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Maciejewski, M. F.

Publications and source records attributed to Maciejewski, M. F..

7 recordsLinked to original sources

Building neuroanatomical resources for three-spined sticklebacks: Brain areas important for social behavior

IntroductionThree-spined stickleback fish are famous for their diversity and charismatic social behavior. However, there are few neuroanatomical resources for studying the neural and brain mechanisms underlying their fascinating behavior. Methods and ResultsWe identify 11 brain areas important for social behavior by referencing brain atlases for six other teleost fishes. Brain regions were identified via neuroanatomical landmarks and we characterized the presence / absence of tyrosine hydroxylase (TH), a key gene product of the dopaminergic system, in those regions. Comparing the neuroanatomical location of these regions in the stickleback brain and the expression of TH therein to that of other fish species highlights similarities and differences and the need for a brain atlas specific to sticklebacks. This resource serves as a map of the location of regions important for social behavior in the stickleback brain. ConclusionThis resource will help guide future studies connecting gene function to social behavior through the brain and will enable future work to understand the evolution of neural mechanisms that contribute to the diversity of social behavior in this emerging model organism.

neuroscience↗

Rapid genome-wide introgression reveals fitness advantage of immigrant genotypes

Evolutionary biology has long recognized the tendency for populations to be locally adapted to their ancestral habitat, resulting in higher resident fitness. However, immigrants can also introduce beneficial alleles. The resulting adaptive introgression is usually inferred retrospectively, rather than as a contemporary process. Here, we document exceptionally rapid ongoing adaptive introgression in a lake population of threespine stickleback (Gasterosteus aculeatus). In the first generations after a discrete immigration event, all chromosomes exhibited large increases in immigrant ancestry due to linkage disequilibrium. After a decade, the extent of introgression varied across the genome. The fastest-evolving genes included Spi1b, which enables an increased fibrosis defense against a previously common tapeworm, whose prevalence then declined dramatically. This case study highlights the capacity for immigration to supply beneficial alleles that drive rapid genome-wide evolution.

evolutionary biology↗

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↗

Evidence of parental care as a novel reproductive isolating mechanism

Variation in behavior can contribute to reproductive isolation by preventing gene flow among populations. Here, we tested the novel hypothesis that parental care, when dysregulated, can function as a reproductive isolating mechanism in three-spined stickleback fish (Gasterosteus aculeatus). In the typical "common" stickleback ecotype, males provide care to their offspring by fanning with their pectoral fins and defending their nest. In contrast, a divergent "white" stickleback ecotype has evolutionarily lost care and disperses embryos into the surrounding environment. We examined how paternal care from common, white, and F1 hybrid fathers influenced offspring survival. We detected no intrinsic incompatibilities in embryos, but F1 hybrid fathers exhibited dysregulated parental care that coincided with decreased survival of parented offspring. The increased offspring mortality may be explained by further dysregulation of feeding and parenting circuitry, as F2 hybrids exhibited significantly higher rates of post-fertilization filial cannibalism than common or white fathers. Additionally, despite strong divergence in nesting-building and courtship behavior, F1 hybrids achieved mating success at a similar rate as male commons and whites, suggesting that prezygotic barriers against hybrids may be weak. The observed postzygotic isolation, and potentially weak prezygotic isolation in lab-based studies, suggest that hybridization is likely occurring at low rates in the wild. Population genetic analysis supported this, as low proportions of putative hybrids were detected in sympatric sites. Together, these results may help explain why genetic divergence between these phenotypically distinct ecotypes is low and provide evidence that dysregulated parental behavior can act as a newly discovered postzygotic reproductive isolating barrier.

evolutionary biology↗

An evolutionary shift to prioritizing mating over care is associated with consistently high androgen levels in male threespine stickleback

Steroid hormones play a role in regulating social behaviors in vertebrates, but how they mediate the evolution of these traits remains an open question. Here, we use liquid chromatography-mass spectrometry (LC-MS/MS) to quantify a panel of steroids in breeding males of two recently diverged populations of threespine stickleback. The common ecotype provides paternal care, while the white ecotype has evolutionarily lost paternal care. Hormone levels were quantified in both ecotypes at three reproductive stages: (1) after completing a nest, (2) soon after mating, when commons start to provide care and whites disperse the embryos, and (3) four days after mating, when commons are performing parental care and no longer courting females while whites are not providing care and are courting females. Androgens declined in the common ecotype as they began providing care but remained elevated in the white ecotype across stages, possibly to maintain the production of "spiggin," the androgen-dependent glue males use to construct nests. Progestogen levels were low in whites and were lowest in commons after mating, suggesting an antagonistic relationship between progestogens and sexual behavior. Both ecotypes showed elevated glucocorticoids after mating, suggesting the stress axis may not have diverged between ecotypes. Altogether, these results provide evidence that the ecotypes regulate steroid levels differently to support the ways they balance mating and parental effort. Our data suggest a variety of mechanisms by which steroid signaling and regulation can change during the early stages of divergence between behaviorally distinct populations.

animal behavior and cognition↗

Locomotor effects of a fibrosis-based immune response in stickleback fish

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.

evolutionary biology↗

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↗