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Pespeni, M. H.

Publications and source records attributed to Pespeni, M. H..

8 recordsLinked to original sources

Revealing the abiotic and biotic drivers of past and future local adaptation in a coastal dogwhelk

Predicting whether populations can persist under rapid environmental change requires identifying the ecological drivers of local adaptation, uncovering their genetic bases, and understanding how adaptive variation will respond to future selection. Here, we combine landscape genomics, environmental data, and evolutionary simulations to identify the selective forces shaping adaptation across 1,500 km of the west coast of North America in the low-dispersing coastal dogwhelk Nucella canaliculata, determine their genomic bases, and forecast future evolutionary responses. We found strong associations of genome-wide variation with both abiotic (i.e., mean pH) and biotic variation (i.e., cross-sectional shell thickness of the mussel prey species, Mytilus californianus). These patterns are underlain by two large-effect loci, including a biomineralization gene associated with pH tolerance and a locus near a thiamine transporter associated with prey shell thickness. Genomic offset analyses and population genetic simulations further predict that ongoing ocean acidification will disrupt existing adaptive patterns and generate maladaptation in high latitude populations, with evolutionary outcomes strongly influenced by gene flow, which determines the rate at which adaptive alleles spread across the species range. Together, these findings reveal how biotic and abiotic selective pressures shape adaptive genomic variation and provide a framework for forecasting evolutionary responses to future global change.

evolutionary biology↗

A novel CTmax assay reveals divergent thermal acclimation capacity across three ecologically distinct sea urchins

Global change is driving rapid ocean warming, exposing organisms to both chronic temperature increases and acute marine heatwaves. Understanding how species cope with thermal stress is critical for predicting ecosystem resilience. Echinoderms are globally distributed and often function as foundational species, yet comparative assessments of upper thermal tolerance among species occupying contrasting thermal environments remain limited. Here, we address this gap by comparing upper thermal tolerance across three sea urchins with distinct biogeographic distributions: the latitudinally broad purple sea urchin (Strongylocentrotus purpuratus), the circumpolar green sea urchin (S. droebachiensis), and the tropical variegated sea urchin (Lytechinus variegatus). We quantified thermal limits after two acclimation treatments: ambient temperatures approximating native habitat conditions for each species and an elevated temperature (+6 C). We developed a novel assay to measure critical thermal maximum (CTmax), comparing variability and inconsistencies associated among multiple assays. Upper thermal tolerance increased with acclimation to elevated temperatures in all three species, but acclimatory capacity differed markedly, with S. droebachiensis showing the strongest response and S. purpuratus the weakest. Conversely, S. purpuratus had the highest thermal safety margin and thus the lowest proximity to its thermal ceiling. Our adhesion based CTmax method was more reproducible and the most precise compared to other metrics tested, providing an improved framework for quantifying physiological thermal limits of sea urchins. Together, these findings reveal substantial but unevenly distributed thermal resilience in ecologically diverse sea urchins, advancing our understanding of how foundational marine species may respond to future global change.

evolutionary biology↗

Evidence of Adaptation in Structural Variants among Wild Populations of the purple sea urchin, Strongylocentrotus purpuratus

Structural variants (SVs) are increasingly recognized as important components of genetic architecture, complementing and extending beyond traditionally studied single nucleotide polymorphisms. Though growing, our understanding of the evolutionary forces maintaining SVs in natural populations is limited. Chromosomal inversions in particular can facilitate local adaptation in populations with high gene flow, including many marine species. The purple sea urchin (Strongylocentrotus purpuratus) is a powerful system to study these dynamics due to its high gene flow, lack of population structure, and broad latitudinal range. We analyzed whole genome sequence data from 137 individuals from seven populations to identify structural variants using local PCA, linkage disequilibrium, and FST analyses. We integrated Bayesian selection scans and population genetic statistics to test for signatures of selection in putative inversions. We identified nine loci showing signatures consistent with inversion polymorphisms, including three-way genotype clustering, long range linkage, and the characteristic hanging-bridge pattern. These loci are polymorphic within sites and along the species range with three loci showing concordant signatures of selection based on enrichment of XTX outliers and distinct patterns of allelic age consistent with positive and balancing selection. In addition, these loci show enrichment for genes associated with biomineralization and development. Our results are the first instance of identifying putative inversions in the purple sea urchin, adding to the genomic repertoire of this model species. Our results add to the growing evidence that chromosomal inversions are a key component of standing genetic variation in natural populations with an important role in adaptation to heterogeneous environments. Significance statementChromosomal inversion polymorphisms are an important part of the repertoire of standing genetic variation in wild populations and can facilitate adaptation in the face of strong gene flow. The purple sea urchin, a widely studied marine species, exhibits high gene flow, large population sizes, and extensive genetic diversity across diverse environmental conditions, making it an ideal model for evolutionary genomics. We identified nine putative inversions, three with signatures of selection, adding echinoderms to the growing list of phyla with putatively adaptive inversions. These findings provide new insights into structural variation in a highly dispersive marine species and highlight potential evolutionary mechanisms maintaining these polymorphisms.

evolutionary biology↗

Experimental evolution reveals the synergistic genomic mechanisms of adaptation to ocean warming and acidification in a marine copepod

Metazoan adaptation to global change will rely on selection of standing genetic variation. Determining the extent to which this variation exists in natural populations, particularly for responses to simultaneous stressors, is therefore essential to make accurate predictions for persistence in future conditions. Here, we identify the genetic variation enabling the copepod Acartia tonsa to adapt to experimental ocean warming, acidification, and combined ocean warming and acidification (OWA) conditions over 25 generations. Replicate populations showed a strong and 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 genomic changes into selection, drift, and lab adaptation and found that the majority of allele frequency change in warming (56%) and OWA (63%) was driven by selection but acidification was dominated by drift (66%). OWA and warming shared 37% of their response to selection but OWA and acidification shared just 1%. Accounting for lab adaptation was essential for not inflating a shared response to selection between all treatments. Finally, the mechanisms of adaptation in the multiple-stressor OWA conditions were not an additive product of warming and acidification, but rather a synergistic response where 47% of the allelic responses to selection were unique. These results are among the first to disentangle how the genomic targets of selection differ between single and multiple stressors and to demonstrate the complexity that non-additive multiple stressors will contribute to attempts to predict adaptive responses to complex environments.

evolutionary biology↗

Rapid, but limited, zooplankton adaptation to simultaneous warming and acidification

Predicting the response of marine metazoans to climate change is hampered by a lack of studies on evolutionary adaptation, particularly to combined ocean warming and acidification (OWA). We provide evidence for rapid adaptation to OWA in the foundational copepod species, Acartia tonsa, by assessing changes in population fitness based on a comprehensive suite of life-history traits, using an orthogonal experimental design of nominal temperature (18{degrees}C, 22{degrees}C) and pCO2 (400, 2000 atm) for 25 generations (~1 year). Egg production and hatching success initially decreased under OWA, resulting in a 56% reduction in fitness. However, both traits recovered by the third generation and average fitness was reduced thereafter by only 9%. Antagonistic interactions between warming and acidification in later generations decreased survival, thereby limiting full fitness recovery. Our results suggest such interactions constrain evolutionary rescue and add complexity to predictions of the responses of metazoan populations to climate change.

evolutionary biology↗

Global change adaptation limits future resilience

Adaptive evolution from standing genetic variation and physiological plasticity will fuel resilience in the geologically unprecedented warming and acidification of the earths oceans. For marine animals, however, we have much to learn about the mechanisms, interactions, and costs of adaptation. Here, using 20 generations of experimental evolution followed by three generations of reciprocal transplantation, we investigate the relationship between adaptation and plasticity in the marine copepod, Acartia tonsa, in future greenhouse conditions (high temperature, high CO2). We find highly parallel genetic adaptation to greenhouse conditions in genes related to stress response, gene expression regulation, actin regulation, developmental processes, and energy production. However, reciprocal transplantation showed that genetic adaptation resulted in a loss of transcriptional plasticity, reduced fecundity, and reduced population growth when greenhouse animals were returned to ambient conditions or reared in low food conditions, suggestive of genetic assimilation after 20 generations of adaptation. Despite the loss of plasticity at F21, after three successive transplant generations, greenhouse-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 the power of experimental evolution from natural populations to reveal the mechanisms, timescales of responses, consequences, and reversibility of complex, physiological adaptation. While plasticity facilitated initial survival in global change conditions, it eroded after 20 generations as populations genetically adapted, limiting resilience to new stressors and previously benign environments.

evolutionary biology↗

Rare genetic variation is important for survival in extreme low pH conditions

Standing genetic variation is important for population persistence in extreme environmental conditions. While some species may have the capacity to adapt to predicted average future global change conditions, the ability to survive extreme events is largely unknown. We used single generation selection experiments on hundreds of thousands of Strongylocentrotus purpuratus sea urchin larvae generated from wild-caught adults to identify adaptive genetic variation responsive to moderate (pH 8.0) and extreme (pH 7.5) low pH conditions. Sequencing genomic DNA from pools of larvae, we identified consistent changes in allele frequencies across replicate cultures of both conditions and observed increased linkage disequilibrium around selected loci, revealing selection on recombined standing genetic variation. We found that loci responding uniquely to either selection regime were at low starting allele frequencies while variants that responded to both pH conditions (11.6% of selected variants) started at high frequencies. Loci under selection performed functions related to energetics, pH tolerance, cell growth, and actin/cytoskeleton dynamics. These results highlight that persistence in future conditions will require two classes of genetic variation: common, pH-responsive variants maintained by balancing selection in a heterogeneous environment, and rare variants, particularly for extreme conditions, that must be maintained by large population sizes.

evolutionary biology↗

Gene expression across tissues, sex, and life stages in the sea urchin Tripneustes gratilla

The pan-tropical sea urchin Tripneustes gratilla is an ecologically and economically important shallow water algal grazer. The aquaculture of T. gratilla has spurred growing interest in the population biology of the species, and by extension the generation of more molecular resources. To this purpose, de novo transcriptomes of T. gratilla were generated for two adults, a male and a female, as well as for a cohort of approximately 1,000 plutei larvae. Gene expression profiles of three adult tissue samples were quantified and compared. These samples were of gonadal tissue, the neural ring, and pooled tube feet and pedicellariae. Levels of shared and different gene expression between sexes, as well as across functional categories of interest, including the immune system, toxins, genes involved in fertilization, and sensory genes are highlighted. Differences in expression of Sex determining Region Y-related High Mobility Group box groups and general isoform expression between the sexes is observed. Additionally an expansion of the tumor suppressor DMBT1 was observed in T. gratilla when compared to the annotated genome of the sea urchin Strongylocentrotus purpuratus. The draft transcriptome of T. gratilla is presented here in order to facilitate more genomic level analysis of de-novo sea urchin systems.

molecular biology↗