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Biology subjects

Brennan, R. S.

Publications and source records attributed to Brennan, R. S..

11 recordsLinked to original sources

Pollution-Driven Selection in Riparian Ecosystems: Genome-Wide Responses to Bacillus thuringiensis israelensis and Copper in a Non-biting Midge

Riparian ecosystems are vital interfaces between aquatic and terrestrial environments but are increasingly impacted by anthropogenic pollution. In these systems, merolimnic insects serve as crucial ecological links, occupying aquatic habitats as larvae and terrestrial environments as adults, thus being an essential food source in both. Consequently, pollutant exposure during the aquatic larval stage can have cascading effects across ecosystem boundaries. While the ecological consequences of such exposure are well documented, the evolutionary potential of merolimnic insects to adapt to chronic pollution remains poorly understood. To address this, we previously conducted a selection experiment exposing populations of the non-biting midge Chironomus riparius to the mosquito larvicide Bacillus thuringiensis israelensis (Bti) or heavy metal copper over approximately eight generations, which revealed only limited evidence of consistent phenotypic adaptation. Here we use whole-genome sequencing of these populations to assess their genomic responses to chronic pollutant exposure. Despite similar phenotypic sensitivity in pre-exposed and naive populations, we detected distinct stressor-specific genomic responses. Copper exposure induced a significant genome-wide reduction in nucleotide diversity and evidence of selection-driven allele frequency changes, while Bti effects were dominated by heterogeneous, replicate-specific shifts, potentially reflecting drift or selection on multiple redundant pathways. Functional enrichment analyses indicated early-stage adaptation: immune- and apoptosis-related pathways were enriched under Bti, while metal detoxification and DNA repair pathways were enriched under copper, highlighting distinct adaptive mechanisms despite weak genome-wide signals of selection. Our findings demonstrate that Evolve and Resequencing approaches enable the detection of early genomic signals of adaptation even when phenotypic change is subtle or absent, offering a powerful framework for studying evolutionary responses to environmental pollution.

evolutionary biology↗

Local Adaptation and Transcriptomic Plasticity of the Copepod Acartia tonsa Under Low Salinity Stress

Salinity--an essential factor shaping marine species distributions--is rapidly shifting due to global change, yet the mechanisms of salinity tolerance and adaptation remain poorly understood. We investigated local adaptation in the calanoid copepod Acartia tonsa, a broadly distributed marine species that thrives in the brackish Baltic Sea. Using a common-garden design, we compared physiological and transcriptomic responses to low salinity between populations from the North Sea (>25 PSU) and the Baltic Sea (<15 PSU). Baltic copepods exhibited significantly higher survival under low salinity, indicating local adaptation. While both populations shared a core osmoregulatory strategy involving active ion transport and regulation of amino acids, transcriptomic profiles revealed population-specific differences. Baltic individuals showed a reduced overall gene expression response, yet maintained higher relative expression of osmoregulatory genes--suggesting higher plasticity and a primed response. In contrast, North Sea copepods exhibited broader transcriptional shifts, including downregulation of metabolic and developmental pathways after prolonged stress exposure, possibly reflecting energy conservation mechanisms. These findings reveal that A. tonsa possesses both a plastic osmoregulatory strategy and population-level adaptation that enable survival in extreme salinity conditions. While both populations tolerate short-term exposure to low salinity, local adaptation has enhanced the Baltic populations resilience. This suggests that A. tonsa is broadly tolerant of moderate climate-driven salinity declines across most of its distribution. However, our data also indicate potential range contractions in the lowest salinity zones of the Baltic Sea, underscoring the importance of identifying physiological and genetic thresholds in climate resilience studies.

molecular biology↗

Drivers of genetic diversity across the marine tree of life

Why do some species have more genetic diversity than others? This question is one of the greatest remaining mysteries in evolutionary biology, yet we still know little about what factors predict genetic diversity among species. Efforts to quantify diversity or understand its distribution have been hampered by a lack of genomic data analyzed in a consistent way with statistical approaches that can move beyond the population level to generate species-wide estimates of genetic diversity. We address this critical gap by generating standardized estimates of genomic-level genetic diversity for 93 species sampled over 9,000 localities. Because marine species have evolved a strikingly diverse array of biological traits that have long been hypothesized to affect species-level genetic diversity, we focus our study on marine taxa. For each species, we aggregated biotic traits related to life history and abiotic features of the species range. We show that genetic diversity increases with species range extent and planktonic dispersal. We hypothesize that these traits increase a species ability to avoid or recover from bottlenecks, thereby maintaining genetic diversity. Our findings provide insights into how biotic and abiotic factors interact to shape genomic variation in the ocean, and offer a predictive framework for understanding marine biodiversity in the face of global change. Significance statementSpecies exhibit vast trait diversity that allows populations to persist. However, diversity in these traits -- e.g., how organisms reproduce, disperse, and feed -- is not easily linked to what is known of genomic diversity, even in well-studied organisms. We investigate a diverse assemblage of marine species to begin to build a predictive framework for how species traits drive genomic diversity across the worlds oceans. We find that species with larger geographic ranges have higher genomic diversity. More dispersive species also harbor higher diversity, suggesting that greater dispersal facilitates resilience to environmental change. As available datasets increase, our ability to understand fundamental links between trait and genetic diversity and how they shape species responses to environmental change will continue to improve.

evolutionary biology↗

Thermal selection shifts genetic diversity and performance in blue mussel juveniles

Mussels from the genus Mytilus, key inhabitants of the benthos, are important for the aquaculture industry and one of the most sustainable sources of animal protein available. Species within the Mytilus edulis complex (M. edulis, M. galloprovincialis and M. trossulus) are commonly found in temperate regions globally and can easily hybridise whenever their geographic distributions overlap. In the Baltic Sea, populations are formed by M. edulis and M. trossulus hybrids with low levels of M. galloprovincialis introgression. Given the economic and ecological relevance of mussels, this study aimed to investigate mechanisms through which their resilience towards global warming may be fast-tracked. For this, we developed two cohorts of juvenile mussels (i.e. recently settled animals) from the Baltic Sea (Kiel, Germany), one exposed to an extreme heat event early in life and one naive to this stressor. Both cohorts were then exposed to experimental temperatures at the proposed upper thermal limit for this population, 21{degrees}C to 26{degrees}C, with animal performance measured after 25 days. We then assessed the impacts of thermal stress on the genetic composition of each cohort by genotyping 50 individuals using the blue mussel 60K SNP-array. We observed a significant increase in M. edulis genotypes together with a decrease in M. trossulus in the S cohort in comparison with NS juveniles. We also found that exposure to high temperature has an effect on the performance of mussel cohorts, reducing dry tissue weight of the selected individuals. Results from this study provide relevant insights on how selection through thermal stress impacts performance and genetic composition of blue mussel juveniles, with key implications for understanding and managing mussel populations under future warming scenarios.

genomics↗

Genomic Evidence of Fisheries Induced Evolution in Eastern Baltic cod

Humans have become one of the greatest evolutionary forces, and their perturbations are expected to elicit strong evolutionary responses. Accordingly, during (size) selective overharvesting of wild populations, marked phenotypic changes have been documented, while the evolutionary basis is often unresolved. Time-series collections combined with genomic tools present unique opportunities to study how evolutionary changes are manifested at the genome-wide level. Here, we take advantage of a unique temporal dataset from the overexploited Eastern Baltic cod (Gadus morhua) population that exhibited a 48% decrease in asymptotic body length over the last 25 years. A genome-wide association study revealed pronounced peaks of outliers linked to growth performance. The contributing loci showed signals of directional selection with significantly high autocovariance in the allele frequency and excessive intersections with regions of high Fst as well as genes relevant to growth and reproduction. Moreover, pattern of directional selection for ancestral haplotype of the well-known chromosomal inversions in Atlantic cod (on linkage group 12) was observed, while the double crossover ([~]1Mb) enharbouring the vitellogenin genes within this region showed signs of drift or balancing selection. Our results demonstrate evident response of the genome over a relatively short time frame and further underscore implications for fisheries management and conservation policy regarding the adaptive potential of marine populations.

evolutionary biology↗

Phenotypic Plasticity Drives Seasonal Thermal Tolerance in a Baltic Copepod

Seasonal changes in environmental conditions require substantial physiological responses for population persistence. Phenotypic plasticity is a common mechanism to tolerate these changes, but for organisms with short generation times rapid adaptation may also be a contributing factor. Here, we aimed to disentangle the impacts of adaptation from phenotypic plasticity on thermal tolerance of the calanoid copepod Acartia hudsonica collected throughout spring and summer of a single year. We used a common garden (11 {degrees}C and 18 {degrees}C) design to determine the relative impacts of plasticity versus adaptation. Acartia hudsonica were collected from five time points across the season and thermal tolerance was determined using critical thermal maximum (CTmax) followed by additional measurements after one generation of common garden. As sea surface temperature increased through the season, field collected individuals showed corresponding increases in thermal tolerance but decreases in body size. Despite different thermal tolerances of wild collections, common garden animals did not differ in CTmax within thermal treatments. Instead, there was evidence of phenotypic plasticity where higher temperatures were tolerated by the 18 {degrees}C versus the 11 {degrees}C treatment animals across all collections. Acclimation also had significant effects on body size, with higher temperatures resulting in smaller individuals, consistent with the temperature size rule. Therefore, the differences in thermal tolerance and body size observed in field collected A. hudsonica were likely driven by plasticity rather than adaptation. However, the observed decrease in body size suggests that nutrient availability and ecosystem functioning could be impacted if temperatures consistently increase with no change in copepod abundance. This is the first record of A. hudsonica in the Baltic Sea known to the authors. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=113 SRC="FIGDIR/small/551281v1_ufig1.gif" ALT="Figure 1"> View larger version (33K): org.highwire.dtl.DTLVardef@814a70org.highwire.dtl.DTLVardef@3e17f0org.highwire.dtl.DTLVardef@95cb3corg.highwire.dtl.DTLVardef@51eb1c_HPS_FORMAT_FIGEXP M_FIG Graphical Abstract C_FIG HighlightsPhenotypic Plasticity Drives Seasonal Thermal Tolerance in a Baltic Copepod Alexandra Hahn, Reid S. Brennan O_LIAcartia hudsonica shows strong seasonality in thermal tolerance. C_LIO_LIThe observed seasonal differences in CTmax are driven by phenotypic plasticity not adaptation. C_LIO_LIBody size in A. hudsonica is negatively correlated to environmental and developmental temperature. C_LIO_LIThis is the first record of A. hudsonica in the Baltic Sea known to the authors. C_LI

ecology↗

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↗

Genome-wide selection scans integrated with association mapping reveal mechanisms of physiological adaptation across a salinity gradient in killifish

Adaptive divergence between marine and freshwater environments is important in generating phyletic diversity within fishes, but the genetic basis of adaptation to freshwater habitats remains poorly understood. Available approaches to detect adaptive loci include genome scans for selection, but these can be difficult to interpret because of incomplete knowledge of the connection between genotype and phenotype. In contrast, genome wide association studies (GWAS) are powerful tools for linking genotype to phenotype, but offer limited insight into the evolutionary forces shaping variation. Here, we combine GWAS and selection scans to identify loci important in the adaptation of complex physiological traits to freshwater environments. We focused on freshwater (FW)-native and brackish water (BW)-native populations of the Atlantic killifish (Fundulus heteroclitus) as well as a population that is a natural admixture of these two populations. We measured phenotypes for multiple physiological traits that differ between populations and that may contribute to adaptation across osmotic niches (salinity tolerance, hypoxia tolerance, metabolic rate, and body shape) and used a reduced representation approach for genome-wide genotyping. Our results show patterns of population divergence in physiological capabilities that are consistent with local adaptation. Selection scans between BW-native and FW-native populations identified genomic regions that presumably aect fitness between BW and FW environments, while GWAS revealed loci that contribute to variation for each physiological trait. There was substantial overlap in the genomic regions putatively under selection and loci associated with the measured physiological traits, suggesting that these phenotypes are important for adaptive divergence between BW and FW environments. Our analysis also implicates candidate genes likely involved in physiological capabilities, some of which validate a priori hypotheses. Together, these data provide insight into the mechanisms that enable diversification of fishes across osmotic boundaries.\n\nAuthor SummaryIdentifying the genes that underlie adaptation is important for understanding the evolutionary process, but this is technically challenging. We bring multiple lines of evidence to bear for identifying genes that underlie adaptive divergence. Specifically, we integrate genotype-phenotype association mapping with genome-wide scans for signatures of natural selection to reveal genes that underlie phenotypic variation and that are adaptive in populations of killifish that are diverging between marine and freshwater environments. Because adaptation is likely manifest in multiple physiological traits, we focus on hypoxia tolerance, salinity tolerance, and metabolic rate; traits that are divergent between marine and freshwater populations. We show that each of these phenotypes is evolving by natural selection between environments; genetic variants that contribute to variation in these physiological traits tend to be evolving by natural selection between marine and freshwater populations. Furthermore, one of our top candidate genes provides a mechanistic explanation for previous hypotheses that suggest the adaptive importance of cellular tight junctions. Together, these data demonstrate a powerful approach to identify genes involved in adaptation and help to reveal the mechanisms enabling transitions of fishes across osmotic boundaries.

evolutionary biology↗