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The Evolutionary Biology of the Three Spine Sticklebacks
Journal of Animal Ecology
... Substantial research shows that threespine sticklebacks show extensive geographic variation among populations in a multitude of phenotypic traits and are often genetically differentiated (M. A. Bell and Foster 1994).This includes variation among populations in predation regimes and anti-predator responses (Nick Giles and Huntingford 1984;Ålund et al. 2022), as well as the overall incidence of parasitism and which parasites typically infect them (Young and MacColl 2016). Recently, population variation in the microbiome and its role in adapting to distinct environments has received attention(Rennison, Rudman, and Schluter 2019; Härer et al. 2023) including adapting to varying parasite communities (C. ...
Background
The role of predation stress in driving behavioral and microbial-host interaction changes is recognized, but the impact of microbial composition in aquatic organisms and its relationship with stress-related behavior remains poorly understood. This study explored the relationship between antipredator behavior, parasitism, and the gut microbiome in wild stickleback fish populations from two different lakes: Galtaból, clear and spring-fed versus Þristikla, turbid and glacial-fed. We aimed to identify potential links between these factors by analyzing behavioral responses to simulated predation, comparing microbiomes between populations with or without parasite infection, and examining potential correlations between behavior and microbiome composition.
Results
Behavioral analysis revealed differences between populations, with each exhibiting unique baseline behaviors i.e., higher activity in Galtaból fish and higher angular velocity in Þristikla fish, and varied responses to the presence of predator i.e., increased boldness in Galtaból fish and higher activity in Þristikla fish. The response to the predator attack was similar between fish from both populations. Parasitism influenced behavior, with parasitized fish displaying increased boldness. Microbiome analysis showed that a small proportion of its variation was explained by population, likely reflecting differences in lake environments. Only the marine genus Pseudoalteromonas abundance differed between populations. Parasitism in Galtaból fish population was linked to decreased alpha diversity in the microbiome, with an increase in specific microbial taxa, including potential pathogens, and a decrease in commensal microbes.
Conclusions
Our findings suggest that behavior and microbiome correlations may primarily reflect environmental adaptations and parasite status rather than direct gut-brain interactions. However, some tentative evidence suggests a potential innate connection between swimming activity, stress levels, and specific microbes. The study highlights the complexity of the gut-brain axis in wild populations and suggests future research directions, including experimental manipulations to uncover causal relationships between microbiome composition and behavior.
... Threespine stickleback have repeatedly colonized freshwater lakes, rivers, and streams in the Northern Hemisphere (McPhail 1993, Bell andFoster 1994). Most male threespine sticklebacks develop a bright red throat in the breeding season that extends from the mouth to the pelvic spines, and contrasts with a blue-black eye (Fig. 1). ...
Sensory drive can lead to the evolution of signals that are optimized to the environment in which they are perceived. However, when environmental conditions change, the interactions between signal, environment, and receiver may also shift, leading to the evolution of a new signal optimum or more categorical shifts in sexual signals (gains or losses). We evaluated how visual systems have evolved following a change in environment and male signal, and whether visual system divergence contributes to reproductive isolation between ancestral and derived types in red and black morphs of Pacific Northwest freshwater threespine stickleback. We found that opsin sequence was tuned to enhance the perceived contrast of black fish on a red-shifted light background, whereas opsin expression was not. Further, we found no evidence for homotypic preferences or assortative mating between colour morphs; males of both morphs were equally successful in no-choice mating contexts, perhaps because black males are more vigorous courters. Together, our results suggest that habitat transitions in black stickleback have led to a shift in sensory-drive dynamics with some aspects of the visual system and behaviour evolving in response to other factors (foraging or predation) or lagging behind the evolution of opsin sequences in red-shifted environments.
... Our findings highlight the value of web-building spiders as a model system to examine the role of context dependence in the evolution of adaptations. The literature offers many examples of morphological and behavioral antipredator adaptations, from sticklebacks to guppies and beyond (Bell andFoster 1995, Valkonen et al. 2012), but limited treatment of extended phenotypes also being subject to, and feeding back on such pressures. Lessons from the spider system can illuminate the interplay of forces shaping animals and the structures they build. ...
Animals exhibit a variety of strategies to avoid predation; spiders are no exception. We explored whether web-building spiders that differ in the architecture of their webs exhibit morphologies or behaviors suggestive of antipredator strategies that trade-off with the degree of protection offered by their webs. Spiders build webs of 3 types: the more protected tangles and sheet-and-tangles, which are three-dimensional (3D), and the more exposed orbs, which are two-dimensional (2D), both with or without a refuge. We hypothesize that spiders whose webs offer greater protection—a 3D architecture or a refuge—will be less likely to be armored or brightly colored when compared to spiders without these protections. We collected data on 446 spiders and their webs in 2 lowland tropical rainforest sites. We show that 2D web builders with no refuges tended to be brightly colored (background contrasting) and spiny (spiky), whereas those with refuges tended to blend against the background of their refuges. 3D web builders, on the other hand, were neither cryptic nor brightly colored nor armored but were more likely to drop out of the web upon simulated predator contact. These results support the hypothesis that web-building spiders tend to be protected either through the architecture of their webs or their morphology and behavior, suggesting a trade-off between different types of antipredator strategies.
... First, diversification in geographic radiations is facilitated by higher opportunities for allopatric speciation due to the presence of plentiful geographic barriers (Simões et al., 2016). Indeed, geographic barriers played a significant role in several adaptive radiations, including Darwin's finches on the Galapagos islands (Abzhanov, 2010), anoles in the Neotropics (Poe et al., 2017), and threespine sticklebacks in North American lakes (Bell & Foster, 1995). Consequently, besides an undisputed role of morphological and ecological divergence in these radiations, geographic barriers might have acted additively to accelerate the diversification of these clades. ...
Evolutionary radiations provide important insights into species diversification, which is especially true of adaptive radiations. New World wood warblers (Parulidae) are a family of small, insectivorous, forest-dwelling passerine birds, often considered an exemplar adaptive radiation due to their rapid diversification followed by a slowdown. However, they deviate from the expectations of an adaptive radiation scenario due to the lack of conspicuous morphological and ecological differentiation. We fitted several macroevolutionary models to trait data in 105 species of wood warblers. We tested whether morphological traits underwent an early burst of evolution (suggesting adaptation to new ecological niches in adaptive radiations) and whether song and colour underwent a diversity-dependent acceleration of trait evolutionary rate (consistent with reproductive interference driving signal evolution). Morphology and song evolved gradually under stabilizing selection, suggesting niche conservatism, with morphology possibly acting as a constraint on song evolution. In contrast, many feather colour traits underwent a diversity-dependent burst of evolution occurring late in the clade’s history. We suggest that a two-step process has led to the remarkable diversification of wood warblers. First, their early diversification probably proceeded by allopatric speciation. Second, feather colour divergence likely occurred during secondary contact after range expansion. This diversification of signalling traits might have facilitated species coexistence, in combination with behavioural niche partitioning. Wood warblers seem to present characteristics of both adaptive and non-adaptive radiations.
... There is also substantial data on stickleback with which to form predictions about the spatial and ecological factors associated with infection. Threespine stickleback are present throughout much of the coastal and inland waters of the northern hemisphere, with occasional sightings even in the ocean's depths (Bell & Foster, 1994). Stickleback possess high levels of morphological variation throughout their range, and have freshwater and anadromous populations which return to freshwater to breed. ...
Although adaptive morphological variation has been identified across a great diversity of taxa, little work has been dedicated to animal parasites. This is surprising given the expectation that antagonistic interactions between hosts and parasites are expected to drive rapid evolution. While morphological evidence of host adaptation to parasites is widespread, for most parasites we lack even basic information about intraspecific variation, let alone hypotheses on how this variation is connected to infection outcomes due to the host-centric focus. To address this data gap, I investigated morphological variation within populations of the cestode Schistocephalus solidus across numerous Alaskan populations of threespine stickleback. Previous studies have noted high levels of parasite-associated adaptive immune variation in the cestode's specific host-threespine stickleback (Gasterosteus aculeatus), and this work developed strong field and lab methods for measuring infection phenotypes. Although I measured many features of S. solidus morphological variation, I predicted that the parasite's tegument, the primary site of all interactions with the fish host, would be a strong candidate site for adaptive evolution due to the constant arms race in this coevolutionary model. I found that most features of parasite morphology were constrained across populations, but tegument thickness (relative to total parasite diameter) was best explained by the host population's recent marine or freshwater ancestry, with the marine populations having an approximately 17% reduction in relative tegument size. I further showed that this variation could be recapitulated in the lab, suggesting that cestode tegument thickness exhibits phenotypic plasticity, reflecting genetic differences in hosts and the intra-host environment, not cestodes. These results show. how well-described host-parasite models can be used to fill gaps in knowledge about coevolutionary dynamics.
... The stickleback evolutionary history consists of colonization of a wide range of aquatic habitats, both marine and freshwater, and has been associated with adaptive divergence among derived populations (Reynolds et al. 1995). Due to their unique population genetic structure, recent studies have utilized stickleback to understand host-microbe interactions in the gut microbiome (Barber and Scharsack 2010). ...
There have been several significant new findings regarding Microsporidia of fishes over the last decade. Here we provide an update on new taxa, new hosts and new diseases in captive and wild fishes since 2013. The importance of microsporidiosis continues to increase with the rapid growth of finfish aquaculture and the dramatic increase in the use of zebrafish as a model in biomedical research. In addition to reviewing new taxa and microsporidian diseases, we include discussions on advances with diagnostic methods, impacts of microsporidia on fish beyond morbidity and mortality, novel findings with transmission and invertebrate hosts, and a summary of the phylogenetics of fish microsporidia.Keywords
Glugea anomala
Molecular phylogeneticsMaternal transmission
Desmozoon lepeophtherii
Ovipleistophora diplostomuri
When conducting research, reproducibility and correct assessment of the results obtained are important tasks that require the use of modern methods and approaches. To assess the state of biological systems, significance testing of the null hypothesis with respect to the assumed values of the “norm” is often used. To assess the state of biological systems, a common approach is to test the significance of the null hypothesis in relation to the assumed values of the “norm”. Recently, however, the dichotomous approach of confirming or rejecting the null hypothesis has been criticized by data analysts due to the lack of validation of methods for assessing p-level significance and the biological validity of the hypotheses under investigation. Consequently, a novel methodology for identifying the “normal” state of biological systems was proposed and developed into the theory of reference values (RV). Furthermore, the concepts of reference interval (RI) and reference values have become prevalent in various research fields. Our study evaluated the relative intervals of several antioxidant system (AOS) parameters (glutathione S-transferase, catalase, guaiacol-dependent peroxidase, superoxide dismutase) in the liver and muscles of male three-spined stickleback Gasterosteus aculeatus L. in the Seldianaya Inlet of White Sea during the spawning period. The three-spined stickleback is a species that is abundant in the White Sea and has been the subject of numerous studies on population genetics, evolutionary biology, and ecology. AOS plays a role in the defense of the organism against the negative influence of exogenous and endogenous factors causing oxidative stress. Its indicators are used as biomarkers of the physiological state of the organism. The activity of AOS enzymes in stickleback samples from other biotopes of the White Sea (Sukhaya Salma Strait and Koliushkovaya Lagoon) was also compared with each other and relatively calculated RI. Stickleback from the Koliushkovaya Lagoon and the Sukhaya Salma Strait differed in liver superoxide dismutase activity, and the mean values of enzyme activity were included in the RI. To assess the reproducibility of statistical tests, the effect of stickleback sample size on the result of comparing samples was modeled using t-criterion, and the type of dependence and sample sizes at 50% probability of a positive test were determined. The data obtained on biomarkers of oxidative stress in male G. aculeatus may prove useful for monitoring the state of stickleback populations with the aim of developing this species as a model object for ecological studies of both the White Sea ecosystem and the fish population in this reservoir.
The context and cause of adaptive radiations have been widely described and explored but why rapid evolutionary diversification does not occur in related evolutionary lineages has yet to be understood. The standard answer is that evolutionary diversification is provoked by ecological opportunity and that some lineages do not encounter the opportunity. Three‐spined sticklebacks on the Scottish island of North Uist show enormous diversification, which seems to be associated with the diversity of aquatic habitats. Sticklebacks on the neighboring island of South Uist have not been reported to show the same level of evolutionary diversity, despite levels of environmental variation that we might expect to be similar to North Uist. In this study, we compared patterns of morphological and environmental diversity on North and South Uist. Ancestral anadromous sticklebacks from both islands exhibited similar morphology including size and bony “armor.” Resident sticklebacks showed significant variation in armor traits in relation to pH of water. However, North Uist sticklebacks exhibited greater diversity of morphological traits than South Uist and this was associated with greater diversity in pH of the waters of lochs on North Uist. Highly acidic and highly alkaline freshwater habitats are missing, or uncommon, on South Uist. Thus, pH appears to act as a causal factor driving the evolutionary diversification of stickleback in local adaptation in North and South Uist. This is consistent with diversification being more associated with ecological constraint than ecological opportunity. Evolutionary diversification is often thought to arise from “ecological opportunity:” A reduction in competition for resources following the invasion of a new habitat. Here, we show that diversification may be provoked by ecological constraint: Organisms invading habitats, in this case, acid freshwater, may be free from competition but have poor resource availability.
Appendages have been reduced or lost hundreds of times during vertebrate evolution. This phenotypic convergence may be underlain by shared or different molecular mechanisms in distantly related vertebrate clades. To investigate, we reviewed the developmental and evolutionary literature of appendage reduction and loss in more than a dozen vertebrate genera from fish to mammals. We found that appendage reduction and loss was nearly always driven by modified gene expression as opposed to changes in coding sequences. Moreover, expression of the same genes was repeatedly modified across vertebrate taxa. However, the specific mechanisms by which expression was modified were rarely shared. The multiple routes to appendage reduction and loss suggest that adaptive loss of function phenotypes might arise routinely through changes in expression of key developmental genes. Appendages have been independently reduced or lost hundreds of times during vertebrate evolution. Despite that selection seems to routinely favor a reduced appendage, we found that the specific mechanisms to appendage reduction and loss are rarely shared, even when the same genes were involved.
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