nuclear loci. At broad spatial scales, the markers were consistent with each other and with previous findings. At finer spatial scales, there was new evidence of genetic substructure, but our three marker sets differed slightly in their ability to detect these patterns. Specifically, we found subtle structure between the barrier reef and Turneffe Atoll, with SNPs resolving this pattern most effectively. We also documented isolation by distance within the barrier reef. Sensitivity analyses revealed that the number of loci (and alleles) had a strong effect on the detection of structure for all three marker sets, particularly at small spatial scales. Taken together, these results illustrate empirically that high-throughput genotyping data can elucidate subtle genetic structure at previously-undetected scales in a dispersive marine fish.

The Evolution of Marine Larval Dispersal Kernels in Spatially Structured Habitats: Analytical Models, Individual-Based Simulations, and Comparisons with Empirical Estimates.

Understanding the causes of larval dispersal is a major goal of marine ecology, yet most research focuses on proximate causes. Here we ask how ultimate, evolutionary causes affect dispersal. Building on Hamilton and May's classic 1977 article "Dispersal in Stable Habitats," we develop analytic and simulation models for the evolution of dispersal kernels in spatially structured habitats. First, we investigate dispersal in a world without edges and find that most offspring disperse as far as possible, opposite the pattern of empirical data. Adding edges to our model world leads to nearly all offspring dispersing short distances, again a mismatch with empirical data. Adding resource heterogeneity improves our results: most offspring disperse short distances with some dispersing longer distances. Finally, we simulate dispersal evolution in a real seascape in Belize and find that the simulated dispersal kernel and an empirical dispersal kernel from that seascape both have the same shape, with a high level of short-distance dispersal and a low level of long-distance dispersal. The novel contributions of this work are to provide a spatially explicit analytic extension of Hamilton and May's 1977 work, to demonstrate that our spatially explicit simulations and analytic models provide equivalent results, and to use simulation approaches to investigate the evolution of dispersal kernel shape in spatially complex habitats. Our model could be modified in various ways to investigate dispersal evolution in other species and seascapes, providing new insights into patterns of marine larval dispersal.

The formation of marine kin structure: effects of dispersal, larval cohesion, and variable reproductive success.

The spatial distribution of relatives has profound effects on kin interactions, inbreeding, and inclusive fitness. Yet, in the marine environment, the processes that generate patterns of kin structure remain understudied because larval dispersal on ocean currents was historically assumed to disrupt kin associations. Recent genetic evidence of co-occurring siblings challenges this assumption and raises the intriguing question of how siblings are found together after a (potentially) disruptive larval phase. Here, we develop individual-based models to explore how stochastic processes operating at the individual level affect expected kinship at equilibrium. Specifically, we predict how limited dispersal, sibling cohesion, and variability in reproductive success differentially affect patterns of kin structure. All three mechanisms increase mean kinship within populations, but their spatial effects are markedly different. We find that (1) when dispersal is limited, kinship declines monotonically as a function of the distance between individuals; (2) when siblings disperse cohesively, kinship increases within a site relative to between sites; and (3) when reproductive success varies, kinship increases equally at all distances. The differential effects of these processes therefore only become apparent when individuals are sampled at multiple spatial scales. Notably, our models suggest that aggregative larval behaviors, such as sibling cohesion, are not necessary to explain documented levels of relatedness within marine populations. Together, these findings establish a theoretical framework for disentangling the drivers of marine kin structure.

Patterns, causes, and consequences of marine larval dispersal.

Quantifying the probability of larval exchange among marine populations is key to predicting local population dynamics and optimizing networks of marine protected areas. The pattern of connectivity among populations can be described by the measurement of a dispersal kernel. However, a statistically robust, empirical dispersal kernel has been lacking for any marine species. Here, we use genetic parentage analysis to quantify a dispersal kernel for the reef fish Elacatinus lori, demonstrating that dispersal declines exponentially with distance. The spatial scale of dispersal is an order of magnitude less than previous estimates-the median dispersal distance is just 1.7 km and no dispersal events exceed 16.4 km despite intensive sampling out to 30 km from source. Overlaid on this strong pattern is subtle spatial variation, but neither pelagic larval duration nor direction is associated with the probability of successful dispersal. Given the strong relationship between distance and dispersal, we show that distance-driven logistic models have strong power to predict dispersal probabilities. Moreover, connectivity matrices generated from these models are congruent with empirical estimates of spatial genetic structure, suggesting that the pattern of dispersal we uncovered reflects long-term patterns of gene flow. These results challenge assumptions regarding the spatial scale and presumed predictors of marine population connectivity. We conclude that if marine reserve networks aim to connect whole communities of fishes and conserve biodiversity broadly, then reserves that are close in space (<10 km) will accommodate those members of the community that are short-distance dispersers.

Genetic models reveal historical patterns of sea lamprey population fluctuations within Lake Champlain.

The origin of sea lamprey (Petromyzon marinus) in Lake Champlain has been heavily debated over the past decade. Given the lack of historical documentation, two competing hypotheses have emerged in the literature. First, it has been argued that the relatively recent population size increase and concomitant rise in wounding rates on prey populations are indicative of an invasive population that entered the lake through the Champlain Canal. Second, recent genetic evidence suggests a post-glacial colonization at the end of the Pleistocene, approximately 11,000 years ago. One limitation to resolving the origin of sea lamprey in Lake Champlain is a lack of historical and current measures of population size. In this study, the issue of population size was explicitly addressed using nuclear (nDNA) and mitochondrial DNA (mtDNA) markers to estimate historical demography with genetic models. Haplotype network analysis, mismatch analysis, and summary statistics based on mtDNA noncoding sequences for NCI (479 bp) and NCII (173 bp) all indicate a recent population expansion. Coalescent models based on mtDNA and nDNA identified two potential demographic events: a population decline followed by a very recent population expansion. The decline in effective population size may correlate with land-use and fishing pressure changes post-European settlement, while the recent expansion may be associated with the implementation of the salmonid stocking program in the 1970s. These results are most consistent with the hypothesis that sea lamprey are native to Lake Champlain; however, the credibility intervals around parameter estimates demonstrate that there is uncertainty regarding the magnitude and timing of past demographic events.

Marine ecology: reaping the benefits of local dispersal.

A central question of marine ecology is, how far do larvae disperse? Evidence is accumulating that the probability of dispersal declines rapidly with distance. This provides an incentive for communities to manage their own fish stocks and cooperate with neighbors.