Loss of plasticity in maturation timing after ten years of captive spawning in a delta smelt conservation hatchery.

Adaptation to captivity in spawning programs can lead to unintentional consequences, such as domestication that results in reduced fitness in the wild. The timing of sexual maturation has been shown to be a trait under domestication selection in fish hatcheries, which affects a fish's access to mating opportunities and aligning their offspring's development with favorable environmental conditions. Earlier maturing fish may be favored in hatchery settings where managers provide artificially optimal growing conditions, but early maturation may reduce fitness in the wild if, for example, there is a mismatch between timing of reproduction and availability of resources that support recruitment. We investigated patterns of maturation timing in a delta smelt (Hypomesus transpacificus) conservation hatchery by quantifying changes to the median age at maturity since the captive spawning program was initiated in 2008. Over the span of a decade, we observed a small, but significant increase in age at maturity among broodstock by 2.2 weeks. This trait had low heritability and was largely controlled by phenotypic plasticity that was dependent on the time of year fish were born. Fish that were born later in the year matured faster, potentially a carryover from selection favoring synchronous spawning in the wild. However, higher DI (domestication index) fish showed a loss of plasticity, we argue, as a result of hatchery practices that breed individuals past peak periods of female ripeness. Our findings suggest that the hatchery setting has relaxed selection pressures for fish to mature quickly at the end of the year and, consequently, has led to a loss of plasticity in age at maturity. Hatchery fish that are re-introduced in the wild may not be able to align maturation with population peaks if their maturation rates are too slow with reduced plasticity, potentially resulting in lower fitness.

A draft reference genome of the red abalone, Haliotis rufescens, for conservation genomics.

Red abalone, Haliotis rufescens, are herbivorous marine gastropods that primarily feed on kelp. They are the largest and longest-lived of abalone species with a range distribution in North America from central Oregon, United States, to Baja California, MEX. Recently, red abalone have been in decline as a consequence of overharvesting, disease, and climate change, resulting in the closure of the commercial fishery in the 1990s and the recreational fishery in 2018. Protecting this ecologically and economically important species requires an understanding of their current population dynamics and connectivity. Here, we present a new red abalone reference genome as part of the California Conservation Genomics Project (CCGP). Following the CCGP genome strategy, we used Pacific Biosciences HiFi long reads and Dovetail Omni-C data to generate a scaffold-level assembly. The assembly comprises 616 scaffolds for a total size of 1.3 Gb, a scaffold N50 of 45.7 Mb, and a BUSCO complete score of 97.3%. This genome represents a significant improvement over a previous assembly and will serve as a powerful tool for investigating seascape genomic diversity, local adaptation to temperature and ocean acidification, and informing management strategies.

Evolutionary Change in the Eastern Oyster, Crassostrea Virginica, Following Low Salinity Exposure.

The presence of standing genetic variation will play a role in determining a population's capacity to adapt to environmentally relevant stressors. In the Gulf of Mexico, extreme climatic events and anthropogenic changes to local hydrology will expose productive oyster breeding grounds to stressful low salinity conditions. We identified genetic variation for performance under low salinity (due to the combined effects of low salinity and genetic load) using a single-generation selection experiment on larvae from two populations of the eastern oyster, Crassostrea virginica. We used pool-sequencing to test for allele frequency differences at 152 salinity-associated genes for larval families pre- and post-low salinity exposure. Our results have implications for how evolutionary change occurs during early life history stages at environmentally relevant salinities. Consistent with observations of high genetic load observed in oysters, we demonstrate evidence for purging of deleterious alleles at the larval stage in C. virginica. In addition, we observe increases in allele frequencies at multiple loci, suggesting that natural selection for low salinity performance at the larval stage can act as a filter for genotypes found in adult populations.

Selection Experiments in the Sea: What Can Experimental Evolution Tell Us About How Marine Life Will Respond to Climate Change?

AbstractRapid evolution may provide a buffer against extinction risk for some species threatened by climate change; however, the capacity to evolve rapidly enough to keep pace with changing environments is unknown for most taxa. The ecosystem-level consequences of climate adaptation are likely to be the largest in marine ecosystems, where short-lived phytoplankton with large effective population sizes make up the bulk of primary production. However, there are substantial challenges to predicting climate-driven evolution in marine systems, including multiple simultaneous axes of change and considerable heterogeneity in rates of change, as well as the biphasic life cycles of many marine metazoans, which expose different life stages to disparate sources of selection. A critical tool for addressing these challenges is experimental evolution, where populations of organisms are directly exposed to controlled sources of selection to test evolutionary responses. We review the use of experimental evolution to test the capacity to adapt to climate change stressors in marine species. The application of experimental evolution in this context has grown dramatically in the past decade, shedding light on the capacity for evolution, associated trade-offs, and the genetic architecture of stress-tolerance traits. Our goal is to highlight the utility of this approach for investigating potential responses to climate change and point a way forward for future studies.

Transgenerational plasticity and the capacity to adapt to low salinity in the eastern oyster, Crassostrea virginica.

Salinity conditions in oyster breeding grounds in the Gulf of Mexico are expected to drastically change due to increased precipitation from climate change and anthropogenic changes to local hydrology. We determined the capacity of the eastern oyster, Crassostrea virginica, to adapt via standing genetic variation or acclimate through transgenerational plasticity (TGP). We outplanted oysters to either a low- or medium-salinity site in Louisiana for 2 years. We then crossed adult parents using a North Carolina II breeding design, and measured body size and survival of larvae 5 dpf raised under low or ambient salinity. We found that TGP is unlikely to significantly contribute to low-salinity tolerance since we did not observe increased growth or survival in offspring reared in low salinity when their parents were also acclimated at a low-salinity site. However, we detected genetic variation for body size, with an estimated heritability of 0.68 ± 0.25 (95% CI). This suggests there is ample genetic variation for this trait to evolve, and that evolutionary adaptation is a possible mechanism through which oysters will persist with future declines in salinity. The results of this experiment provide valuable insights into successfully breeding low-salinity tolerance in this commercially important species.

An Experimental Test of Adaptive Introgression in Locally Adapted Populations of Splash Pool Copepods.

As species struggle to keep pace with the rapidly warming climate, adaptive introgression of beneficial alleles from closely related species or populations provides a possible avenue for rapid adaptation. We investigate the potential for adaptive introgression in the copepod, Tigriopus californicus, by hybridizing two populations with divergent heat tolerance limits. We subjected hybrids to strong heat selection for 15 generations followed by whole-genome resequencing. Utilizing a hybridize evolve and resequence (HER) technique, we can identify loci responding to heat selection via a change in allele frequency. We successfully increased the heat tolerance (measured as LT50) in selected lines, which was coupled with higher frequencies of alleles from the southern (heat tolerant) population. These repeatable changes in allele frequencies occurred on all 12 chromosomes across all independent selected lines, providing evidence that heat tolerance is polygenic. These loci contained genes with lower protein-coding sequence divergence than the genome-wide average, indicating that these loci are highly conserved between the two populations. In addition, these loci were enriched in genes that changed expression patterns between selected and control lines in response to a nonlethal heat shock. Therefore, we hypothesize that the mechanism of heat tolerance divergence is explained by differential gene expression of highly conserved genes. The HER approach offers a unique solution to identifying genetic variants contributing to polygenic traits, especially variants that might be missed through other population genomic approaches.

Differential responses to ocean acidification between populations of Balanophyllia elegans corals from high and low upwelling environments.

Ocean acidification (OA), the global decrease in surface water pH from absorption of anthropogenic CO2 , may put many marine taxa at risk. However, populations that experience extreme localized conditions, and are adapted to these conditions predicted in the global ocean in 2,100, may be more tolerant to future OA. By identifying locally adapted populations, researchers can examine the mechanisms used to cope with decreasing pH. One oceanographic process that influences pH is wind-driven upwelling. Here we compare two Californian populations of the coral Balanophyllia elegans from distinct upwelling regimes, and test their physiological and transcriptomic responses to experimental seawater acidification. We measured respiration rates, protein and lipid content, and gene expression in corals from both populations exposed to pH levels of 7.8 and 7.4 for 29 days. Corals from the population that experiences lower pH due to high upwelling maintained the same respiration rate throughout the exposure. In contrast, corals from the low upwelling site had reduced respiration rates, protein content and lipid-class content at low pH exposure, suggesting they have depleted their energy reserves. Using RNA-Seq, we found that corals from the high upwelling site upregulated genes involved in calcium ion binding and ion transport, most likely related to pH homeostasis and calcification. In contrast, corals from the low upwelling site downregulated stress response genes at low pH exposure. Divergent population responses to low pH observed in B. elegans highlight the importance of multi-population studies for predicting a species' response to future OA.