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Gene regulatory divergence is thought to play an important role in adaptation, yet its extent and underlying mechanisms remain largely elusive for local adaptation with gene flow. Local adaptation is widespread in marine species despite generally high connectivity and is often associated with tightly linked genomic architectures, such as chromosomal inversions. To investigate gene regulatory evolution under gene flow and the role of inversions associated with local adaptation to a steep thermal gradient, we generated RNA-seq data from Atlantic silversides (Menidia menidia) from two locally adapted populations and their F1 hybrids, reared under two temperatures. We found substantial divergence in gene expression and thermal plasticity between populations, with up to 31% of genes being differentially expressed. Reduced thermal plasticity, temperature-dependent gene misexpression, and the disruption of coexpression networks in hybrids point toward a role of regulatory incompatibilities in local adaptation, particularly under colder temperatures. Chromosomal inversions show an accumulation of regulatory incompatibilities but are not consistently enriched for differentially expressed genes. Together, these results suggest that gene regulation can diverge substantially among populations despite gene flow, partly due to the accumulation of temperature-dependent regulatory incompatibilities within inversions.

 

Metazoan adaptation to global change relies on selection of standing genetic variation. Determining the extent to which this variation exists in natural populations, particularly for responses to simultaneous stressors, is essential to make accurate predictions for persistence in future conditions. Here, we identified the genetic variation enabling the copepod Acartia tonsa to adapt to experimental ocean warming, acidification, and combined ocean warming and acidification (OWA) over 25 generations of continual selection. Replicate populations showed a consistent polygenic response to each condition, targeting an array of adaptive mechanisms including cellular homeostasis, development, and stress response. We used a genome-wide covariance approach to partition the allelic changes into three categories: selection, drift and replicate-specific selection, and laboratory adaptation responses. The majority of allele frequency change in warming (57%) and OWA (63%) was driven by shared selection pressures across replicates, but this effect was weaker under acidification alone (20%). OWA and warming shared 37% of their response to selection but OWA and acidification shared just 1%, indicating that warming is the dominant driver of selection in OWA. Despite the dominance of warming, the interaction with acidification was still critical as the OWA selection response was highly synergistic with 47% of the allelic selection response unique from either individual treatment. These results disentangle how genomic targets of selection differ between single and multiple stressors and demonstrate the complexity that nonadditive multiple stressors will contribute to predictions of adaptation to complex environmental shifts caused by global change. 

Northern sand lance (Ammodytes dubius) are essential forage fish in most offshore, temperate-to-polar waters on the Northwest Atlantic shelf (NWA), but their population structure and genetic separation from the American sand lance (A. americanus) remain unresolved. We assembled a reference genome for A. dubius (first in the Ammodytidae) and then used low-coverage whole genome sequencing on 262 specimens collected across the species distribution (Mid-Atlantic Bight to Greenland) to quantify genetic differentiation between geographic regions based on single nucleotide polymorphisms. We found strong separation between A. dubius from locations north and south of the Scotian Shelf, largely due to massive genetic differentiation spanning most of chromosomes 21 and 24. Genetic distance increased with geographic distance in the smaller southern cluster but not in the larger northern cluster, where genetic homogeneity appeared across large geographic distances (>103 km). The two genetic clusters coincide with a clear break in winter sea surface temperature, suggesting that differential offspring survival, rather than limited transport, causes a break in realized connectivity. Nuclear and mitochondrial DNA both clearly delineated A. dubius from A. americanus, thereby confirming a species boundary through spatial niche partitioning into inshore (A. americanus) and offshore (A. dubius) sand lance species on the NWA.

 

This dataset includes hatch and larval period for sand lance collected in 2019 and results from particle tracking runs of simulated sand lance larvae throughout the Northeast U.S. Shelf as part of Long-Term Ecological Research (NES-LTER). Release dates vary by region, corresponding to hatch and settlement dates of settling sand lance collected in 2019. Particles were depth-keeping throughout the upper 40 m to best replicate our understanding of the vertical distribution of sand lance larvae. Data were used to determine the average particle transport pathways from these sand lance habitats, including connectivity among the three hotspots, and spatial variability of connectivity within each hotspot. Further information can be found within the manuscript: Suca, J. J., Ji, R., Baumann, H., Pham, K., Silva, T. L., Wiley, D. N., Feng, Z., & Llopiz, J. K. (2022). Larval transport pathways from three prominent sand lance habitats in the Gulf of Maine. Fisheries Oceanography, 31( 3), 333-352. https://doi.org/10.1111/fog.12580 

Adaptive evolution and phenotypic plasticity will fuel resilience in the geologically unprecedented warming and acidification of the earth’s oceans, however, we have much to learn about the interactions and costs of these mechanisms of resilience. Here, using 20 generations of experimental evolution followed by three generations of reciprocal transplants, we investigated the relationship between adaptation and plasticity in the marine copepod,Acartia tonsa, in future global change conditions (high temperature and high CO₂). We found parallel adaptation to global change conditions in genes related to stress response, gene expression regulation, actin regulation, developmental processes, and energy production. However, reciprocal transplantation showed that adaptation resulted in a loss of transcriptional plasticity, reduced fecundity, and reduced population growth when global change-adapted animals were returned to ambient conditions or reared in low food conditions. However, after three successive transplant generations, global change-adapted animals were able to match the ambient-adaptive transcriptional profile. Concurrent changes in allele frequencies and erosion of nucleotide diversity suggest that this recovery occurred via adaptation back to ancestral conditions. These results demonstrate that while plasticity facilitated initial survival in global change conditions, it eroded after 20 generations as populations adapted, limiting resilience to new stressors and previously benign environments.

 

Abstract Experiments examining fish sensitivities to future oceanic CO2 levels have greatly expanded over past decades and identified many potentially affected traits. Curiously, data on reproductive trait responses to high CO2 are still scarce, despite their strong link to Darwinian fitness and thus to population vulnerability to ocean acidification. We conducted two rearing experiments on the first broadcast-spawning marine fish model (Atlantic silverside, Menidia menidia) to examine how long-term and novel whole life-cycle exposures to predicted future CO2 levels (∼2,000 µatm) affect laboratory spawning, temperature-specific reproductive investment, fecundity, and size distributions of maturing oocytes. At low temperatures (17°C), female body size and therefore potential fecundity (FPot, oocytes/female) slightly increased with CO2, while relative fecundity (FRel, oocytes/g female) remained unaffected. At high temperatures (24°C), high CO2 substantially reduced both FPot (−19%) and FRel (−28%) relative to control treatments. Irrespective of CO2, females at 24°C grew larger and heavier than those at 17°C, and although larger females produced larger oocytes at some developmental stages, they also had lower gonadosomatic indices and lower FRel. Our findings contrast with most previous studies and thus highlight the need to investigate reproductive impacts of increasing CO2 on multiple fish species with contrasting life history strategies.