Biology subjects

Bolnick, D.

Publications and source records attributed to Bolnick, D..

10 recordsLinked to original sources

bioRxiv2026

Among-population variation in the threespine stickleback ( Gasterosteus aculeatus ) liver metabolome: effects of ancestry and environment

Untargeted metabolomics offers a powerful lens for quantifying high-dimensional phenotypic variation within and among species in nature, but has yet to be widely adopted in evolutionary ecology. Some important initial questions are whether metabolome composition differs among populations, and to what extent such variation is genetic or plastic. Here, we use untargeted liquid chromatography tandem mass spectrometry to characterize the relative abundance of 5,939 molecular features of the threespine stickleback (Gasterosteus aculeatus) liver metabolome. Native lake populations differ in metabolome composition, reflecting effects of sex, size, geography, and population ecotype (benthic versus limnetic). Stickleback from these lakes were translocated to found new populations in nine recently fishless lakes, permuting fish ecotypes across benthic and limnetic lake habitats. Several generations later, metabolomes in these experimental populations reflect effects both of their genetic ancestry (e.g., taurocholic acid, a cholane steroid bile acid, was elevated in limnetic-ancestries), as well as their present habitat (e.g., acylcarnitines). Additionally, ecotypes transplanted into a habitat to which they were maladapted exhibited a distinctive metabolomic profile. We conclude that stickleback exhibit both heritable and plastic among-population differences in liver metabolome, which could represent an important phenotypic basis of rapid evolution, population divergence, and perhaps local adaptation.

Molecular Biology↗

bioRxiv2026

An intestinal cell atlas and organoid model for the threespine stickleback

The intestine plays a crucial role in physiology, nutrition, and immune function, but intestinal anatomy and cell types have yet to be fully characterized in many fish species, the most diverse group of vertebrates. To address this gap, we characterized the structure and composition of the intestine of threespine stickleback (Gasterosteus aculeatus), an emerging model teleost in biological research. Using histology, myeloperoxidase staining, single-cell RNA sequencing, and RNA in situ hybridization, we defined major intestinal epithelial, immune, stromal, and stem/progenitor populations. Goblet cells were abundant in proximal and hindgut, while myeloperoxidase-positive granulocytes were evenly distributed throughout the intestine. To facilitate future experimental studies of stickleback intestinal function, we also developed the first intestinal organoid culture from stickleback and show that these cultures recapitulate epithelial architecture and retain expression of canonical intestinal epithelial markers. This organoid platform enables future functional studies of mucosal immunity, host-microbe interactions, and intestinal physiology in stickleback and related teleosts. Together, our integrated approach provides a comprehensive cell atlas and a novel experimental model for studying digestive and immune functions in threespine stickleback.

Cell Biology↗

bioRxiv2024

Among-Population Differentiation in the Tapeworm Proteome through Prediction of Excretory/Secretory and Transmembrane Proteins in Schistocephalus solidus

BackgroundParasites secrete and excrete a variety of molecules evolve to help establish and sustain infections within hosts. Parasite adaptation to their host may lead to between-population divergence in these excretory and secretory products (ESPs), but few studies have tested for intraspecific variation in helminth proteomes. MethodsSchistocephalus solidus is a cestode that parasitizes three spined stickleback, Gasterosteus aculeatus. We used an ultra-performance liquid chromatography-mass spectrometry protocol to characterize the ESP and whole-body proteome of S. solidus. Specifically, we characterized the proteome of S. solidus at the plerocercoid stage from wild caught stickleback from three lakes on Vancouver Island (British Columbia, Canada) and one lake in Alaska (United States). We tested for differences in proteome composition among the four populations and specifically between ESPs and body tissue. ResultsOverall, we identified 1362 proteins in the total proteome of S. solidus, with 542 of the 1362 proteins detected exclusively in the ESPs. Of the ESP proteins, we found signaling peptides and transmembrane proteins that were previously not detected or characterized in S. solidus. We also found protein spectrum counts greatly varied between all lake populations. ConclusionsThese population-level differences were observed in both ESP and tissue types. Our study suggests that S. solidus can excrete and secrete a wide range of proteins which are distinct among populations. These differences might reflect plastic responses to host genotype differences, or evolved adaptations by Schistocephalus to different local host populations.

evolutionary biology↗

bioRxiv2019

Scale-dependent effects of geography, host ecology, and host genetics on diversity of a stickleback parasite metacommunity

Many metacommunities are distributed across habitat patches that are themselves aggregated into groups. Perhaps the clearest example of this nested metacommunity structure comes from multi-species parasite assemblages, which occupy individual hosts that are aggregated into host populations. At both spatial scales, we expect parasite community diversity in a given patch (either individual host or population) to depend on patch characteristics that affect colonization rates and species sorting. But, are these patch effects consistent across spatial scales? Or, do different processes govern the distribution of parasite community diversity among individual hosts, versus among host patches? To answer these questions, we document the distribution of parasite richness among host individuals and among populations in a metapopulation of threespine stickleback (Gasterosteus aculeatus). We find some host traits (host size, gape width) are associated with increased parasite richness at both spatial scales. Other patch characteristics affect parasite richness only among individuals (sex), or among populations (lake size, lake area, elevation, and population mean heterozygosity). These results demonstrate that some rules governing parasite richness in this metacommunity are shared across scales, while others are scale-specific.

ecology↗

bioRxiv2019

The Goldilocks effect of lake size on within-population diversity in stickleback

Many generalist species consist of disparate specialized individuals, a phenomenon known as individual specialization. This within-population niche variation can stabilize population dynamics, reduce extinction risk, and alter community composition. But, we still only vaguely understand the ecological contexts that promote niche variation and its stabilizing effects. Adaptive dynamics models predict that intraspecific variation should be greater in environments with two or more equally-profitable resources, but reduced in environments dominated by one resource. Here, we confirm this prediction using a comparison of threespine stickleback in 33 lakes in on Vancouver Island, Canada. Stickleback consume a combination of benthic and limnetic invertebrates, focusing on the former in small lakes, the latter in large lakes. Intermediate-sized lakes support generalist populations, which arise via greater among-individual diet variation, not by greater individual diet breadth. These intermediate lakes exhibit correspondingly greater morphological diversity, while genomic diversity increases linearly with lake size. These results support the theoretical expectation that habitats with an intermediate ratio of resources are \"just right\" for promoting ecologically relevant intraspecific diversification.

ecology↗

bioRxiv2019

Host sex and genotype modify the gut microbiome response to helminth infection

The microbial community can be altered by direct/indirect interactions with parasites infecting host. Direct interactions can arise from physical/chemical contact with the parasite. Indirect interactions can involve parasite-induced changes in host immunity. If so, this would represent a case of genetic polymorphism in one species controlling an ecological interaction between other species. Here, we report a test of this expectation: we experimentally exposed Gasterosteus aculeatus to their naturally co-evolved parasite, Schistocephalus solidus. The host microbiome differed in response to parasite exposure, and between infected and uninfected fish. The microbial response to infection differed between host sexes, and also varied between variants at autosomal quantitative trait loci (QTL). These results indicate that host genotype regulates the indirect effect of infection on a vertebrate gut microbiome. Our results also raise the possibility that this sex-bias may be related to sex-specific microbial responses to the presence (or, absence) of helminthes. Therefore, helminth-based therapeutics as possible treatments for inflammatory bowel diseases might need to take account of these interactions, potentially requiring therapies tailored to host sex or genotype.

microbiology↗

bioRxiv2017

Adaptive plasticity generates microclines in threespine stickleback male nuptial color

Adaptive phenotypic divergence is typically studied across relatively broad spatial scales (continents, archipelagos, river basins) because at these scales we expect environmental differences to be strong, and the homogenizing effect of gene flow to be weak. However, phenotypic plasticity and phenotype-dependent habitat choice are additional mechanisms that could also drive adaptation across spatially variable environments. We present evidence for apparently adaptive phenotypic variation across surprisingly small spatial scales (<2 vertical meters) in the threespine stickleback. We find that male breeding coloration varies as a function of the lakes optical-depth gradient, and these small-scale clines ( microclines) appear to be an adaptive response to ambient light gradients, as male color changes predictably in the opposite direction ( countergradient) to ambient light spectral shifts. Using visual models and field enclosure experiments, we show that these microclines result from phenotypic plasticity that maintains male conspicuousness. Our results show that adaptive phenotypic clines can exist across small spatial scales, because phenotypic plasticity rapidly generates repeatable trait-environment correlations despite the overwhelming opportunity for gene flow. Furthermore, these results provide strong evidence that phenotypic plasticity in nuptial coloration is an important mechanism for adjusting the conspicuousness of a visual signal to conspecifics.

evolutionary biology↗

bioRxiv2017

Gene Expression Stasis And Plasticity Following Migration Into A Foreign Environment

Selection against migrants is key to maintaining genetic differences between populations linked by dispersal. Yet, migrants are not just passively weeded out by selection. Migrants may mitigate fitness costs by proactively choosing among available habitats, or by phenotypic plasticity. We previously reported that a reciprocal transplant of lake and stream stickleback (Gasterosteus aculeatus) found little support for divergent selection. We revisit that experiment to test whether phenotypic plasticity in gene expression may have helped migrants adjust to unfamiliar habitats. We measured gene expression profiles in stickleback via TagSeq and tested whether migrants between lake and stream habitats exhibited a plastic response to their new environment that allowed them to converge on the expression profile of adapted natives. We report extensive gene expression differences between genetically divergent lake and stream stickleback, despite gene flow. But for many genes, expression was highly plastic. Fish transplanted into the adjoining habitat partially converged on the expression profile typical of their new habitat. This suggests that expression plasticity may soften the impact of migration. Nonetheless, lake and stream fish differed in survival rates and parasite infection rates in our study, implying that expression plasticity is not fast or extensive enough to fully homogenize fish performance.

evolutionary biology↗

bioRxiv2017

The role of gene expression in the recent evolution of resistance in a model host parasite system

Damage by parasites is a perpetual challenge for hosts, often leading to the evolution of elaborate mechanisms of avoidance, immunity, or tolerance. Host resistance can evolve via changes in immune protein coding and/or expression. Heritable population differences in gene expression following infection can reveal mechanisms of immune evolution. We compared gene expression in infected and uninfected threespine stickleback (Gasterosteus aculeatus) from two natural populations that differ in their resistance to a native cestode parasite, Schistocephalus solidus. Genes in both the innate and adaptive immune system were differentially expressed as a function of host population, infection status, and their interaction. These genes were enriched for loci controlling immune functions that we independently verified differ between host populations, or in response to infection. For instance, populations differ strongly in reactive oxygen (ROS) production, and we observed corresponding differences in expression of ROS-affecting loci. Differentially expressed genes also were involved in fibroblast activation, B-cell activation, and leukocyte trafficking. Coexpression network analysis identified two distinct immune processes contributing to stickleback resistance; several modules of genes are correlated with parasite survival while a different set of modules are correlated with suppression of cestode growth. Comparison of networks between populations showed resistant fish have a dynamic expression profile while susceptible fish are static. In summary, recent evolutionary divergence between two vertebrate populations has generated population-specific gene expression responses to parasite infection, which reveal a few immune modules likely to separately affect cestode establishment, and growth.

evolutionary biology↗

bioRxiv2016

NATURAL SELECTION ON MHC IIB IN PARAPATRIC LAKE AND STREAM STICKLEBACK: BALANCING, DIVERGENT, BOTH, OR NEITHER?

Major histocompatibility (MHC) genes encode proteins that play a central role in vertebrates adaptive immunity to parasites. MHC loci are among the most polymorphic in vertebrates genomes, inspiring many studies to identify evolutionary processes driving MHC polymorphism within populations, and divergence between populations. Leading hypotheses include balancing selection favoring rare alleles within populations, and spatially divergent selection. These hypotheses do not always produce diagnosably distinct predictions, causing many studies of MHC to yield inconsistent or ambiguous results. We suggest a novel strategy to distinguish balancing versus divergent selection on MHC, taking advantage of natural admixture between parapatric populations. With divergent selection, immigrant alleles will be more infected and less fit because they are susceptible to novel parasites in their new habitat. With balancing selection, locally-rare immigrant alleles will be more fit (less infected). We tested these contrasting predictions using threespine stickleback from three replicate pairs of parapatric lake and stream habitats. We found numerous positive and negative associations between particular MHC II{beta} alleles and particular parasite taxa. A few allele-parasite comparisons supported balancing selection, others supported divergent selection between habitats. But, there was no overall tendency for fish with immigrant MHC alleles to be more or less heavily infected. Instead, locally rare MHC alleles (not necessarily immigrants) were associated with heavier infections. Our results illustrate the complex relationship between MHC II{beta} allelic variation and spatially varying multi-species parasite communities: different hypotheses may be concurrently true for different allele-parasite combinations.

evolutionary biology↗