Biology subjects

Fuess, L. E.

Publications and source records attributed to Fuess, L. E..

14 recordsLinked to original sources

bioRxiv2025

Environmental conditions modulate constitutive and induced host immunity contributing to spatial patterns of coral disease susceptibility

Disease outbreaks have caused mass mortality and threaten the persistence of numerous vulnerable species, including reef-building corals. Spatiotemporal variations in disease prevalence suggest environmental conditions exacerbate disease susceptibility, potentially by compromising host immunity. Understanding how these variations influence disease dynamics and immunity may enable improved prediction of future disease outbreaks. We combined field observations and statistical modeling to identify the environmental drivers of stony coral tissue loss disease (SCTLD) in Florida. We then performed environmental manipulation experiments to confirm the effects of identified factors on immunity in the massive coral Montastraea cavernosa. SCTLD susceptibility was influenced most by the interaction between temperature and chlorophyll-a concentration (nutrients proxy) the month prior to disease survey, as well as the interaction between chlorophyll-a and three-month mean PAR. SCTLD prevalence was highest when temperatures were low (<30 {degrees}C) and chlorophyll-a concentration exceeded [~]6 mg m-3 and/or when PAR and chlorophyll-a concentrations were high. SCTLD severity had a negative relationship with temperature, a colony had a higher probability of dying during the SCTLD outbreak when temperatures stayed below 31.08 {degrees}C, a finding in contrast to previous coral disease studies. In the laboratory, coral fragments were exposed to temperature and nutrient manipulation, then immune challenged. Heat stress largely drove suppression of baseline immunity but increased production of some antioxidants, suggesting host stress. Fragments exposed to moderate ammonium concentration induced the strongest immune responses compared to those grown under high or no ammonium conditions. Combined with modeling results, these findings support long-standing hypotheses that coral disease susceptibility is at least, in part, modulated by environmentally induced changes in immunity. Overall, our results enhance the understanding of the impact of environmental conditions on SCTLD outbreaks and on general coral immunity. They also highlight the possibility of increased disease severity as anthropogenic pressure on marine environments increases.

ecology↗

bioRxiv2025

Changes in gene regulation are associated with the evolution of resistance to a novel parasite

Host-parasite interactions are ubiquitous and are important drivers of diversification and evolution. Host immune systems in particular are frequent targets of parasite-driven selection. The resulting rapid evolution of immune genes is usually framed as an ongoing arms race between a co-evolving pair of host and parasite species. But, often immune evolution may be driven by the acquisition of a new and unfamiliar parasite. For instance, when marine populations of threespine stickleback (Gasterosteus aculeatus) colonized freshwater lakes [~]12,000 years ago, they encountered and evolved resistance to a freshwater-restricted cestode Schistocephalus solidus. We compared the transcriptomic responses of lab-reared stickleback from three populations with varying cestode susceptibility (naive marine, susceptible lake, and resistant lake), when exposed to several immune stimuli. The resulting changes in expression reveal strong evidence for shared and population-specific responses during evolution of defense against a new parasite. Our investigation highlights the roles of several key immunological processes in underlying a general physiological response to tissue damage (fibrosis), and the importance of regulation of this fibrosis as a necessary step for its co-option into parasite defense. Furthermore, we highlight changes in expression of fibrosis-associated genes which facilitate faster and more targeted deployment of this defense against parasites; fish from resistant populations have higher and more consistent expression of fibrosis genes, which experience strong negative feedback in response to cestode stimuli only. Combined, our results provide strong evidence that changes in gene regulation and increased negative feedback to mitigate immunopathology are essential steps in the evolution of novel parasite defense.

immunology↗

bioRxiv2025

Differential regulation of apoptosis, autophagy and Symbiodiniaceae energy transfer mediate the link between bleaching and disease in Exaiptasia diaphana

Anthropogenic climate change has caused unprecedented declines across a number of marine taxa. Coral reef ecosystems, which are formed by scleractinian corals, face widespread declines in ecosystem health and function due to co-occurring environmental stressors. Frequent exposure of corals to a variety of biotic and abiotic stressors makes these cnidarians a prime candidate for investigating the effects of multiple stressors on marine ecosystems. In recent decades, hyperthermic bleaching events and disease outbreaks have been prominent stressors on reefs. Disease outbreaks often follow hyperthermic bleaching events, yet the mechanisms driving the diffuse associations between bleaching and disease are poorly understood. Here we investigated the mechanisms linking sequential bleaching and disease using the model cnidarian Exaiptasia diaphana. We examined the transcriptomic responses of anemones to immune challenge during acute recovery from prior heat stress. We observed notable upregulation of apoptotic pathways and downregulation of autophagic pathways in previously heat-stressed anemones, while anemones maintained at ambient temperatures displayed an inverse pattern characterized by downregulation of apoptosis. Furthermore, network analyses suggest that disruption of host-Symbiodiniaceae nutrient exchange during bleaching recovery of previously heat-stressed anemones may contribute to observed immune suppression following heat stress. These results provide insight regarding the cellular mechanisms facilitating increased disease susceptibility during recovery from heat stress, highlighting the roles of immunological regulation and nutrient availability in these processes.

ecology↗

bioRxiv2024

Macroevolutionary changes in gene expression response to an immune stimulus across the diversity of fishes

Our understanding of the vertebrate immune system is dominated by a few model organisms such as mice. This use of a few model systems is reasonable if major features of the immune systems evolve slowly and are conserved across most vertebrates, but may be problematic if there is substantial macroevolutionary change in immune responses. Here, we present a test of the macroevolutionary stability, across 15 species of jawed fishes, of the transcriptomic response to a standardized immune challenge. Intraperitoneal injection of an immune adjuvant (alum) induces a fibrosis response in nearly all jawed fishes, which in some species contributes to anti-helminth resistance. Despite this conserved phenotypic response, the underlying transcriptomic response is highly inconsistent across species. Although many gene orthogroups exhibit differential expression between saline versus alum-injected fish in at least one species, few orthogroups exhibit consistent differential expression across species. This result suggests that although the phenotypic response to alum (fibrosis) is highly conserved, the underlying gene regulatory architecture is very flexible and cannot readily be extrapolated from any one species to fishes (or vertebrates) more broadly. The vertebrate immune response is remarkably changeable over macroevolutionary time, requiring a diversity of model organisms to describe effectively.

evolutionary biology↗

bioRxiv2024

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↗

bioRxiv2024

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↗

bioRxiv2024

Photosymbiont density is correlated with constitutive and induced immunity in the facultatively symbiotic coral, Astrangia poculata

Scleractinian corals, essential ecosystem engineers that form the base of coral reef ecosystems, have faced unprecedented mortality in recent decades due climate-change related stressors, including disease outbreaks. Despite this emergent threat to corals, many questions still remain regarding mechanisms underlying observed variation in disease susceptibility. Emergent data suggests at least some degree of variation in disease response may be linked to variability in the relationship between host corals and their algal photosymbionts (Family Symbiodineaceae). Still, the nuances of connections between symbiosis and immunity in cnidarians, including scleractinian corals, remain poorly understood. Here we leveraged an emergent model species, the facultatively symbiotic, temperate, scleractinian coral Astrangia poculata, to investigate associations between symbiont density and both constitutive and induced immunity. We used a combination of controlled immune challenges with heat-inactivated pathogens and transcriptomic analyses. Our results demonstrate that A. poculata mounts a robust initial response to pathogenic stimuli that is highly similar to responses documented in tropical corals. Furthermore, we document positive associations between symbiont density and both constitutive and induced immune responses, in agreement with recent preliminary studies in A. poculata. A suite of immune genes, including those coding for antioxidant peroxidoxin biosynthesis, are constitutively positively associated with symbiont density in A. poculata. Furthermore, variation in symbiont density is associated with distinct patterns of immune response; low symbiont density corals induce preventative immune mechanisms whereas high symbiont density corals mobilize energetic resources to fuel humoral immune responses. In summary, our study reveals the need for more nuanced study of symbiosis-immune interplay across diverse scleractinian corals, preferably including quantitative energy budget analysis for full disentanglement of these complex associations and their effects on pathogen susceptibility.

immunology↗

bioRxiv2023

Prior heat stress increases pathogen susceptibility in the model cnidarian Exaptasia diaphana

Anthropogenic climate change has significantly altered terrestrial and marine ecosystems globally, often in the form of climate-related events such as thermal anomalies and disease outbreaks. Although the isolated effects of these stressors have been well documented, a growing body of literature suggests that stressors often interact, resulting in complex effects on ecosystems, including coral reefs where sequential associations between heat stress and disease have had profound impacts. Here we used the model cnidarian Exaiptasia diaphana to investigate mechanisms linking prior heat stress to increased disease susceptibility. We examined anemone pathogen susceptibility and physiology (symbiosis, immunity, and energetics) following recovery from heat stress. We observed significantly increased pathogen susceptibility in anemones previously exposed to heat stress. Notably, prior heat stress reduced anemone energetic reserves (carbohydrate concentration), and activity of multiple immune components. Minimal effects of prior heat stress on symbiont density were observed. Together, results suggest changes in energetic availability might have the strongest effect on pathogen susceptibility and immunity following heat stress. The results presented here provide critical insight regarding the interplay between heat stress recovery and pathogen susceptibility in cnidarians and are an important first step towards understanding temporal associations between these stressors.

ecology↗

bioRxiv2023

Characterization of trade-offs between immunity and reproduction in Astrangia poculata

BackgroundLiving organisms face ubiquitous pathogenic threats and have consequently evolved immune systems to protect against potential invaders. However, many components of the immune system are physiologically costly to maintain and engage, often drawing resources away from other organismal processes such as growth and reproduction. Evidence from a diversity of systems has demonstrated that organisms use complex resource allocation mechanisms to manage competing needs and optimize fitness. However, understanding of resource allocation patterns is limited across taxa. Cnidarians, which include ecologically important organisms like hard corals, have been historically understudied in the context of resource allocations. Improving understanding of resource allocation-associated tradeoffs in cnidarians is critical for understanding future ecological dynamics in the face of rapid environmental change. MethodsHere, we characterize trade-offs between constitutive immunity and reproduction in the facultatively symbiotic coral Astrangia poculata. Male colonies underwent ex situ spawning and sperm output was quantified. We then examined the effects of variable symbiont density and energetic budget on physiological traits, including immune activity and reproductive investment. Furthermore, we tested for potential trade-offs between immune activity and reproductive investment. ResultsWe found limited effects of energetic budget on immune metrics; melanin production was significantly positively associated with energetic budget. However, we failed to document any associations between immunity and reproductive output which would be indicative of trade-offs, possibly due to experimental limitations. Our results provide a preliminary framework for future studies investigating immune trade-offs in cnidarians.

immunology↗

bioRxiv2022

Variation in symbiont density is linked to changes in constitutive immunity in the facultatively symbiotic coral, Astrangia poculata

Scleractinian corals are essential ecosystem engineers, forming the basis of coral reef ecosystems. However, these organisms are in decline globally, in part due to rising disease prevalence. Most corals are dependent on symbiotic interactions with single-celled algae from the family Symbiodiniaceae to meet their nutritional needs, however suppression of host immunity may be essential to this relationship. To explore immunological consequences of algal symbioses in scleractinian corals, we investigated constitutive immune activity in the facultatively symbiotic coral, Astrangia poculata. We compared immune metrics (melanin synthesis, antioxidant production, and antibacterial activity) between coral colonies of varying symbiont density. Symbiont density was positively correlated to both antioxidant activity and melanin concentration. Our results suggest that the relationship between algal symbiosis and host immunity may be more complex than originally hypothesized and highlight the need for nuanced approaches when considering these relationships.

ecology↗

bioRxiv2021

Single-cell RNA sequencing reveals micro-evolution of the stickleback immune system

Pathogenic infection is an important driver of many ecological processes. Furthermore, variability in immune function is an important driver of differential infection outcomes. New evidence would suggest that immune variation extends to broad cellular structure of immune systems. However, variability at such broad levels is traditionally difficult to detect in non-model systems. Here we leverage single cell transcriptomic approaches to document signatures of microevolution of immune system structure in a natural system, the three-spined stickleback (Gasterosteus aculeatus). We sampled nine adult fish from three populations with variability in resistance to a cestode parasite, Schistocephalus solidus, to create the first comprehensive immune cell atlas for G. aculeatus. Eight major immune cell types, corresponding to major vertebrate immune cells, were identified. We were also able to document significant variation in both abundance and expression profiles of the individual immune cell types, among the three populations of fish. This variability may contribute to observed variability in parasite susceptibility. Finally, we demonstrate that identified cell type markers can be used to reinterpret traditional transcriptomic data. Combined our study demonstrates the power of single cell sequencing to not only document evolutionary phenomena (i.e. microevolution of immune cells), but also increase the power of traditional transcriptomic datasets.

immunology↗

bioRxiv2020

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↗

bioRxiv2020

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↗

bioRxiv2020

Rapid Evolution of Parasite Resistance via Improved Recognition and Accelerated Immune Activation and Deactivation

Closely related populations often differ in resistance to a given parasite, as measured by infection success or failure. Yet, the immunological mechanisms of these evolved differences are rarely specified. Does resistance evolve via changes to the hosts ability to recognize that an infection exists, actuate an effective immune response, or attenuate that response? We tested whether each of these phases of the host response contributed to threespine sticklebacks recently evolved resistance to their tapeworm Schistocephalus solidus. While marine stickleback and some susceptible lake fish permit fast-growing tapeworms, other lake populations are resistant and suppress tapeworm growth via a fibrosis response. We subjected lab-raised fish from three populations (susceptible marine ancestors, a susceptible lake, a resistant lake), to a novel immune challenge (injection of: 1) a saline control, 2) alum, a generalized pro-inflammatory adjuvant that causes fibrosis, 3) a tapeworm protein extract, and 4) a combination of alum and tapeworm protein). All three populations were capable of a robust fibrosis response to the alum treatments (but not the saline control). Yet, only the resistant population exhibited a fibrosis response to the tapeworm protein alone. Thus, these populations differed in their ability to recognize the tapeworm but shared an intact fibrosis pathway. However, the resistant population also initiated fibrosis faster, and was able to attenuate fibrosis, unlike the susceptible populations slow but longer-lasting response to alum. As fibrosis has presumed pathological side-effects, this difference may reflect adaptions to mitigate costs of immunity in the resistant population. Broadly, our results confirm that parasite detection, activation speed, and immune attenuation simultaneously contribute to adaptations to parasite infection in natural populations. IMPACT SUMMARYDramatic variation in parasite resistance is common in nature, even to the same parasite, yet we are still working to understand the mechanisms of how such differences evolve. Many evolution studies focus on the broad outcomes of infection (infected or not) when studying this question, without specifying what part of the immune response has evolved. Here, we experimentally partition different sequential stages in the host immune response (recognition, actuation, attenuation), to evaluate which stage(s) underly the evolution of host resistance to infection. This study compares three populations of threespine stickleback that naturally differ in their exposure and their ability to resist infections of a freshwater tapeworm. These include a "resistant" lake population, a "susceptible" lake population, and an ancestral marine population that is rarely exposed to the tapeworm in nature, but is susceptible when exposed in the lab. The resistant population exhibits a fibrosis immune response to infection, which has previously been linked to suppressed tapeworm growth and viability. We injected different immune challenges directly into the site of infection (peritoneal cavity) and measured the subsequent fibrosis response through time. We found that all populations were capable of producing fibrosis in response to a general immune stimulant (alum). But, only the resistant population was able to recognize and respond to tapeworm protein alone. This population also responded faster than the others, within 24 hours, and attenuated its fibrosis by 90 days post-injections whereas the other populations exhibited a slower response that did not attenuate in the study time-frame. We concluded that variation in parasite recognition, an early phase in the host response, shapes the evolution of the initiation and resolution of the physical response to infection. Broadly, our results support that parasite detection mechanisms could play a key role in the rapid evolution of parasite resistance.

evolutionary biology↗