Genetic decline and recovery of a demographically rebuilt fishery species.

The demographic history of a population is important for conservation and evolution, but this history is unknown for many populations. Methods that use genomic data have been developed to infer demography, but they can be challenging to implement and interpret, particularly for large populations. Thus, understanding if and when genetic estimates of demography correspond to true population history is important for assessing the performance of these genetic methods. Here, we used double-digest restriction-site associated DNA (ddRAD) sequencing data from archived collections of larval summer flounder (Paralichthys dentatus, n = 279) from three cohorts (1994-1995, 1997-1998 and 2008-2009) along the U.S. East coast to examine how contemporary effective population size and genetic diversity responded to changes in abundance in a natural population. Despite little to no detectable change in genetic diversity, coalescent-based demographic modelling from site frequency spectra revealed that summer flounder effective population size declined dramatically in the early 1980s. The timing and direction of change corresponded well with the observed decline in spawning stock census abundance in the late 1980s from independent fish surveys. Census abundance subsequently recovered and achieved the prebottleneck size. Effective population size also grew following the bottleneck. Our results for summer flounder demonstrate that genetic sampling and site frequency spectra can be useful for detecting population dynamics, even in species with large effective sizes.

Genomic signatures of spatially divergent selection at clownfish range margins.

Understanding how evolutionary forces interact to drive patterns of selection and distribute genetic variation across a species' range is of great interest in ecology and evolution, especially in an era of global change. While theory predicts how and when populations at range margins are likely to undergo local adaptation, empirical evidence testing these models remains sparse. Here, we address this knowledge gap by investigating the relationship between selection, gene flow and genetic drift in the yellowtail clownfish, Amphiprion clarkii, from the core to the northern periphery of the species range. Analyses reveal low genetic diversity at the range edge, gene flow from the core to the edge and genomic signatures of local adaptation at 56 single nucleotide polymorphisms in 25 candidate genes, most of which are significantly correlated with minimum annual sea surface temperature. Several of these candidate genes play a role in functions that are upregulated during cold stress, including protein turnover, metabolism and translation. Our results illustrate how spatially divergent selection spanning the range core to the periphery can occur despite the potential for strong genetic drift at the range edge and moderate gene flow from the core populations.

Using multiple natural tags provides evidence for extensive larval dispersal across space and through time in summer flounder.

Dispersal sets the fundamental scales of ecological and evolutionary dynamics and has important implications for population persistence. Patterns of marine dispersal remain poorly understood, partly because dispersal may vary through time and often homogenizes allele frequencies. However, combining multiple types of natural tags can provide more precise dispersal estimates, and biological collections can help to reconstruct dispersal patterns through time. We used single nucleotide polymorphism genotypes and otolith core microchemistry from archived collections of larval summer flounder (Paralichthys dentatus, n = 411) captured between 1989 and 2012 at five locations along the US East coast to reconstruct dispersal patterns through time. Neither genotypes nor otolith microchemistry alone were sufficient to identify the source of larval fish. However, microchemistry identified clusters of larvae (n = 3-33 larvae per cluster) that originated in the same location, and genetic assignment of clusters could be made with substantially more confidence. We found that most larvae probably originated near a biogeographical break (Cape Hatteras) and that larvae were transported in both directions across this break. Larval sources did not shift north through time, despite the northward shift of adult populations in recent decades. Our novel approach demonstrates that summer flounder dispersal is widespread throughout their range, on both intra- and intergenerational timescales, and may be a particularly important process for synchronizing population dynamics and maintaining genetic diversity during an era of rapid environmental change. Broadly, our results reveal the value of archived collections and of combining multiple natural tags to understand the magnitude and directionality of dispersal in species with extensive gene flow.

Genomic signatures of environmental selection despite near-panmixia in summer flounder.

Rapid environmental change is altering the selective pressures experienced by marine species. While adaptation to local environmental conditions depends on a balance between dispersal and natural selection across the seascape, the spatial scale of adaptation and the relative importance of mechanisms maintaining adaptation in the ocean are not well understood. Here, using population assignment tests, Approximate Bayesian Computation (ABC), and genome scans with double-digest restriction-site associated DNA sequencing data, we evaluated population structure and locus-environment associations in a commercially important species, summer flounder (Paralichthys dentatus), along the U.S. east coast. Based on 1,137 single nucleotide polymorphisms across 232 individuals spanning nearly 1,900 km, we found no indication of population structure across Cape Hatteras, North Carolina (F ST = 0.0014) or of isolation by distance along the coast using individual relatedness. ABC estimated the probability of dispersal across the biogeographic break at Cape Hatteras to be high (95% credible interval: 7%-50% migration). However, we found 15 loci whose allele frequencies were associated with at least one of four environmental variables. Of those, 11 were correlated with bottom temperature. For summer flounder, our results suggest continued fisheries management as a single population and identify likely response mechanisms to climate change. Broadly speaking, our findings suggest that spatial balancing selection can manifest in adaptive divergence on regional scales in marine fish despite high dispersal, and that these conditions likely result in the widespread distribution of adaptive alleles and a high potential for future genetic adaptation in response to changing environmental conditions. In the context of a rapidly changing world, a landscape genomics perspective offers a useful approach for understanding the causes and consequences of genetic differentiation.

Persistent carry-over effects of planktonic exposure to ocean acidification in the Olympia oyster.

Predicting impacts of global environmental change is challenging due to the complex life cycles that characterize many terrestrial and aquatic taxa. Different life stages often interact with the physical environment in distinct ways, and a growing body of work suggests that stresses experienced during one life stage can "carry over" to influence subsequent stages. Assessments of population responses to environmental perturbation must therefore consider how effects might propagate across life-history transitions. We investigated consequences of ocean acidification (decreased pH and carbonate saturation) for early life stages of the Olympia oyster (Ostrea lurida), a foundation species in estuaries along the Pacific coast of North America. We reared oysters at three levels of seawater pH, including a control (8.0) and two additional levels (7.9 and 7.8). Oysters were cultured through their planktonic larval period to metamorphosis and into early juvenile life. Larvae reared under pH 7.8 exhibited a 15% decrease in larval shell growth rate, and a 7% decrease in shell area at settlement, compared to larvae reared under control conditions. Impacts were even more pronounced a week after settlement, with juveniles that had been reared as larvae under reduced pH exhibiting a 41% decrease in shell growth rate. Importantly, the latter effect arose regardless of the pH level the oysters experienced as juveniles, indicating a strong carry-over effect from the larval phase. Adverse impacts of early exposure to low pH persisted for at least 1.5 months after juveniles were transferred to a common environment. Overall, our results suggest that a stringent focus on a single phase of the life cycle (e.g., one perceived as the "weakest link") may neglect critical impacts that can be transferred across life stages in taxa with complex life histories.