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1.
Anim Microbiome ; 6(1): 38, 2024 Jul 01.
Article in English | MEDLINE | ID: mdl-38951941

ABSTRACT

To promote sustainable aquaculture, the formulation of Atlantic salmon (Salmo salar) feeds has changed in recent decades, focusing on replacing standard marine-based ingredients with plant-based alternatives, increasingly demonstrating successful outcomes in terms of fish performance. However, little is known about how these plant-based diets may impact the gut microbiota at first feeding and onwards. Nutritional programming (NP) is one strategy applied for exposing fish to a plant-based (V) diet at an early stage in life to promote full utilisation of plant-based ingredients and prevent potential adverse impacts of exposure to a plant-rich diet later in life. We investigated the impact of NP on gut microbiota by introducing fish to plant ingredients (V fish) during first feeding for a brief period of two weeks (stimulus phase) and compared those to fish fed a marine-based diet (M fish). Results demonstrated that V fish not only maintained growth performance at 16 (intermediate phase) and 22 (challenge phase) weeks post first feeding (wpff) when compared to M fish but also modulated gut microbiota. PERMANOVA general effects revealed gut microbiota dissimilarity by fish group (V vs. M fish) and phases (stimulus vs. intermediate vs. challenge). However, no interaction effect of both groups and phases was demonstrated, suggesting a sustained impact of V diet (nutritional history) on fish across time points/phases. Moreover, the V diet exerted a significant cumulative modulatory effect on the Atlantic salmon gut microbiota at 16 wpff that was not demonstrated at two wpff, although both fish groups were fed the M diet at 16 wpff. The nutritional history/dietary regime is the main NP influencing factor, whereas environmental and host factors significantly impacted microbiota composition in M fish. Microbial metabolic reactions of amino acid metabolism were higher in M fish when compared to V fish at two wpff suggesting microbiota played a role in digesting the essential amino acids of M feed. The excessive mucin O-degradation revealed in V fish at two wpff was mitigated in later life stages after NP, suggesting physiological adaptability and tolerance to V diet. Future studies are required to explore more fully how the microbiota functionally contributes to the NP.

2.
Ecol Evol ; 14(6): e11503, 2024 Jun.
Article in English | MEDLINE | ID: mdl-38932947

ABSTRACT

Eco-evolutionary experiments are typically conducted in semi-unnatural controlled settings, such as mesocosms; yet inferences about how evolution and ecology interact in the real world would surely benefit from experiments in natural uncontrolled settings. Opportunities for such experiments are rare but do arise in the context of restoration ecology-where different "types" of a given species can be introduced into different "replicate" locations. Designing such experiments requires wrestling with consequential questions. (Q1) Which specific "types" of a focal species should be introduced to the restoration location? (Q2) How many sources of each type should be used-and should they be mixed together? (Q3) Which specific source populations should be used? (Q4) Which type(s) or population(s) should be introduced into which restoration sites? We recently grappled with these questions when designing an eco-evolutionary experiment with threespine stickleback (Gasterosteus aculeatus) introduced into nine small lakes and ponds on the Kenai Peninsula in Alaska that required restoration. After considering the options at length, we decided to use benthic versus limnetic ecotypes (Q1) to create a mixed group of colonists from four source populations of each ecotype (Q2), where ecotypes were identified based on trophic morphology (Q3), and were then introduced into nine restoration lakes scaled by lake size (Q4). We hope that outlining the alternatives and resulting choices will make the rationales clear for future studies leveraging our experiment, while also proving useful for investigators considering similar experiments in the future.

3.
Am Nat ; 204(1): 15-29, 2024 Jul.
Article in English | MEDLINE | ID: mdl-38857340

ABSTRACT

AbstractAdaptation to replicated environmental conditions can be remarkably predictable, suggesting that parallel evolution may be a common feature of adaptive radiation. An open question, however, is how phenotypic variation itself evolves during repeated adaptation. Here, we use a dataset of morphological measurements from 35 populations of threespine stickleback, consisting of 16 parapatric lake-stream pairs and three marine populations, to understand how phenotypic variation has evolved during transitions from marine to freshwater environments and during subsequent diversification across the lake-stream boundary. We find statistical support for divergent phenotypic covariance (P) across populations, with most diversification of P occurring among freshwater populations. Despite a close correspondence between within-population phenotypic variation and among-population divergence, we find that variation in P is unrelated to total variation in population means across the set of populations. For lake-stream pairs, we find that theoretical predictions for microevolutionary change can explain more than 30% of divergence in P matrices across the habitat boundary. Together, our results indicate that divergence in variance structure occurs primarily in dimensions of trait space with low phenotypic integration, correlated with disparate lake and stream environments. Our findings illustrate how conserved and divergent features of multivariate variation can underlie adaptive radiation.


Subject(s)
Biological Evolution , Lakes , Smegmamorpha , Animals , Smegmamorpha/genetics , Smegmamorpha/physiology , Smegmamorpha/anatomy & histology , Ecosystem , Phenotype , Adaptation, Physiological , Rivers , Adaptation, Biological
4.
Article in English | MEDLINE | ID: mdl-38858075

ABSTRACT

What drives the emergence of new species has fascinated biologists since Darwin. Reproductive barriers to gene flow are a key step in the formation of species, and recent advances have shed new light on how these are established. Genetic, genomic, and comparative techniques, together with improved theoretical frameworks, are increasing our understanding of the underlying mechanisms. They are also helping us forecast speciation and reveal the impact of human activity.

5.
bioRxiv ; 2024 Mar 30.
Article in English | MEDLINE | ID: mdl-38585912

ABSTRACT

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.

6.
Oecologia ; 204(2): 317-325, 2024 Feb.
Article in English | MEDLINE | ID: mdl-37386196

ABSTRACT

Parasitic infections are a global occurrence and impact the health of many species. Coinfections, where two or more species of parasite are present in a host, are a common phenomenon across species. Coinfecting parasites can interact directly or indirectly via their manipulation of (and susceptibility to) the immune system of their shared host. Helminths, such as the cestode Schistocephalus solidus, are well known to suppress immunity of their host (threespine stickleback, Gasterosteus aculeatus), potentially facilitating other parasite species. Yet, hosts can evolve a more robust immune response (as seen in some stickleback populations), potentially turning facilitation into inhibition. Using wild-caught stickleback from 20 populations with non-zero S. solidus prevalence, we tested an a priori hypothesis that S. solidus infection facilitates infection by other parasites. Consistent with this hypothesis, individuals with S. solidus infections have 18.6% higher richness of other parasites compared to S. solidus-uninfected individuals from the same lakes. This facilitation-like trend is stronger in lakes where S. solidus is particularly successful but is reversed in lakes with sparse and smaller cestodes (indicative of stronger host immunity). These results suggest that a geographic mosaic of host-parasite co-evolution might lead to a mosaic of between-parasite facilitation/inhibition effects.


Subject(s)
Coinfection , Smegmamorpha , Humans , Animals , Coinfection/veterinary , Lakes
7.
Oecologia ; 204(2): 427-437, 2024 Feb.
Article in English | MEDLINE | ID: mdl-37358647

ABSTRACT

Parasite infections are ubiquitous and their effects on hosts could play a role in ecosystem processes. Ecological stoichiometry provides a framework to study linkages between consumers and their resource, such as parasites and their host, and ecosystem process; however, the stoichiometric traits of host-parasite associations are rarely quantified. Specifically, it is unclear whether parasites' elemental ratios closely resemble those of their host or if infection is related to host stoichiometry, especially in vertebrate hosts. To answer such questions, we measured the elemental content (%C, %N, and %P) and molar ratios (C:N, C:P, and N:P) of parasitized and unparasitized Gasterosteus aculeatus (three-spined stickleback) and their cestode parasite, Schistocephalus solidus. Host and parasite elemental content were distinct from each other, and parasites were generally higher in %C and lower in %N and %P. Parasite infections were related to host C:N, with infected hosts being lower in C:N. Parasite elemental content was independent of their host, but parasite body mass and parasite density were important drivers of parasite stoichiometry. Overall, these potential effects of parasite infections on host stoichiometry along with parasites' distinct elemental compositions suggest parasites may further contribute to differences in how individual hosts store and recycle nutrients.


Subject(s)
Parasitic Diseases , Smegmamorpha , Animals , Host-Parasite Interactions , Ecosystem , Nutrients
8.
J Exp Biol ; 226(23)2023 12 01.
Article in English | MEDLINE | ID: mdl-37947155

ABSTRACT

The vertebrate immune system provides an impressively effective defense against parasites and pathogens. However, these benefits must be balanced against a range of costly side-effects including energy loss and risks of auto-immunity. These costs might include biomechanical impairment of movement, but little is known about the intersection between immunity and biomechanics. Here, we show that a fibrosis immune response to Schistocephalus solidus infection in freshwater threespine stickleback (Gasterosteus aculeatus) has collateral effects on their locomotion. Although fibrosis is effective at reducing infection, some populations of stickleback actively suppress this immune response, possibly because the costs of fibrosis outweigh the benefits. We quantified the locomotor effects of the fibrosis immune response in the absence of parasites to investigate whether there are incidental costs of fibrosis that could help explain why some fish forego this effective defense. To do this, we induced fibrosis in stickleback and then tested their C-start escape performance. Additionally, we measured the severity of fibrosis, body stiffness and body curvature during the escape response. We were able to estimate performance costs of fibrosis by including these variables as intermediates in a structural equation model. This model revealed that among control fish without fibrosis, there is a performance cost associated with increased body stiffness. However, fish with fibrosis did not experience this cost but rather displayed increased performance with higher fibrosis severity. This result demonstrates that the adaptive landscape of immune responses can be complex with the potential for wide-reaching and unexpected fitness consequences.


Subject(s)
Cestoda , Cestode Infections , Fish Diseases , Parasites , Smegmamorpha , Animals , Fish Diseases/parasitology , Fishes , Cestoda/physiology , Immunity , Host-Parasite Interactions , Cestode Infections/parasitology
9.
Ecol Lett ; 26 Suppl 1: S127-S139, 2023 Sep.
Article in English | MEDLINE | ID: mdl-37840026

ABSTRACT

Most studies assessing rates of phenotypic change focus on population mean trait values, whereas a largely overlooked additional component is changes in population trait variation. Theoretically, eco-evolutionary dynamics mediated by such changes in trait variation could be as important as those mediated by changes in trait means. To date, however, no study has comprehensively summarised how phenotypic variation is changing in contemporary populations. Here, we explore four questions using a large database: How do changes in trait variances compare to changes in trait means? Do different human disturbances have different effects on trait variance? Do different trait types have different effects on changes in trait variance? Do studies that established a genetic basis for trait change show different patterns from those that did not? We find that changes in variation are typically small; yet we also see some very large changes associated with particular disturbances or trait types. We close by interpreting and discussing the implications of our findings in the context of eco-evolutionary studies.


Subject(s)
Biological Evolution , Biological Variation, Population , Humans , Phenotype
10.
bioRxiv ; 2023 Jun 26.
Article in English | MEDLINE | ID: mdl-37425734

ABSTRACT

The vertebrate immune system provides an impressively effective defense against parasites and pathogens. However, these benefits must be balanced against a range of costly side-effects including energy loss and risks of auto-immunity. These costs might include biomechanical impairment of movement, but little is known about the intersection between immunity and biomechanics. Here, we show that a fibrosis immune response in threespine stickleback (Gasterosteus aculeatus) has collateral effects on their locomotion. When freshwater stickleback are infected with the tapeworm parasite Schistocephalus solidus, they face an array of fitness consequences ranging from impaired body condition and fertility to an increased risk of mortality. To fight the infection, some stickleback will initiate a fibrosis immune response in which they produce excess collagenous tissue in their coelom. Although fibrosis is effective at reducing infection, some populations of stickleback actively suppress this immune response, possibly because the costs of fibrosis outweigh the benefits. Here we quantify the locomotor effects of the fibrosis immune response in the absence of parasites to investigate whether there are collateral costs of fibrosis that could help explain why some fish forego this effective defense. To do this, we induce fibrosis in stickleback and then test their C-start escape performance. Additionally, we measure the severity of fibrosis, body stiffness, and body curvature during the escape response. We were able to estimate performance costs of fibrosis by including these variables as intermediates in a structural equation model. This model reveals that among control fish without fibrosis, there is a performance cost associated with increased body stiffness. However, fish with fibrosis did not experience this cost but rather displayed increased performance with higher fibrosis severity. This result demonstrates that the adaptive landscape of immune responses can be complex with the potential for wide reaching and unexpected fitness consequences.

11.
Ecol Evol ; 13(6): e10155, 2023 Jun.
Article in English | MEDLINE | ID: mdl-37287852

ABSTRACT

Host-parasite coevolution may lead to patterns of local adaptation in either the host or parasite. For parasites with complex multi-host life cycles, this coevolution may be more challenging as they must adapt to multiple geographically varying hosts. The tapeworm Schistocephalus solidus exhibits some local adaptation to its second intermediate host, threespine stickleback, to which the parasite is strictly specialized. However, the tapeworm's adaptation to its first intermediate host (any of a number of copepod species) is not documented. We investigated if there was local adaptation and host specify in the tapeworm Schistocephalus solidus to its copepod first intermediate hosts. We exposed copepods from five lakes in Vancouver Island (BC, Canada) to local (i.e. same lake) and foreign tapeworms in a reciprocal exposure experiment. Results indicate that the tapeworm is not locally adapted to the copepods. Instead, we observed moderate-effect host specificity, infection rates being higher in certain copepod species than in others. Infection rates also varied among cestode populations. These results show that although S. solidus infects multiple copepod genera, they are not equally competent hosts. Differences in S. solidus epidemiology among lakes is likely to be driven more by this partial specialization, than by local adaptation to first intermediate hosts.

12.
bioRxiv ; 2023 May 19.
Article in English | MEDLINE | ID: mdl-37292793

ABSTRACT

Parasitic infections are a global occurrence and impact the health of many species. Coinfections, where two or more species of parasite are present in a host, are a common phenomenon across species. Coinfecting parasites can interact directly, or indirectly via their manipulation of (and susceptibility to) the immune system of their shared host. Helminths, such as the cestode Schistocephalus solidus , are well known to suppress immunity of their host (threespine stickleback, Gasterosteus aculeatus ), potentially facilitating other parasite species. Yet, hosts can evolve a more robust immune response (as seen in some stickleback populations), potentially turning facilitation into inhibition. Using wild-caught stickleback from 21 populations with non-zero S. solidus prevalence, we tested an a priori hypothesis that S. solidus infection facilitates infection by other parasites. Consistent with this hypothesis, individuals with S. solidus infections have 18.6% higher richness of other parasites, compared to S. solidus -uninfected individuals from the same lakes. This facilitation-like trend is stronger in lakes where S. solidus is particularly successful but is reversed in lakes with sparse and smaller cestodes (indicative of stronger host immunity). These results suggest that a geographic mosaic of host-parasite coevolution might lead to a mosaic of between-parasite facilitation/inhibition effects.

13.
J Evol Biol ; 36(6): 847-873, 2023 06.
Article in English | MEDLINE | ID: mdl-37255207

ABSTRACT

Driven by co-evolution with pathogens, host immunity continuously adapts to optimize defence against pathogens within a given environment. Recent advances in genetics, genomics and transcriptomics have enabled a more detailed investigation into how immunogenetic variation shapes the diversity of immune responses seen across domestic and wild animal species. However, a deeper understanding of the diverse molecular mechanisms that shape immunity within and among species is still needed to gain insight into-and generate evolutionary hypotheses on-the ultimate drivers of immunological differences. Here, we discuss current advances in our understanding of molecular evolution underpinning jawed vertebrate immunity. First, we introduce the immunome concept, a framework for characterizing genes involved in immune defence from a comparative perspective, then we outline how immune genes of interest can be identified. Second, we focus on how different selection modes are observed acting across groups of immune genes and propose hypotheses to explain these differences. We then provide an overview of the approaches used so far to study the evolutionary heterogeneity of immune genes on macro and microevolutionary scales. Finally, we discuss some of the current evidence as to how specific pathogens affect the evolution of different groups of immune genes. This review results from the collective discussion on the current key challenges in evolutionary immunology conducted at the ESEB 2021 Online Satellite Symposium: Molecular evolution of the vertebrate immune system, from the lab to natural populations.


Subject(s)
Adaptive Immunity , Biological Evolution , Animals , Adaptive Immunity/genetics , Vertebrates/genetics , Evolution, Molecular , Immunity, Innate/genetics
14.
Genome Biol Evol ; 15(4)2023 04 06.
Article in English | MEDLINE | ID: mdl-37039516

ABSTRACT

The risk and severity of pathogen infections in humans, livestock, or wild organisms depend on host immune function, which can vary between closely related host populations or even among individuals. This immune variation can entail between-population differences in immune gene coding sequences, copy number, or expression. In recent years, many studies have focused on population divergence in immunity using whole-tissue transcriptomics. But, whole-tissue transcriptomics cannot distinguish between evolved differences in gene regulation within cells, versus changes in cell composition within the focal tissue. 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 broad 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. Furthermore, we demonstrate that identified cell type markers can be used to reinterpret traditional transcriptomic data: we reevaluate previously published whole-tissue transcriptome data from a quantitative genetic experimental infection study to gain better resolution relating infection outcomes to inferred cell type variation. Our combined 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 data sets.


Subject(s)
Cestoda , Cestode Infections , Smegmamorpha , Humans , Animals , Cestode Infections/parasitology , Smegmamorpha/genetics , Cestoda/genetics , Immune System , Sequence Analysis, RNA , Host-Parasite Interactions
15.
bioRxiv ; 2023 Feb 12.
Article in English | MEDLINE | ID: mdl-36798170

ABSTRACT

Indirect genetic effects (IGEs) exist when there is heritable variation in one species' ability to alter a second species' traits. For example, parasites can evolve disparate strategies to manipulate host immune response, whether by evading detection or suppressing immunity. A complication arises during coinfection, when two or more parasite genotypes may try to impose distinct IGEs on the same host trait: which parasite's IGE will be dominant? Here, we apply the notion of dominance to IGEs during coinfection. Using a mathematical model we show that the dominance of IGEs can alter the evolutionary dynamics of parasites. We consider a resident parasite population receiving rare immigrants with a different immune manipulation trait. These immigrants' relative fitness depends on resident prevalence (e.g., the probability immigrants are alone in a host, or coinfecting with a native), and the dominance of the immigrant's IGE on host immunity. Next, we show experimentally that the cestode Schistocephalus solidus exerts an IGE on a host immune trait: parasite antigens from different populations produced different intensities of fibrosis. We then evaluated IGE dominance, finding evidence for overdominance (coinjected antigens induced an even stronger host immune response) which would be detrimental to immigrants when resident prevalence is high. This combination of experimental and modeling results shows that parasites do exhibit IGEs on host traits, and that the dominance of these IGEs during coinfection can substantially alter parasite evolution.

16.
Evolution ; 77(1): 318-328, 2023 Jan 23.
Article in English | MEDLINE | ID: mdl-36622661

ABSTRACT

The concept of a "speciation continuum" has gained popularity in recent decades. It emphasizes speciation as a continuous process that may be studied by comparing contemporary population pairs that show differing levels of divergence. In their recent perspective article in Evolution, Stankowski and Ravinet provided a valuable service by formally defining the speciation continuum as a continuum of reproductive isolation, based on opinions gathered from a survey of speciation researchers. While we agree that the speciation continuum has been a useful concept to advance the understanding of the speciation process, some intrinsic limitations exist. Here, we advocate for a multivariate extension, the speciation hypercube, first proposed by Dieckmann et al. in 2004, but rarely used since. We extend the idea of the speciation cube and suggest it has strong conceptual and practical advantages over a one-dimensional model. We illustrate how the speciation hypercube can be used to visualize and compare different speciation trajectories, providing new insights into the processes and mechanisms of speciation. A key strength of the speciation hypercube is that it provides a unifying framework for speciation research, as it allows questions from apparently disparate subfields to be addressed in a single conceptual model.


Subject(s)
Genetic Speciation , Reproductive Isolation
17.
Evolution ; 77(1): 110-122, 2023 Jan 23.
Article in English | MEDLINE | ID: mdl-36622692

ABSTRACT

Recent studies have shown that the repeated evolution of similar phenotypes in response to similar ecological conditions (here "parallel evolution") often occurs through mutations in the same genes. However, many previous studies have focused on known candidate genes in a limited number of systems. Thus, the question of how often parallel phenotypic evolution is due to parallel genetic changes remains open. Here, we used quantitative trait locus (QTL) mapping in F2 intercrosses between lake and stream threespine stickleback (Gasterosteus aculeatus) from four independent watersheds on Vancouver Island, Canada to determine whether the same QTL underlie divergence in the same phenotypes across, between, and within watersheds. We find few parallel QTL, even in independent crosses from the same watershed or for phenotypes that have diverged in parallel. These findings suggest that different mutations can lead to similar phenotypes. The low genetic repeatability observed in these lake-stream systems contrasts with the higher genetic repeatability observed in other stickleback systems. We speculate that differences in evolutionary history, gene flow, and/or the strength and direction of selection might explain these differences in genetic parallelism and emphasize that more work is needed to move beyond documenting genetic parallelism to identifying the underlying causes.


Subject(s)
Smegmamorpha , Animals , Smegmamorpha/genetics , Rivers , Lakes , Phenotype , Genetic Drift
18.
Ecol Lett ; 26(1): 111-123, 2023 Jan.
Article in English | MEDLINE | ID: mdl-36450600

ABSTRACT

Species competing for resources also commonly share predators. While competition often drives divergence between species, the effects of shared predation are less understood. Theoretically, competing prey species could either diverge or evolve in the same direction under shared predation depending on the strength and symmetry of their interactions. We took an empirical approach to this question, comparing antipredator and trophic phenotypes between sympatric and allopatric populations of threespine stickleback and prickly sculpin fish that all live in the presence of a trout predator. We found divergence in antipredator traits between the species: in sympatry, antipredator adaptations were relatively increased in stickleback but decreased in sculpin. Shifts in feeding morphology, diet and habitat use were also divergent but driven primarily by stickleback evolution. Our results suggest that asymmetric ecological character displacement indirectly made stickleback more and sculpin less vulnerable to shared predation, driving divergence of antipredator traits between sympatric species.


Subject(s)
Perciformes , Smegmamorpha , Animals , Predatory Behavior , Ecosystem , Fishes , Smegmamorpha/genetics , Smegmamorpha/anatomy & histology , Acclimatization
19.
Science ; 377(6611): 1206-1211, 2022 09 09.
Article in English | MEDLINE | ID: mdl-36074841

ABSTRACT

Parasites impose fitness costs on their hosts. Biologists often assume that natural selection favors infection-resistant hosts. Yet, when the immune response itself is costly, theory suggests that selection may sometimes favor loss of resistance, which may result in alternative stable states where some populations are resistant and others are tolerant. Intraspecific variation in immune costs is rarely surveyed in a manner that tests evolutionary patterns, 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 cestode Schistocephalus solidus. Extensive peritoneal fibrosis and inflammation are a commonly observed phenotype that contributes to suppression of cestode growth and viability but also imposes a substantial cost on fecundity. Combining genetic mapping and population genomics, we find that opposing selection generates immune system differences between tolerant and resistant populations, consistent with divergent optimization.


Subject(s)
Cestoda , Fish Diseases , Smegmamorpha , Animals , Cestoda/genetics , Fish Diseases/parasitology , Host-Parasite Interactions/genetics , Immunity , Lakes , Smegmamorpha/genetics
20.
Evol Lett ; 6(2): 162-177, 2022 Apr.
Article in English | MEDLINE | ID: mdl-35386836

ABSTRACT

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 host's 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. Although 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 population, and a resistant lake population) to a novel immune challenge using an injection of (1) a saline control, (2) alum, a generalized pro-inflammatory adjuvant that causes fibrosis, (3) a tapeworm protein extract, or (4) a combination of alum and tapeworm protein. With enough time, all three populations generated a robust fibrosis response to the alum treatments. Yet, only the resistant population exhibited a fibrosis response to the tapeworm protein alone. Thus, these populations differed in their ability to respond to the tapeworm protein but shared an intact fibrosis pathway. The resistant population also initiated fibrosis faster in response to alum, and was able to attenuate fibrosis, unlike the susceptible populations' slow but longer lasting response to alum. As fibrosis has pathological side effects that reduce fecundity, the faster recovery by the resistant population may reflect an adaptation to mitigate the costs of immunity. Broadly, our results confirm that parasite detection and immune initiation, activation speed, and immune attenuation simultaneously contribute to the evolution of parasite resistance and adaptations to infection in natural populations.

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