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Steinel, N. C.

Publications and source records attributed to Steinel, N. C..

10 recordsLinked to original sources

Intrinsic fitness differences outweigh environmental matching in shaping introduction outcomes in nature

Species introductions and transplants offer powerful contexts to understand evolutionary patterns and processes, and they are increasingly critical for conservation. However, introduction success varies widely, and predicting outcomes remains challenging. Introducing multiple source populations should increase the chance of success, while also providing an opportunity to explore the factors that predict success of individual source populations in the same environment. We used replicated, mixed-population introductions of >12,000 threespine stickleback (Gasterosteus aculeatus) to test whether source population success could be predicted by environmental matching between source and recipient environments and/or by intrinsic source population characteristics. We introduced four to eight source populations of stickleback into each of nine natural lakes and tracked their relative success over the following two years (up to two generations). Source population success was largely consistent across lakes, despite divergent environmental conditions. These results point to the importance of intrinsic source population characteristics rather than environmental matching in predicting introduction success in natural settings. Source populations that were consistently successful tended to have greater stress tolerance (mortality rate during translocation) and higher genetic diversity, though these relationships were not conclusive. Our study highlights the value of considering factors that generate fitness differences independent of environmental contexts in predicting ecological and evolutionary dynamics and planning conservation programs. Significance StatementPredicting which populations will succeed when introduced to new environments is a central challenge in ecology, evolution, and conservation. Environmental conditions are often assumed to be crucial in determining which populations succeed, given the expectation that populations preadapted to local conditions should perform best. We test this assumption by introducing >12,000 threespine stickleback fish from up to eight source populations into nine natural lakes spanning diverse environmental conditions. We show that the relative success of individual source populations was remarkably consistent across lakes and environmental conditions, indicating that some populations are intrinsically better suited to introductions. Our findings underscore the importance of considering intrinsic population characteristics alongside environmental conditions when predicting ecological and evolutionary outcomes and guiding conservation efforts.

evolutionary biology↗

Lake size shapes the relationship between body mass and gut microbiota in threespine stickleback (Gasterosteus aculeatus)

Host-microbe interactions are shaped by both host and environmental factors. However, little is known about how host-microbe interactions vary across populations within a species. Here, we characterized the gut microbiota of 191 wild threespine stickleback fish (Gasterosteus aculeatus) from six populations from Alaskan lakes spanning a gradient of surface area. We tested how environmental context (lake size and ecotype) and host traits (sex, body mass, gravidity, Schistocephalus solidus (S. solidus) infection, and fibrosis) influence stickleback gut microbial composition using 16S rRNA gene sequencing. We found that the lake surface area strongly predicted fish gut microbial alpha diversity. Fish from intermediate-sized lakes harbored significantly more diverse microbiota than those from small and large lakes, independent of ecotype. Body mass was associated with gut microbial diversity. Model-predicted marginal effects from the mass and lake surface area interaction analysis showed that the association between fish mass and microbial alpha diversity was strongly negative in the smallest lakes, weakest in intermediate-sized lakes, and strongly positive in the largest lakes. In addition, sex and S. solidus infection were significantly associated with gut microbiota alpha and beta diversity, whereas fibrosis and gravidity showed minimal effects. Differential abundance analysis revealed lake size-dependent associations between body mass and individual taxa. Together, these results demonstrate that both habitat context and host variation interactively shape stickleback gut microbial communities in the wild. Integrating lake-level and individual-level analyses reveals how ecological setting modulates host-microbe associations, offering insights into the role of the gut microbiota in host adaptation and population divergence.

microbiology↗

Excretory-secretory products from the parasite Schistocephalus solidus enhance viability and function of threespine stickleback splenocytes

Helminths can modulate the immune systems of their hosts through the release of soluble molecules known as excretory-secretory products (ESPs). To better understand the extent and mechanisms behind helminth-mediated immunosuppression, we used an emerging model of host-parasite interactions, threespine stickleback, Gasterosteus aculeatus, and its tapeworm parasite Schistocephalus solidus. We examined the impacts of exposure to ESPs of S. solidus (SsESPs) originating from four Canadian lakes on the viability and function of threespine stickleback splenocytes. We found that 24 hours of exposure to low concentrations of SsESPs significantly increased overall splenocyte viability with the greatest impact on the lymphocyte population. While SsESP exposure did not alter baseline splenocyte respiratory burst activity, SsESP-treated splenic cultures demonstrated significant increases in ROS production in response to phorbol 12-myristate 13-acetate (PMA) stimulation, suggesting that SsESPs may lower the threshold for activation of the respiratory burst. These results in splenocytes contrast with previous studies demonstrating that SsESPs suppress head kidney leukocytes (HKL) viability and function, suggest that S. solidus-derived excretory secretory products may have cell-or tissue-specific immunomodulatory effects, and highlight the importance of studying host-parasite interactions across diverse immune tissues.

immunology↗

Rates of evolution differ between cell types identified by single-cell RNAseq in threespine stickleback

Rates of evolutionary change vary by gene. While some broad gene categories are highly conserved with little divergence over time, others undergo continuous selection pressure and are highly divergent. Here, we combine single-cell RNA sequencing (scRNAseq) with evolutionary genomics to understand whether certain cell types exhibit faster evolutionary divergence (using their characteristic genes), than other types of cells. Merging scRNAseq with population genomic data, we show that cell types differ in the rate at which their characteristic genes evolve, as measured by allele frequency divergence among many populations (FST) and between species (dN/dS ratios). Neutrophils, B cells, and fibroblasts exhibit elevated FST at characteristic genes, while eosinophils in the intestine and thrombocytes in the head kidney exhibit lower FST than the average for 1000 random genes. Gene network centrality also differed between immune- and non-immune-associated genes, and closeness centrality was positively related to gene FST. These results highlight the value of merging single cell RNA sequencing technology with evolutionary population genomic data, and reveal that genes which define immune cell types exhibit especially rapid evolution.

evolutionary biology↗

A spectral framework to map QTLs affecting joint differential networks of gene co-expression

Studying the mechanisms underlying the genotype-phenotype association is crucial in genetics. Gene expression studies have deepened our understanding of the genotype [->] expression [->] phenotype mechanisms. However, traditional expression quantitative trait loci (eQTL) methods often overlook the critical role of gene co-expression networks in translating genotype into phenotype. This gap highlights the need for more powerful statistical methods to analyze genotype [->] network [->] phenotype mechanism. Here, we develop a network-based method, called snQTL, to map quantitative trait loci affecting gene co-expression networks. Our approach tests the association between genotypes and joint differential networks of gene co-expression via a tensor-based spectral statistics, thereby overcoming the ubiquitous multiple testing challenges in existing methods. We demonstrate the effectiveness of snQTL in the analysis of three-spined stickleback (Gasterosteus aculeatus) data. Compared to conventional methods, our method snQTL uncovers chromosomal regions affecting gene co-expression networks, including one strong candidate gene that would have been missed by traditional eQTL analyses. Our framework suggests the limitation of current approaches and offers a powerful network-based tool for functional loci discoveries. Significance statementThis work addresses a key gap in understanding the mechanistic foundations for genotype-phenotype associations. While existing expression quantitative trait loci (eQTL) methods identify candidate loci affecting gene expression variants, they often neglect the crucial role of gene co-expression networks. Here, we develop a network-based QTL framework to map genetic loci affecting the gene co-expression network. Utilizing a tensor-based spectral approach, our snQTL method estimates the differential co-expression patterns and effectively identifies the associated genetic loci. Application of snQTL to three-spined sticklebacks revealed candidate loci missed by standard methods. This work suggests the limitations of current approaches and highlights the potential of network-based functional loci discovery.

genetics↗

Exploring Gene Expression Patterns and Evolutionary Responses in Host-Parasite inteactions: Insights from the Schistocephalus solidus - Threespine stickleback System

Helminth parasites pose a significant threat to host survival and reproductive success, imposing strong selection pressure on hosts to evolve countermessures (e.g., immune responses and behavioral changes). To gain insights into the underlying mechanisms of host-parasite co-evolution, we examined differences in gene expression in immune tissues of two Alaskan stickleback (Gasterosteus aculeatus) populations with varying susceptibility to infection by the cestode Schistocephalus solidus. Our analyses revealed distinct patterns of immune gene expression at the population-level in response to infection. Infected fish from the high infection population displayed signs of immune manipulation by the parasite, whereas this phenomenon was absent in fish from the low infection population. Notably, we found significant differences in immune gene expression between the populations, with uninfected Rocky Lake fish showing up-regulation of innate immune genes associated with inflammation compared to uninfected Walby Lake fish. These findings highlight the divergent evolutionary paths taken by different stickleback populations in their response to the same parasite.

immunology↗

Evolution of a costly immunity to cestode parasites is a pyrrhic victory

Parasites impose fitness costs on their hosts. Biologists therefore tend to assume that natural selection favors infection-resistant hosts. Yet, when the immune response itself is costly, theory suggests selection may instead favor loss of resistance. Immune costs are rarely documented in nature, and there are few examples of adaptive loss of resistance. Here, we show that when marine threespine stickleback colonized freshwater lakes they gained resistance to the freshwater-associated tapeworm, Schistocephalus solidus. Extensive peritoneal fibrosis and inflammation contribute to suppression of cestode growth and viability, but also impose a substantial cost of reduced fecundity. Combining genetic mapping and population genomics, we find that the immune differences between tolerant and resistant populations arise from opposing selection in both populations acting, respectively, to reduce and increase resistance consistent with divergent optimization. One Sentence SummaryRecently-evolved freshwater populations of stickleback frequently evolve increased resistance to tapeworms, involving extensive fibrosis that suppresses parasite growth; because this fibrosis greatly reduces fish fecundity, in some freshwater populations selection has favored an infection-tolerant strategy with fibrosis suppression.

evolutionary biology↗

Immune gene expression covaries with gut microbiome composition in stickleback

Commensal microbial communities have immense effects on their vertebrate hosts, contributing to a number of physiological functions as well as host fitness. In particular, host immunity is strongly linked to microbiota composition through poorly understood bi-directional links. Gene expression may be a potential mediator of these links between microbial communities and host function. However few studies have investigated connections between microbiota composition and expression of host immune genes in complex systems. Here we leverage a large study of laboratory-raised fish from the species Gasterosteus aculeatus (three-spined stickleback) to document correlations between gene expression and microbiome composition. First, we examined correlations between microbiome alpha diversity and gene expression. Our results demonstrate robust positive associations between microbial alpha diversity and expression of host immunity. Next, we examined correlations between host gene expression and abundance of microbial taxa. We identified 15 microbial families that were highly correlated to host gene expression. These families were all tightly correlated to host expression of immune genes and processes, falling into one of three categories: those positively correlated, negatively correlated, and neutrally related to immune processes. Furthermore, we highlight several important immune processes that are commonly associated with abundance of these taxons, including both macrophage and B cell functions. Further functional characterization of microbial taxa will help disentangle the mechanisms of the correlations described here. In sum, our study supports prevailing hypotheses of intimate links between host immunity and gut microbiome composition.

immunology↗

A test of the Baldwin Effect: Differences in both constitutive expression and inducible responses to parasites underlie variation in host response to a parasite

Despite the significant effect of host-parasite interactions on both ecological systems and organism health, there is still limited understanding of the mechanisms driving evolution of host resistance to parasites. One model of rapid evolution, the Baldwin Effect, describes the role of plasticity in adaptation to novel conditions, and subsequent canalization of associated traits. While mostly applied in the context of environmental conditions, this theory may be relevant to the evolution of host resistance to novel parasites. Here we test the applicability of the Baldwin Effect to the evolution of resistance in a natural system using threespine stickleback fish (Gasterosteus aculeatus) and their cestode parasite Schistochephalus solidus. We leverage a large transcriptomic data set to describe the response to S. solidus infection by three different genetic crosses of stickleback, from a resistant and a tolerant population. Hosts mount a multigenic response to the parasite that is similar among host genotypes. In addition, we document extensive constitutive variation in gene expression among host genotypes. However, although many genes are both infection-induced and differentially expressed between genotypes, this overlap is not more extensive than expected by chance. We also see little evidence of canalization of infection-induced gene expression in the derived resistant population. These patterns do not support the Baldwin Effect, though they illustrate the importance of variation in both constitutive expression and induced responses to parasites. Finally, our results improve understanding of the cellular mechanisms underlying a putative resistance phenotype (fibrosis). Combined, our results highlight the importance of both constitutive and inducible variation in the evolution of resistance to parasites, and identify new target genes contributing to fibrosis. These findings advance understanding of host-parasite interactions and co-evolutionary relationships in natural systems.

immunology↗

Recent evolution of cestode growth suppression by threespine stickleback

Parasites can be a major cause of natural selection on hosts, which consequently evolve a variety of strategies to avoid, eliminate, or tolerate infection. When ecologically similar host populations present disparate infection loads, this natural variation can reveal immunological strategies underlying adaptation to infection and population divergence. For instance, the tapeworm Schistocephalus solidus persistently infects between 0% to 80% of threespine stickleback (Gasterosteus aculeatus) in lakes on Vancouver Island. To test whether these heterogeneous infection rates are due to evolved differences in immunity, we experimentally exposed lab-reared fish from high-and low-infection populations, which are not known to differ in natural exposure risk, to controlled doses of Schistocephalus. We observed heritable between-population differences in several immune traits: fish from the naturally uninfected population initiated a stronger granulocyte response to Schistocephalus infection, and their granulocytes constitutively generated threefold more reactive oxygen species (ROS). Despite these immunological differences, Schistocephalus was equally successful at establishing initial infections in both host populations. However, the low-infection fish dramatically suppressed tapeworm growth relative to high-infection fish, and parasite size was intermediate in F1 hybrid hosts. Our results show that stickleback recently evolved heritable variation in their capacity to suppress helminth growth. Comparative data from many from natural populations indicate that growth suppression is widespread but not universal and, when present, is associated with reduced infection prevalence. Host suppression of helminth somatic growth may be an important immune strategy that aids in parasite clearance, or in mitigating the fitness costs of persistent infection.\n\nSignificanceLarge parasites remain a persistent source of morbidity and mortality in humans, domesticated animals, and wildlife. Hosts are subject to strong natural selection to eliminate or tolerate these parasite infections. Here, we document the recent evolution of a striking form of resistance by a vertebrate host (threespine stickleback) against its cestode parasite (Schistocephalus solidus). After Pleistocene glacial retreat, marine stickleback colonized freshwater lakes, encountered Schistocephalus, and evolved varying levels of resistance to it. We show that a heavily-and a rarely-infected population of stickleback have similar resistance to Schistocephalus colonization, but rarely-infected fish suppress parasite growth by orders of magnitude. These populations represent ends of a natural continuum of cestode growth suppression, which is associated with reduced infection prevalence.

evolutionary biology↗