Populations Of Threespine Stickleback Research Articles

Salinity-induced transcriptome profiles in marine and freshwater threespine stickleback after an abrupt 6-hour exposure.

Saltwater and freshwater environments have opposing physiological challenges, yet, there are fish species that are able to enter both habitats during short time spans, and as individuals they must therefore adjust quickly to osmoregulatory contrasts. In this study, we conducted an experiment to test for plastic responses to abrupt salinity changes in two populations of threespine stickleback, Gasterosteus aculeatus, representing two ecotypes (freshwater and ancestral saltwater). We exposed both ecotypes to abrupt native (control treatment) and non‐native salinities (0‰ and 30‰) and sampled gill tissue for transcriptomic analyses after 6 h of exposure. To investigate genomic responses to salinity, we analyzed four different comparisons; one for each ecotype (in their control and exposure salinity; (1) and (2), one between ecotypes in their control salinity (3), and the fourth comparison included all transcripts identified in (3) that did not show any expressional changes within ecotype in either the control or the exposed salinity (4)). Abrupt salinity transfer affected the expression of 10 and 1530 transcripts for the saltwater and freshwater ecotype, respectively, and 1314 were differentially expressed between the controls, including 502 that were not affected by salinity within ecotype (fixed expression). In total, these results indicate that factors other than genomic expressional plasticity are important for osmoregulation in stickleback, due to the need for opposite physiological pathways to survive the abrupt change in salinity.

The timing and development of infections in a fish-cestode host-parasite system.

The cestode Schistocephalus solidus is a common parasite in freshwater threespine stickleback populations, imposing strong fitness costs on their hosts. Given this, it is surprising how little is known about the timing and development of infections in natural stickleback populations. Previous work showed that young-of-year stickleback can get infected shortly after hatching. We extended this observation by comparing infection prevalence of young-of-year stickleback from 3 Alaskan populations (Walby, Cornelius and Wolf lakes) over 2 successive cohorts (2018/19 and 2019/20). We observed strong variation between sampling years (2018 vs 2019 vs 2020), stickleback age groups (young-of-year vs 1-year-old) and sampling populations.

Copper exposure improves the upper thermal tolerance in a sex-specific manner, irrespective of fish thermal history.

Ectotherms can respond to climate change via evolutionary adaptation, usually resulting in an increase of their upper thermal tolerance. But whether such adaptation influences the phenotypic plasticity of thermal tolerance when encountering further environmental stressors is not clear yet. This is crucial to understand because organisms experience multiple stressors, besides warming climate, in their natural environment and pollution is one of those. Here, we studied the phenotypic plasticity of thermal tolerance in three-spined stickleback populations inhabiting spatially replicated thermally polluted and pristine areas before and after exposing them to a sublethal concentration of copper for one week. We found that the upper thermal tolerance and its phenotypic plasticity after copper exposure did not depend on the thermal history of fish, suggesting that five decades of thermal pollution did not result in evolutionary adaptation to thermal tolerance. The upper thermal tolerance of fish was, on the other hand, increased by ∼ 1.5°C after 1-week copper exposure in a sex-specific manner, with males having higher plasticity. To our knowledge this is the first study that shows an improvement of the upper thermal tolerance as a result of metal exposure. The results suggest that three-spined sticklebacks are having high plasticity and they are capable of surviving in a multiple-stressor scenario in the wild and that male sticklebacks seem more resilient to fluctuating environmental conditions than female.

No signs of behavioral evolution of threespine stickleback following northern pike invasion

AbstractInvasive predators often impose devastating selection pressures on native prey species. However, their effects can be regionally dependent and influenced by the local ecological conditions of their invaded habitats. Evolved behavioral phenotypes are important mechanisms by which prey adapt to the presence of novel predators. Here, we asked how behavior and behavioral plasticity of threespine stickleback (Gasterosteus aculeatus) populations have evolved following the introduction of the invasive predator, northern pike (Esox lucius). We examined the behavior of F1 offspring generated from three pike-free and three pike-invaded populations and measured how stickleback activity and plant use behaviors, and their plasticity, have evolved following pike introduction. To evaluate plasticity, we exposed juvenile stickleback to predator cues during their first year of development and then evaluated how this repeated exposure influenced behavioral responses to an artificial predation event. We found no overarching effect of pike in either evolved behaviors or behavioral plasticity, and no evidence for the presence of developmental plasticity. Furthermore, we found that depending on the phenotype, pike-invaded stickleback populations have either more or less among-population variation than pike-free populations. Our results suggest that evolution in response to invasive predators may be hidden by local adaptation when enough populations are studied.

Evolution of thermal physiology alters the projected range of threespine stickleback under climate change.

Species distribution models (SDMs) are widely used to predict range shifts but could be unreliable under climate change scenarios because they do not account for evolution. The thermal physiology of a species is a key determinant of its range and thus incorporating thermal trait evolution into SDMs might be expected to alter projected ranges. We identified a genetic basis for physiological and behavioural traits that evolve in response to temperature change in natural populations of threespine stickleback (Gasterosteus aculeatus). Using these data, we created geographical range projections using a mechanistic niche area approach under two climate change scenarios. Under both scenarios, trait data were either static ("no evolution" models), allowed to evolve at observed evolutionary rates ("evolution" models) or allowed to evolve at a rate of evolution scaled by the trait variance that is explained by quantitative trait loci (QTL; "scaled evolution" models). We show that incorporating these traits and their evolution substantially altered the projected ranges for a widespread panmictic marine population, with over 7-fold increases in area under climate change projections when traits are allowed to evolve. Evolution-informed SDMs should improve the precision of forecasting range dynamics under climate change, and aid in their application to management and the protection of biodiversity.

Temperature-Dependent Reproductive Success of Stickleback Lateral Plate Morphs: Implications for Population Polymorphism and Range Shifts Under Ocean Warming

Changing environments associated with rapid climate change can shape direct measures of fitness such as reproductive success by altering mating behavior, fecundity and offspring development. Using a polymorphic oceanic population of threespine stickleback (Gasterosteus aculeatus), we investigated whether a 4°C increase in sea surface temperature influenced clutch siring success, reproductive output, and offspring growth among lateral plate morphs. Since low plated morphs are thought to have a selective advantage in warmer environments, we predicted that low plated males should have higher clutch siring success in +4°C environments, and that thermal plasticity of traits (e.g., egg size, offspring growth) should reflect different trait optima in different environments among plate morphs. Parentage analysis of egg clutches revealed temperature-specific clutch siring success, in that low plated males sired more clutches in +4°C environments and completely plated males sired more clutches at ambient (seasonal) temperature. Both completely and low plated females laid larger eggs when acclimated to +4°C, but only completely plated females had smaller clutches at +4°C. Offspring of low and partially plated females grew much less at +4°C compared to those of completely plated females. Taken together, our results demonstrate that ocean warming could impact reproductive success at various levels, with differential effects depending on phenotype, in this case, lateral plate morph. Some traits (clutch siring success, egg size) showed better performance for low plated fish at +4°C, whereas others (e.g., growth) did not. Higher clutch siring success of low plated males at elevated temperature might indicate a future shift in plate morph composition for polymorphic stickleback populations, with potential implications for colonization ability during range shifts under climate change.

Chromosomal Fusions Facilitate Adaptation to Divergent Environments in Threespine Stickleback.

Chromosomal fusions are hypothesized to facilitate adaptation to divergent environments, both by bringing together previously unlinked adaptive alleles and by creating regions of low recombination that facilitate the linkage of adaptive alleles; but, there is little empirical evidence to support this hypothesis. Here, we address this knowledge gap by studying threespine stickleback (Gasterosteus aculeatus), in which ancestral marine fish have repeatedly adapted to freshwater across the northern hemisphere. By comparing the threespine and ninespine stickleback (Pungitius pungitius) genomes to a de novo assembly of the fourspine stickleback (Apeltes quadracus) and an outgroup species, we find two chromosomal fusion events involving the same chromosomes have occurred independently in the threespine and ninespine stickleback lineages. On the fused chromosomes in threespine stickleback, we find an enrichment of quantitative trait loci underlying traits that contribute to marine versus freshwater adaptation. By comparing whole-genome sequences of freshwater and marine threespine stickleback populations, we also find an enrichment of regions under divergent selection on these two fused chromosomes. There is elevated genetic diversity within regions under selection in the freshwater population, consistent with a simulation study showing that gene flow can increase diversity in genomic regions associated with local adaptation and our demographic models showing gene flow between the marine and freshwater populations. Integrating our results with previous studies, we propose that these fusions created regions of low recombination that enabled the formation of adaptative clusters, thereby facilitating freshwater adaptation in the face of recurrent gene flow between marine and freshwater threespine sticklebacks.

Does genetic differentiation underlie behavioral divergence in response to migration barriers in sticklebacks? A common garden experiment

Water management measures in the 1970s in the Netherlands have produced a large number of “resident” populations of three-spined sticklebacks that are no longer able to migrate to the sea. This may be viewed as a replicated field experiment, allowing us to study how the resident populations are coping with human-induced barriers to migration. We have previously shown that residents are smaller, bolder, more exploratory, more active, and more aggressive and exhibited lower shoaling and lower migratory tendencies compared to their ancestral “migrant” counterparts. However, it is not clear if these differences in wild-caught residents and migrants reflect genetic differentiation, rather than different developmental conditions. To investigate this, we raised offspring of four crosses (migrant ♂ × migrant ♀, resident ♂ × resident ♀, migrant ♂ × resident ♀, resident ♂ × migrant ♀) under similar controlled conditions and tested for differences in morphology and behavior as adults. We found that lab-raised resident sticklebacks exhibited lower shoaling and migratory tendencies as compared to lab-raised migrants, retaining the differences in their wild-caught parents. This indicates genetic differentiation of these traits. For all other traits, the lab-raised sticklebacks of the various crosses did not differ significantly, suggesting that the earlier-found contrast between wild-caught fish reflects differences in their environment. Our study shows that barriers to migration can lead to rapid differentiation in behavioral tendencies over contemporary timescales (~ 50 generations) and that part of these differences reflects genetic differentiation.Significance statementMany organisms face changes to their habitats due to human activities. Much research is therefore dedicated to the question whether and how organisms are able to adapt to novel conditions. We address this question in three-spined sticklebacks, where water management measures cut off some populations, prohibiting their seasonal migration to the North Sea. In a previous study, we showed that wild-caught “resident” fish exhibited markedly different behavior than migrants. To disentangle whether these differences reflect genetic differentiation or differences in the conditions under which the wild-caught fish grew up, we conducted crosses, raising the F1 offspring under identical conditions. As their wild-caught parents, the F1 of resident × resident crosses exhibited lower migratory and shoaling tendencies than the F1 of migrant × migrant crosses, while the F1 of hybrid crosses were intermediate. This suggests that ~ 50 years of isolation are sufficient to induce behaviorally relevant genetic differentiation.

Habitat fragmentation induces rapid divergence of migratory and isolated sticklebacks

AbstractThe adaptive capacity of many organisms is seriously challenged by human-imposed environmental change, which currently happens at unprecedented rates and magnitudes. For migratory fish, habitat fragmentation is a major challenge that can compromise their survival and reproduction. Therefore, it is important to study if fish populations can adapt to such modifications of their habitat. Here, we study whether originally anadromous three-spined stickleback populations (Gasterosteus aculeatus; “migrants”) changed in behavior and morphology in response to human-induced isolation. We made use of a natural field-experiment, where the construction of pumping stations and sluices in the 1970s unintendedly created replicates of land-locked stickleback populations (“resident”) in the Netherlands. For two years, we systematically tested populations of residents and migrants for differences in morphology and behavioral traits (activity, aggressiveness, exploration, boldness, and shoaling) in lab-based assays. We detected differences between migrant and resident populations in virtually all phenotypic traits studied: compared with the ancestral migrants, residents were smaller in size, had fewer and smaller plates and were significantly more active, aggressive, exploratory and bolder, and shoaled less. Despite large ecological differences between 2018 and 2019, results were largely consistent across the two years. Our study shows that human-induced environmental change has led to the rapid and consistent morphological and behavioral divergence of stickleback populations in about 50 generations. Such changes may be adaptive but this remains to be tested.

Ecological predictors of lateral line asymmetry in stickleback (Gasterosteus aculeatus)

Threespine stickleback exhibit a row of superficial neuromasts that project through the bony plates on each side of the trunk and which constitute an important sensory modality for detection of near-field water motion. Previously, we have shown that numbers of neuromasts on each structural plate are highly variable among populations. In the current paper, we expand this study to evaluate the extent of deviation from bilateral symmetry of 4344 fish in 57 natural and three transplant populations of threespine stickleback from lakes, streams and oceanic habitats of coastal British Columbia, predicting that neuromasts would be largely bilaterally symmetrical for optimal detection of external stimuli. In contrast, we found asymmetry in all populations, the greatest amount occurring on the anterior buttressing lateral plates and on populations with the fewest neuromasts. We found no consistent trends of signed (directional) asymmetry (SA) among the populations while relative absolute asymmetry (RAA) is lower in dystrophic (stained) habitats than in clearwater habitats (p < 0.001), except for fish with few neuromasts. Sexual dimorphism in RAA is also greater in dystrophic habitats (p < 0.001). Transplants from stained lakes to unstained ponds resulted in a 0.1% to 14% difference in RAA from the source population in less than 12 generations but varied in direction among experiments. Our data suggest a widespread tendency for populations exposed to reduced photic information to exhibit reduced asymmetry in their lateral line system, which can change rapidly in response to a new environment.

Using seasonal genomic changes to understand historical adaptation to new environments: Parallel selection on stickleback in highly-variable estuaries.

Parallel evolution is considered strong evidence for natural selection. However, few studies have investigated the process of parallel selection as it plays out in real time. The common approach is to study historical signatures of selection in populations already well adapted to different environments. Here, to document selection under natural conditions, we study six populations of threespine stickleback (Gasterosteus aculeatus) inhabiting bar-built estuaries that undergo seasonal cycles of environmental changes. Estuaries are periodically isolated from the ocean due to sandbar formation during dry summer months, with concurrent environmental shifts that resemble the long-term changes associated with postglacial colonization of freshwater habitats by marine populations. We used pooled whole-genome sequencing to track seasonal allele frequency changes in six of these populations and search for signatures of natural selection. We found consistent changes in allele frequency across estuaries, suggesting a potential role for parallel selection. Functional enrichment among candidate genes included transmembrane ion transport and calcium binding, which are important for osmoregulation and ion balance. The genomic changes that occur in threespine stickleback from bar-built estuaries could provide a glimpse into the early stages of adaptation that have occurred in many historical marine to freshwater transitions.

Influence of lighting environment on social preferences in sticklebacks from twodifferent photic habitats. II. Shoaling and mate preferences of lab-bred fishes.

Different environmental conditions may lead to diverse morphological, behavioral, and physiological adaptations of different populations of the same species. Lighting conditions, for example, vary vastly especially between aquatic habitats, and have been shown to elicit adaptations. The availability of short-wave ultraviolet (UV) light is especially fluctuating, as UV wavelengths are attenuated strongly depending on water properties. The island of North Uist, Scotland, comprises 2 differential habitat types, tea-stained and clear-water lakes, varying considerably in UV transmission. In previous studies, wild-caught 3-spined stickleback Gasterosteus aculeatus populations (3 populations of each habitat type) were tested with respect to their shoaling and mate preferences for fish viewed under UV-present and UV-absent conditions. The results revealed a habitat-dependent preference of UV cues during shoal choice (tea-stained populations: preference for UV-absent condition in tea-stained water; clear-water populations: no preference in clear-water) but an overall preference for UV-present conditions during mate choice. To assess genetic influences on these behavioral patterns, similar experiments were conducted with lab-bred F1-generations of the same stickleback populations that were raised in a common environment (i.e. standardized clear-water conditions). Offspring of sticklebacks from tea-stained lakes tended to prefer shoals viewed under UV-absent conditions (only in tea-stained water), while sticklebacks from clear-water lakes showed a significant preference for the shoal viewed under UV-present conditions in clear-water but not in tea-stained water. Mate-preference experiments demonstrated that females from the tea-stained lakes significantly preferred and females from the clear-water lakes preferred by trend the male viewed under UV-present conditions in the clear-water treatment. The results for both shoaling- and mate-preference tests were largely similar for wild-caught and lab-bred sticklebacks, thus hinting at a genetic basis for the preference patterns.

Variation in the Sensory Space of Three-spined Stickleback Populations.

The peripheral sensory systems, whose morphological attributes help determine the acquisition of distinct types of information, provide a means to quantitatively compare multiple modalities of a species' sensory ecology. We used morphological metrics to characterize multiple sensory modalities-the visual, olfactory, and mechanosensory lateral line sensory systems-for Gasterosteus aculeatus, the three-spined stickleback, to compare how sensory systems vary in animals that evolve in different ecological conditions. We hypothesized that the dimensions of sensory organs and correlations among sensory systems vary in populations adapted to marine and freshwater environments, and have diverged further among freshwater lake-dwelling populations. Our results showed that among environments, fish differed in which senses are relatively elaborated or reduced. When controlling for body length, littoral fish had larger eyes, more neuromasts, and smaller olfactory tissue area than pelagic or marine populations. We also found differences in the direction and magnitude of correlations among sensory systems for populations even within the same habitat type. Our data suggest that populations take different trajectories in how visual, olfactory, and lateral line systems respond to their environment. For the populations we studied, sensory modalities do not conform in a predictable way to the ecological categories we assigned.

The genomic signature of ecological divergence along the benthic-limnetic axis in allopatric and sympatric threespine stickleback.

The repeated occurrence of similar phenotypes in independent lineages (i.e., parallel evolution) in response to similar ecological conditions can provide compelling insights into the process of adaptive evolution. An intriguing question is to what extent repeated phenotypic changes are underlain by repeated changes at the genomic level and whether patterns of genomic divergence differ with the geographic context in which populations evolve. Here, we combined genomic, morphological and ecological data sets to investigate the genomic signatures of divergence across populations of threespine stickleback (Gasterosteus aculeatus) that adapted to contrasting ecological niches (benthic or limnetic) in either sympatry or allopatry. We found that genome-wide differentiation (FST ) was an order of magnitude higher and substantially more repeatable for sympatric benthic and limnetic specialists compared to allopatric populations with similar levels of ecological divergence. We identified genomic regions consistently differentiated between sympatric ecotypes that were also differentiated between or associated with benthic vs. limnetic niche in allopatric populations. These candidate regions were enriched on three chromosomes known to be involved in the benthic-limnetic divergence of threespine stickleback. Some candidate regions overlapped with QTL for body shape and trophic traits such as gill raker number, traits that strongly differ between benthic and limnetic ecotypes. In summary, our study shows that magnitude and repeatability of genomic signatures of ecological divergence in threespine stickleback highly depend on the geographic context. The identified candidate regions provide starting points to identify functionally important genes for the adaptation to benthic and limnetic niches.

Habitat-Associated Morphological Divergence of Gasterosteus aculeatus in the Southern Caspian Sea Basin

Habitat-associated morphological divergence of the three-spined stickleback, Gasterosteus aculeatus populations was investigated in the southern Caspian Sea basin using landmark-based geometric morphometric method to understand the population structure of this invasive species. A total of 127 specimens were collected from three stations, including the Babol River estuary (center), Gomishan Wetland (east) and the Gisum Coast (west). The left side of each specimen was photographed and 23 landmarks-points were selected to extract body shape data. After generalized procrustes, the data analysis was analyzed using principal components analysis, multivariate analysis of variance/canonical variate analysis and cluster analysis. The results showed a significant difference in body shape between three studied populations (P < 0.001), that were related to the depth and length of the head, the body and caudal peduncle and the positions of the pectoral and ventral fins. Morphological differences of the studied populations can be considered as response to environmental characteristics of their habitats, showing G. aculeatus as a highly successful exotic species to expand its distribution area in the Caspian Sea.

Early life disruption of the microbiota affects organ development and cytokine gene expression in threespine stickleback.

The microbiota that inhabits vertebrates exerts strong effects on host physiology and can be crucial to the development of a normal phenotype. This includes development of the immune system, somatic growth and maintenance, and morphogenesis. However, the genetic background of the host can also affect these life history traits. To this end, we investigated the effects of the microbiota on growth, development, and immune gene expression on two populations of threespine stickleback (Gasterosteus aculeatus), one anadromous and one freshwater. We tested the hypotheses that microbial colonization and the genetic background of the host would affect survival, cytokine gene expression, growth, and development. We raised in vitro crosses of stickleback larvae with and without conventional microbiota. We then exposed all these treatments to Vibrio anguillarum, a potential fish pathogen, in a full factorial design. We found stickleback raised without conventional microbiota had smaller swim bladders relative to those raised with conventional microbiota. Stickleback raised with conventional microbiota exhibited small increases in cytokine gene expression. We found no differences in growth or survival regardless of treatment. These results are consistent with other investigations that show microbiota disruption, in early life, can alter host organ and tissue development and immune responses.

Identification of key proteins involved in stickleback environmental adaptation with system-level analysis.

Using abundance measurements of 1,490 proteins from four separate populations of three-spined sticklebacks, we implemented a system-level approach to correlate proteome dynamics with environmental salinity and temperature and the fish's population and morphotype. We identified robust and accurate fingerprints that classify environmental salinity, temperature, morphotype, and the population sample origin, observing that proteins with specific functions are enriched in these fingerprints. Highly apparent functions represented in all fingerprints include ion transport, proteostasis, growth, and immunity, suggesting that these functions are most diversified in populations inhabiting different environments. Applying a differential network approach, we analyzed the network of protein interactions that differs between populations. Looking at specific population combinations of differential interaction, we identify sets of connected proteins. We find that these sets and their corresponding enriched functions reflect key processes that have diverged between the four populations. Moreover, the extent of divergence, i.e., the number of enriched functions that differ between populations, is highest when all three environmental parameters are different between two populations. Key nodes in the differential interaction network signify functions that are also inherent in the fingerprints, most prominently proteostasis-related functions. However, the differential interaction network also reveals additional functions that have diverged between populations, notably cytoskeletal organization and morphogenesis. The strength of these analyses is that the results are purely data driven. With such an unbiased approach applied on a large proteomic data set, we find the strongest signals given by the data, making it possible to develop more discriminatory and complex biomarkers for specific contexts of interest.

New finding of melanic three-spined sticklebacks Gasterosteus aculeatus in the Scottish Hebrides

Colour traits can be elaborated through sexual selection and have potential to drive reproductive isolation. Male three-spined sticklebacks (Gasterosteus aculeatus) express striking visual signals to attract choosy females during courtship, typically expressed as red carotenoid-based pigmentation on their throat and jaw during the breeding season, along with blue eyes and blue/green flanks. The extent and intensity of red colouration in males have been linked to fitness benefits to females, including body condition, parasite resistance, parental ability and nest defence. In some populations in the Pacific Northwest of North America, male three-spined sticklebacks express melanic nuptial colouration. In these populations, male possess black throats instead of red, and have dark or black bodies. Melanic males are associated with waterbodies that are red-shifted due to the presence of tannins, where the ambient light environment is dominated by long wavelengths. Here we report the first discovery outside North America of melanic populations of three-spined sticklebacks on the island of North Uist in the Scottish Hebrides, on the northwest Atlantic coast of Europe. These populations are associated with a hotspot of stickleback morphological diversity and occur in association with red-shifted waterbodies.

Growth rates in two natural populations of Gasterosteus aculeatus in northwestern Spain: relationships with other life history parameters

We analysed growth rates of two natural populations of the three–spined stickleback fish, Gasterosteus aculeatus, in Galicia (north–west of Spain) where it has a strictly annual life cycle. We used the von Bertalanffy growth model to estimate nonlinear function for length–at–age data sets. These European peripheral populations reach the highest growth rates (k of the von Bertalanffy model &gt; 0.4 month–1) known for this species. Instantaneous mortality rates and fecundity were computed using von Bertalanffy model parameters for each population. Mortality rates found in Galician populations were 2.0–2.3 higher times than those observed in general for Gasterosteidae. Combining both mortality and fertility, different intermediate fitness optima in each population were obtained for mature females. Overall, these differences in life history compared to other studied populations of sticklebacks can be interpreted as local adaptations to a Mediterranean climate type with high degree–days. Consequently, these populations at the edges of the species’ range may have adapted to the unique environmental conditions and may be of interest in ecology and conservation.

Evolution of novel genes in three-spined stickleback populations

Eukaryotic genomes frequently acquire new protein-coding genes which may significantly impact an organism’s fitness. Novel genes can be created, for example, by duplication of large genomic regions or de novo, from previously non-coding DNA. Either way, creation of a novel transcript is an essential early step during novel gene emergence. Most studies on the gain-and-loss dynamics of novel genes so far have compared genomes between species, constraining analyses to genes that have remained fixed over long time scales. However, the importance of novel genes for rapid adaptation among populations has recently been shown. Therefore, since little is known about the evolutionary dynamics of transcripts across natural populations, we here study transcriptomes from several tissues and nine geographically distinct populations of an ecological model species, the three-spined stickleback. Our findings suggest that novel genes typically start out as transcripts with low expression and high tissue specificity. Early expression regulation appears to be mediated by gene-body methylation. Although most new and narrowly expressed genes are rapidly lost, those that survive and subsequently spread through populations tend to gain broader and higher expression levels. The properties of the encoded proteins, such as disorder and aggregation propensity, hardly change. Correspondingly, young novel genes are not preferentially under positive selection but older novel genes more often overlap with FST outlier regions. Taken together, expression of the surviving novel genes is rapidly regulated, probably via epigenetic mechanisms, while structural properties of encoded proteins are non-debilitating and might only change much later.