Thiamin dynamics during the adult life cycle of Atlantic salmon (Salmo salar).

Thiamin is an essential water-soluble B vitamin known for its wide range of metabolic functions and antioxidant properties. Over the past decades, reproductive failures induced by thiamin deficiency have been observed in several salmonid species worldwide, but it is unclear why this micronutrient deficiency arises. Few studies have compared thiamin concentrations in systems of salmonid populations with or without documented thiamin deficiency. Moreover, it is not well known whether and how thiamin concentration changes during the marine feeding phase and the spawning migration. Therefore, samples of Atlantic salmon (Salmo salar) were collected when actively feeding in the open Baltic Sea, after the sea migration to natal rivers, after river migration, and during the spawning period. To compare populations of Baltic salmon with systems without documented thiamin deficiency, a population of landlocked salmon located in Lake Vänern (Sweden) was sampled as well as salmon from Norwegian rivers draining into the North Atlantic Ocean. Results showed the highest mean thiamin concentrations in Lake Vänern salmon, followed by North Atlantic, and the lowest in Baltic populations. Therefore, salmon in the Baltic Sea seem to be consistently more constrained by thiamin than those in other systems. Condition factor and body length had little to no effect on thiamin concentrations in all systems, suggesting that there is no relation between the body condition of salmon and thiamin deficiency. In our large spatiotemporal comparison of salmon populations, thiamin concentrations declined toward spawning in all studied systems, suggesting that the reduction in thiamin concentration arises as a natural consequence of starvation rather than to be related to thiamin deficiency in the system. These results suggest that factors affecting accumulation during the marine feeding phase are key for understanding the thiamin deficiency in salmonids.

Effects of environmental translocation and host characteristics on skin microbiomes of sun-basking fish.

Variation in the composition of skin-associated microbiomes has been attributed to host species, geographical location and habitat, but the role of intraspecific phenotypic variation among host individuals remains elusive. We explored if and how host environment and different phenotypic traits were associated with microbiome composition. We conducted repeated sampling of dorsal and ventral skin microbiomes of carp individuals (Cyprinus carpio) before and after translocation from laboratory conditions to a semi-natural environment. Both alpha and beta diversity of skin-associated microbiomes increased substantially within and among individuals following translocation, particularly on dorsal body sites. The variation in microbiome composition among hosts was significantly associated with body site, sun-basking, habitat switch and growth, but not temperature gain while basking, sex, personality nor colour morph. We suggest that the overall increase in the alpha and beta diversity estimates among hosts were induced by individuals expressing greater variation in behaviours and thus exposure to potential colonizers in the pond environment compared with the laboratory. Our results exemplify how biological diversity at one level of organization (phenotypic variation among and within fish host individuals) together with the external environment impacts biological diversity at a higher hierarchical level of organization (richness and composition of fish-associated microbial communities).

Drivers of neutral and adaptive differentiation in pike (Esox lucius) populations from contrasting environments.

Understanding how eco-evolutionary processes and environmental factors drive population differentiation and adaptation are key challenges in evolutionary biology of relevance for biodiversity protection. Differentiation requires at least partial reproductive separation, which may result from different modes of isolation such as geographic isolation (allopatry) or isolation by distance (IBD), resistance (IBR), and environment (IBE). Despite that multiple modes might jointly influence differentiation, studies that compare the relative contributions are scarce. Using RADseq, we analyse neutral and adaptive genetic diversity and structure in 11 pike (Esox lucius) populations from contrasting environments along a latitudinal gradient (54.9-63.6°N), to investigate the relative effects of IBD, IBE and IBR, and to assess whether the effects differ between neutral and adaptive variation, or across structural levels. Patterns of neutral and adaptive variation differed, probably reflecting that they have been differently affected by stochastic and deterministic processes. The importance of the different modes of isolation differed between neutral and adaptive diversity, yet were consistent across structural levels. Neutral variation was influenced by interactions among all three modes of isolation, with IBR (seascape features) playing a central role, wheares adaptive variation was mainly influenced by IBE (environmental conditions). Taken together, this and previous studies suggest that it is common that multiple modes of isolation interactively shape patterns of genetic variation, and that their relative contributions differ among systems. To enable identification of general patterns and understand how various factors influence the relative contributions, it is important that several modes are simultaneously investigated in additional populations, species and environmental settings.

Size, connectivity and edge effects of stream habitats explain spatio-temporal variation in brown trout (Salmo trutta) density.

Ecological theory postulates that the size and isolation of habitat patches impact the colonization/extinction dynamics that determine community species richness and population persistence. Given the key role of lotic habitats for life-history completion in rheophilic fish, evaluating how the distribution of swift-flowing habitats affects the abundance and dynamics of subpopulations is essential. Using extensive electrofishing data, we show that merging island biogeography with meta-population theory, where lotic habitats are considered as islands in a lentic matrix, can explain spatio-temporal variation in occurrence and density of brown trout (Salmo trutta). Subpopulations in larger and less isolated lotic habitat patches had higher average densities and smaller between-year density fluctuations. Larger lotic habitat patches also had a lower predicted risk of excessive zero-catches, indicative of lower extinction risk. Trout density further increased with distance from the edge of adjacent lentic habitats with predator (Esox lucius) presence, suggesting that edge- and matrix-related mortality contributes to the observed patterns. These results can inform the prioritization of sites for habitat restoration, dam removal and reintroduction by highlighting the role of suitable habitat size and connectivity in population abundance and stability for riverine fish populations.

Intra-population variation in reproductive timing covaries with thermal plasticity of offspring performance in perch Perca fluviatilis.

Life history theory posits that organisms should time their reproduction to coincide with environmental conditions that maximize their fitness. Population-level comparisons have contributed important insights on the adaptive value of reproductive timing and its association to environmental variation. Yet, despite its central role to ecology and evolution, the causes and consequences of variation in reproductive timing among individuals within populations are poorly understood in vertebrates other than birds. Using a combination of observational field studies and a split-brood experiment, we investigated whether differences in breeding time were associated with changes in hatching success, reproductive allocation and reaction norms linking offspring performance to temperature within an anadromous Baltic Sea population of perch Perca fluviatilis. Field observations revealed substantial variation in reproductive timing, with the breeding period lasting almost 2 months and occurring in temperatures ranging from 10 to 21℃. The hatching success of perch decreased as the reproductive season progressed. At the same time, the reproductive allocation strategy changed over the season, late breeders (the offspring of which were introduced into a high resource environment and increased predation pressure) produced more and smaller eggs that resulted in smaller larvae, compared with early breeders. The split-brood experiment in which eggs were incubated in different temperatures (10, 12, 15, 18°C) showed that differences in reproductive timing were associated with a change in the shape of the reaction norm linking offspring performance to water temperature indicative of adaptive phenotypic plasticity, with the offspring of early breeders performing best in low temperatures and the offspring of late breeders performing best in high temperatures. The seasonal changes in reproductive traits and the shape of the thermal performance suggest time-dependent adaptive differences among individuals within the population. Management actions aimed at preserving and restoring variation in the timing of reproductive events will thus likely also influence variation in associated life history traits and thermal performance curves, which could safeguard populations against environmental challenges and changes associated with exploitation and global warming.

Predator-prey role reversal may impair the recovery of declining pike populations.

Many fish populations have experienced declines in recent decades due to anthropogenic disturbances, such as overfishing and habitat exploitation. Despite management actions, many populations show a limited capacity to recover. This may be attributed to reversal of predator-prey roles, yet empirical evidence to that effect remains scarce. Here, we combine field and laboratory studies to investigate the interaction between pike (Esox lucius), a large keystone top predatory fish, and the small-bodied mesopredatory threespine stickleback (Gasterosteus aculeatus) in the Baltic Sea where pike populations have declined. Our data suggest that stickleback predation on pike larvae depletes a large proportion of the recruitment and influences the size distribution through size-selective predation, which is corroborated by a gape-limitation experiment and diet analysis of wild-captured sticklebacks. The effects of stickleback predation are present across several populations and years, and our data suggest that early arrival of sticklebacks has stronger effects on juvenile pike survival. Finally, we use data on pike gape-limitation and the size distribution of sticklebacks to illustrate the process of role reversal. These findings suggest that mesopredator behaviour can reduce recruitment of a top predator species and impair the capacity of populations to recover. This emphasizes predator-prey role reversal as an important ecological and evolutionary driver that influences the outcome of restoration and management actions.

Sun-basking fish benefit from body temperatures that are higher than ambient water.

In terrestrial environments, cold-blooded animals can attain higher body temperatures by sun basking, and thereby potentially benefit from broader niches, improved performance and higher fitness. The higher heat capacity and thermal conductivity of water compared with air have been universally assumed to render heat gain from sun basking impossible for aquatic ectotherms, such that their opportunities to behaviourally regulate body temperature are largely limited to choosing warmer or colder habitats. Here we challenge this paradigm. Using physical models we first show that submerged objects exposed to natural sunlight attain temperatures in excess of ambient water. We next demonstrate that free-ranging carp (Cyprinus carpio) can increase their body temperature during aquatic sun basking close to the surface. The temperature excess gained by basking was larger in dark than in pale individuals, increased with behavioural boldness, and was associated with faster growth. Overall, our results establish aquatic sun basking as a novel ecologically significant mechanism for thermoregulation in fish. The discovery of this previously overlooked process has practical implications for aquaculture, offers alternative explanations for behavioural and phenotypic adaptations, will spur future research in fish ecology, and calls for modifications of models concerning climate change impacts on biodiversity in marine and freshwater environments.

Causes and consequences of repeatability, flexibility and individual fine-tuning of migratory timing in pike.

Many organisms undertake migrations between foraging and breeding habitats and while it is assumed that reproductive timing affects fitness, little is known about the degree of individual consistency, and about the causes and consequences of individual variation in migratory timing in organisms other than birds. Here, we report on a 6-year mark-recapture study, including 2048 individuals, of breeding migration in anadromous pike (Esox lucius), an iteroparous top-predatory fish that displays homing behaviour. By repeated sampling across years at a breeding site, we first quantify individual variation both within and between breeding events and then investigate phenotypic correlates and fitness consequences of arrival timing to the breeding site. Our data demonstrate that males arrive before females, that large males arrive later than small males, that the timing of breeding migration varies among years and that individuals are consistent in their timing across years relative to other individuals in the population. Furthermore, data on return rates indicate that arrival time is under stabilizing viability selection, and that individuals who are more flexible in their timing of arrival during the first reproductive years survive longer compared with less flexible individuals. Finally, longitudinal data demonstrate that individuals consistently fine-tune their arrival timing across years, showing that the timing of arrival to breeding sites is influenced by experience. These findings represent rare evidence of how between- and within-individual variations in migratory timing across breeding events are correlated with phenotypic and fitness traits in an ecologically important keystone species. Our results emphasize the importance of considering variation in migratory timing both between and within individuals in studies investigating the fitness consequences of migratory behaviour and have implications for future management.

Evolutionary divergence of adult body size and juvenile growth in sympatric subpopulations of a top predator in aquatic ecosystems.

Evolutionary theory predicts that different selective regimes may contribute to divergent evolution of body size and growth rate among populations, but most studies have focused on allopatric populations. Here, we studied five sympatric subpopulations of anadromous northern pike (Esox lucius) in the Baltic Sea subjected to allopatric habitats for a short period of their life cycle due to homing behavior. We report differences in adult body size among subpopulations that were in part due to variation in growth rate. Body size of emigrating juveniles also differed among subpopulations, and differences remained when individuals were reared in a common environment, thus indicating evolutionary divergence among subpopulations. Furthermore, a QST-FST comparison indicated that differences had evolved due to divergent selection rather than genetic drift, possibly in response to differences in selective mortality among spawning habitats during the allopatric life stage. Adult and juvenile size were negatively correlated across subpopulations, and reconstruction of growth trajectories of adult fishes suggested that body size differences developed gradually and became accentuated throughout the first years of life. These results represent rare evidence that sympatric subpopulations can evolve differences in key life-history traits despite being subjected to allopatric habitats during only a very short fraction of their life.

Exceptional longevity in northern peripheral populations of Wels catfish (Siluris glanis).

Studies of life-history variation across a species range are crucial for ecological understanding and successful conservation. Here, we examined the growth and age of Wels catfish (Silurus glanis) in Sweden, which represent the northernmost populations in Europe. A total of 1183 individuals were captured, marked and released between 2006 and 2020. Mark-recapture data from 162 individuals (size range: 13-195 cm) were used to estimate von Bertalanffy growth curve parameters which revealed very slow growth rates compared to catfish within the core distribution area (central Europe). The fitted von Bertalanffy growth curve predicted a 150 cm catfish to be around 40 years old, while the largest recaptured individual (length 195 cm) was estimated to be 70 (95% CI 50-112) years old. This was substantially older than the previously documented maximum age of a catfish. The weight at length relationships in these northern peripheral populations were similar to those documented for catfish in central Europe indicating that resources did not constrain growth. This indicates that the slow growth and exceptional high age in the northern catfish populations are the result of lower temperatures and/or local adaptations.

Fish Skin Microbiomes Are Highly Variable Among Individuals and Populations but Not Within Individuals.

Fish skin-associated microbial communities are highly variable among populations and species and can impact host fitness. Still, the sources of variation in microbiome composition, and particularly how they vary among and within host individuals, have rarely been investigated. To tackle this issue, we explored patterns of variation in fish skin microbiomes across different spatial scales. We conducted replicate sampling of dorsal and ventral body sites of perch (Perca fluviatilis) from two populations and characterized the variation of fish skin-associated microbial communities with 16S rRNA gene metabarcoding. Results showed a high similarity of microbiome samples taken from the left and right side of the same fish individuals, suggesting that fish skin microbiomes can be reliably assessed and characterized even using a single sample from a specific body site. The microbiome composition of fish skin differed markedly from the bacterioplankton communities in the surrounding water and was highly variable among individuals. No ASV was present in all samples, and the most prevalent phyla, Actinobacteria, Bacteroidetes, and Proteobacteria, varied in relative abundance among fish hosts. Microbiome composition was both individual- and population specific, with most of the variation explained by individual host. At the individual level, we found no diversification in microbiome composition between dorsal and ventral body sites, but the degree of intra-individual heterogeneity varied among individuals. To identify how genetic and phenotypic characteristics of fish hosts impact the rate and nature of intra-individual temporal dynamics of the skin microbiome, and thereby contribute to the host-specific patterns documented here, remains an important task for future research.

Comparing the Performance of Microsatellites and RADseq in Population Genetic Studies: Analysis of Data for Pike (Esox lucius) and a Synthesis of Previous Studies.

Population genetic studies reveal biodiversity patterns and inform about drivers of evolutionary differentiation and adaptation, including gene flow, drift and selection. This can advance our understanding and aid decision making regarding management and conservation efforts. Microsatellites have long been used in population genetic studies. Thanks to the development of newer techniques, sequencing approaches such as restriction site associated DNA sequencing (RADseq) are on their way to replace microsatellites for some applications. However, the performance of these two marker types in population genetics have rarely been systematically compared. We utilized three neutrally and adaptively differentiated populations of anadromous pike (Esox lucius) to assess the relative performance of microsatellites and RADseq with respect to resolution and conclusiveness of estimates of population differentiation and genetic structure. To this end, the same set of individuals (N = 64) were genotyped with both RADseq and microsatellite markers. To assess effects of sample size, the same subset of 10 randomly chosen individuals from each population (N = 30 in total) were also genotyped with both methods. Comparisons of estimated genetic diversity and structure showed that both markers were able to uncover genetic structuring. The full RADseq dataset provided the clearest detection of the finer scaled genetic structuring, and the other three datasets (full and subset microsatellite, and subset RADseq) provided comparable results. A search for outlier loci performed on the full SNP dataset pointed to signs of selection potentially associated with salinity and temperature, exemplifying the utility of RADseq to inform about the importance of different environmental factors. To evaluate whether performance differences between the markers are general or context specific, the results of previous studies that have investigated population structure using both marker types were synthesized. The synthesis revealed that RADseq performed as well as, or better than microsatellites in detecting genetic structuring in the included studies. The differences in the ability to detect population structure, both in the present and the previous studies, are likely explained by the higher number of loci typically utilized in RADseq compared to microsatellite analysis, as increasing the number of markers will (regardless of the marker type) increase power and allow for clearer detection and higher resolution of genetic structure.

Phenotypic flexibility in background-mediated color change in sticklebacks.

Phenotypic flexibility may incur a selective advantage in changing and heterogeneous environments, and is increasingly recognized as an integral aspect of organismal adaptation. Despite the widespread occurrence and potential importance of rapid and reversible background-mediated color change for predator avoidance, knowledge gaps remain regarding its adaptive value, repeatability within individuals, phenotypic correlates, and whether its expression is context dependent. We used manipulative experiments to investigate these issues in two fish species, the three-spined stickleback (Gasterosteus aculeatus) and nine-spined stickleback (Pungitius pungitius). We sequentially exposed individuals to dark and light visual background treatments, quantified color change from video recordings, and examined associations of color change with phenotypic dimensions that can influence the outcome of predator-prey interactions. G. aculeatus expressed a greater degree of color change compared to P. pungitius. In G. aculeatus, the color change response was repeatable within individuals. Moreover, the color change response was independent of body size but affected by sex and boldness, with males and bolder individuals changing less. Infection by the parasite Schistocephalus solidus did not affect the degree of color change, but it did modulate its association with sex and boldness. G. aculeatus adjusted the expression of color change in response to predation risk, with enhanced color change expression in individuals exposed to either simulated attacks, or olfactory cues from a natural predator. These results provide novel evidence on repeatability, correlated traits, and context dependence in the color change response and highlight how a suite of factors can contribute to individual variation in phenotypic flexibility.

Sex-specific effects of outbreeding on offspring quality in pike (Esox lucius).

Intraspecific genetic admixture occurs when previously separated populations within a species start interbreeding, and it can have either positive, negative, or neutral effects on reproductive performance. As there currently is no reliable predictor for the outcome of admixture, an increased knowledge about admixture effects in different species and populations is important to increase the understanding about what determines the response to admixture. We tested for effects of admixture on F1 offspring quality in three subpopulations of pike (Esox lucius). Gametes were collected in the field, and eggs from each female were experimentally fertilized with milt from a male from each population (one "pure" and two "admixed" treatments). Three offspring quality measures (hatching success, fry survival, and fry length) were determined and compared between (a) pure and admixed population combinations and (b) the sex-specific treatments within each admixed population combination (based on the origin of the male and female, respectively). The results suggested that although there were no overall effects of admixture on offspring quality, the consequences for a given population combination could be sex-specific and thus differ depending on which of the parents originated from one or the other population. All offspring quality traits were influenced by both maternal ID and paternal ID. Sex- and individual-specific effects can have implications for dispersal behavior and gene flow between natural populations, and are important to consider in conservation efforts.

Variation in salinity tolerance between and within anadromous subpopulations of pike (Esox 1ucius).

Environmental heterogeneity is a key determinant of genetic and phenotypic diversity. Stable and homogenous environments tends to result in evolution of specialism and local adaptations, while temporally unpredictable environments may maintain a diversity of specialists, promote generalist strategies, or favour diversified bet hedging strategies. We compared salinity tolerance between two anadromous subpopulations of pike (Esox Lucius) that utilize freshwater spawning sites with different salinity regimes. Eggs from each population were artificially fertilized and incubated in a salinity gradient (0, 3, 5, 7, and 9 psu) using a split-brood design. Effects on embryonic development, hatching success, survival of larvae, and fry body length were compared between populations and families. The population naturally spawning in the stable freshwater habitat showed signs of specialization for freshwater spawning. The population exposed to fluctuating selective pressure in a spawning area with occasional brackish water intrusions tolerated higher salinities and displayed considerable variation in reaction norms. Genetic differences and plasticity of salinity tolerance may enable populations to cope with changes in salinity regimes associated with future climate change. That geographically adjacent subpopulations can constitute separate units with different genetic characteristics must be considered in management and conservation efforts to avoid potentially negative effects of genetic admixture on population fitness and persistence.

Author Correction: Variation in salinity tolerance between and within anadromous subpopulations of pike (Esox lucius).

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has been fixed in the paper.

Testing for Local Adaptation to Spawning Habitat in Sympatric Subpopulations of Pike by Reciprocal Translocation of Embryos.

We tested for local adaption in early life-history traits by performing a reciprocal translocation experiment with approximately 2,500 embryos of pike (Esox lucius) divided in paired split-family batches. The experiment indicated local adaptation in one of the two subpopulations manifested as enhanced hatching success of eggs in the native habitat, both when compared to siblings transferred to a non-native habitat, and when compared to immigrant genotypes from the other subpopulation. Gene-by-environment effects on viability of eggs and larvae were evident in both subpopulations, showing that there existed genetic variation allowing for evolutionary responses to divergent selection, and indicating a capacity for plastic responses to environmental change. Next, we tested for differences in female life-history traits. Results uncovered that females from one population invested more resources into reproduction and also produced more (but smaller) eggs in relation to their body size compared to females from the other population. We suggest that these females have adjusted their reproductive strategies as a counter-adaptation because a high amount of sedimentation on the eggs in that subpopulations spawning habitat might benefit smaller eggs. Collectively, our findings point to adaptive divergence among sympatric subpopulations that are physically separated only for a short period during reproduction and early development-which is rare. These results illustrate how combinations of translocation experiments and field studies of life-history traits might infer about local adaptation and evolutionary divergence among populations. Local adaptations in subdivided populations are important to consider in management and conservation of biodiversity, because they may otherwise be negatively affected by harvesting, supplementation, and reintroduction efforts targeted at endangered populations.

Causes and consequences of intra-specific variation in vertebral number.

Intraspecific variation in vertebral number is taxonomically widespread. Much scientific attention has been directed towards understanding patterns of variation in vertebral number among individuals and between populations, particularly across large spatial scales and in structured environments. However, the relative role of genes, plasticity, selection, and drift as drivers of individual variation and population differentiation remains unknown for most systems. Here, we report on patterns, causes and consequences of variation in vertebral number among and within sympatric subpopulations of pike (Esox lucius). Vertebral number differed among subpopulations, and common garden experiments indicated that this reflected genetic differences. A QST-FST comparison suggested that population differences represented local adaptations driven by divergent selection. Associations with fitness traits further indicated that vertebral counts were influenced both by stabilizing and directional selection within populations. Overall, our study enhances the understanding of adaptive variation, which is critical for the maintenance of intraspecific diversity and species conservation.

Ecology, evolution, and management strategies of northern pike populations in the Baltic Sea.

Baltic Sea populations of the northern pike (Esox lucius) have declined since the 1990s, and they face additional challenges due to ongoing climate change. Pike in the Baltic Sea spawn either in coastal bays or in freshwater streams and wetlands. Pike recruited in freshwater have been found to make up about 50 % of coastal pike stocks and to show natal homing, thus limiting gene flow among closely located spawning sites. Due to natal homing, sub-populations appear to be locally adapted to their freshwater recruitment environments. Management actions should therefore not involve mixing of individuals originating from different sub-populations. We offer two suggestions complying with this advice: (i) productivity of extant freshwater spawning populations can be boosted by modifying wetlands such that they promote spawning and recruitment; and (ii) new sub-populations that spawn in brackish water can potentially be created by transferring fry and imprinting them on seemingly suitable spawning environments.