Gasterosteus Aculeatus Research Articles

Genetic structure and historic demography of endangered unarmoured threespine stickleback at southern latitudes signals a potential new management approach.

Habitat loss, flood control infrastructure, and drought have left most of southern California and northern Baja California's native freshwater fish near extinction, including the endangered unarmoured threespine stickleback (Gasterosteus aculeatus williamsoni). This subspecies, an unusual morph lacking the typical lateral bony plates of the G. aculeatus complex, occurs at arid southern latitudes in the eastern Pacific Ocean and survives in only three inland locations. Managers have lacked molecular data to answer basic questions about the ancestry and genetic distinctiveness of unarmoured populations. These data could be used to prioritize conservation efforts. We sampled G. aculeatus from 36 localities and used microsatellites and whole genome data to place unarmoured populations within the broader evolutionary context of G. aculeatus across southern California/northern Baja California. We identified three genetic groups with none consisting solely of unarmoured populations. Unlike G. aculeatus at northern latitudes, where Pleistocene glaciation has produced similar historical demographic profiles across populations, we found markedly different demographics depending on sampling location, with inland unarmoured populations showing steeper population declines and lower heterozygosity compared to low armoured populations in coastal lagoons. One exception involved the only high elevation population in the region, where the demography and alleles of unarmoured fish were similar to low armoured populations near the coast, exposing one of several cases of artificial translocation. Our results suggest that the current "management-by-phenotype" approach, based on lateral plates, is incidentally protecting the most imperilled populations; however, redirecting efforts toward evolutionary units, regardless of phenotype, may more effectively preserve adaptive potential.

ЭКОЛОГИЯ ПИТАНИЯ СИВУЧА С РЕПРОДУКТИВНОГО ЛЕЖБИЩА НА МЫСЕ КОЗЛОВА (ВОСТОЧНАЯ КАМЧАТКА)

We studied the Steller's sea lion Eumetopias jubatus feeding ecology based on undigested food items found in feces at the Kozlova Cape rookery, Eastern coast of Kamchatka Peninsula, in summers (2004 through 2008). Atka mackerel Pleurogrammus monopterygius and walleye pollock Theragra chalcogramma were dominant in a sea lion diet hauled out at Kozlova Cape rookery in terms of frequency of occurrence. Less frequently occurred were Pacific sand lance Ammodytes hexapterus, Threespine stickleback Gasterosteus aculaeatus, Smelt Osmerus mordax, Sculpins Cottidae, Pacific sandfish Trichodon trichodon, Flatfishes Pleuronectidae, Salmon Oncorhynchus sp., Pacific cod Gadus macrocephalus, and Squid and Octopus Cephalopoda. The contribution of the other food items was not significant. Diet diversity median during sea lion single foraging trip was two prey items, range being one to nine Atka mackerel and Walleye pollock as the major prey objects. Most of sea lion food items were referred to species featuring a marked seasonal presence near the shore or on the shelf. Sea lions feed near the rookery close to the shore on seasonal food aggregations common to the area. Seasonal prey aggregations can be extremely important for breeding animals due to increasing the efficiency of food search and capture, which in turn can affect the reproductive success of animals and their survival. In this regard, the stability of the food resource near Kozlova Cape Rookery may influence sea lion population status there.

A warmer environment can reduce sociability in an ectotherm.

The costs and benefits of being social vary with environmental conditions, so individuals must weigh the balance between these trade-offs in response to changes in the environment. Temperature is a salient environmental factor that may play a key role in altering the costs and benefits of sociality through its effects on food availability, predator abundance, and other ecological parameters. In ectotherms, changes in temperature also have direct effects on physiological traits linked to social behaviour, such as metabolic rate and locomotor performance. In light of climate change, it is therefore important to understand the potential effects of temperature on sociality. Here, we took the advantage of a 'natural experiment' of threespine sticklebacks from contrasting thermal environments in Iceland: geothermally warmed water bodies (warm habitats) and adjacent ambient-temperature water bodies (cold habitats) that were either linked (sympatric) or physically distinct (allopatric). We first measured the sociability of wild-caught adult fish from warm and cold habitats after acclimation to a low and a high temperature. At both acclimation temperatures, fish from the allopatric warm habitat were less social than those from the allopatric cold habitat, whereas fish from sympatric warm and cold habitats showed no differences in sociability. To determine whether differences in sociability between thermal habitats in the allopatric population were heritable, we used a common garden breeding design where individuals from the warm and the cold habitat were reared at a low or high temperature for two generations. We found that sociability was indeed heritable but also influenced by rearing temperature, suggesting that thermal conditions during early life can play an important role in influencing social behaviour in adulthood. By providing the first evidence for a causal effect of rearing temperature on social behaviour, our study provides novel insights into how a warming world may influence sociality in animal populations.

Timing of reproduction modifies transgenerational effects of chronic exposure to stressors in an annual vertebrate.

Stressful environmental conditions can shape both an individual's phenotype and that of its offspring. However, little is known about transgenerational effects of chronic (as opposed to acute) stressors, nor whether these vary across the breeding lifespan of the parent. We exposed adult female (F0 generation) three-spined sticklebacks (Gasterosteus aculeatus) to chronic environmental stressors and compared their reproductive allocation with that of non-exposed controls across early, middle and late clutches produced within the single breeding season of this annual population. There was a seasonal trend (but no treatment difference) in F0 reproductive allocation, with increases in egg mass and fry size in late clutches. We then tested for transgenerational effects in the non-exposed F1 and F2 generations. Exposure of F0 females to stressors resulted in phenotypic change in their offspring and grandoffspring that were produced late in their breeding lifespan: F1 offspring produced from the late-season clutches of stressor-exposed F0 females had higher early life survival, and subsequently produced heavier eggs and F2 fry that were larger at hatching. Changed maternal allocation due to a combination of seasonal factors and environmental stressors can thus have a transgenerational effect by influencing the reproductive allocation of daughters, especially those born late in life.

Spatial heterogeneity in pH, body size and habitat size generates ecological opportunity in an evolutionary radiation.

Much of the biological diversity we see today is thought to be the product of evolutionary radiation, the rapid proliferation of species from a single ancestor into multiple discrete forms. Spatial heterogeneity in environmental variables has been proposed as creating the necessary ecological opportunity to stimulate evolutionary radiation. Nonetheless, the ecological mechanisms generating and maintaining diversity in spatially heterogeneous environments are not fully understood. The authors investigated the role of strong spatial heterogeneity in generating ecological opportunity in an evolutionary radiation of freshwater populations of the three-spined stickleback (Gasterosteus aculeatus L.) on the island of North Uist using a spatially explicit Bayesian model. The authors identified pH, loch surface area and body size as predictors of variance in the number of lateral plates that comprise anti-predator armour in G. aculeatus. An East-West gradient of pH, a product of the distinctive environment of North Uist, generates a robust selective environment facilitating G. aculeatus evolutionary radiation. Larger lochs were associated with atypical phenotypes, possibly related to larger population sizes and greater selection efficiency. An association between pH and lateral plate number is likely an effect of body size, with a positive relationship between body size and lateral plate number that is mediated by swimming efficiency in G. aculeatus.

Risk of invasiveness of non-native fishes in the South Caucasus biodiversity and geopolitical hotspot

Aquatic invasions are one of the major threats for freshwater ecosystems. However, in developing countries, knowledge of biological invasions, essential for the implementation of appropriate legislation, is often limited if not entirely lacking. In this regard, the identification of potentially invasive non-native species by risk screening, followed by a full risk assessment of the species ranked as higher risk, enables decision-makers to be informed about the extent of the threats posed to the recipient (risk assessment) area. In this study, 32 non-native extant and horizon fish species were screened for their risk of invasiveness under current and predicted climate conditions for the South Caucasus – a biodiversity and geopolitical hotspot that includes the countries of Armenia, Azerbaijan and Georgia. Overall, the number of very high-risk species increased from four (12.5%) under current climate conditions to 12 (37.5%) under predicted climate conditions. The highest-risk species under both conditions included the already established gibel carp Carassius gibelio and topmouth gudgeon Pseudorasbora parva, the locally translocated pikeperch Sander lucioperca and the horizon North African catfish Clarias gariepinus. Under predicted climate conditions, a very high risk of invasiveness was predicted also for the translocated three-spined stickleback Gasterosteus aculeatus and Eurasian perch Perca fluviatilis, for the already established eastern mosquitofish Gambusia holbrooki, ruffe Gymnocephalus cernua, sharpbelly Hemiculter leucisculus and Nile tilapia Orechromis niloticus, and for the horizon pumpkinseed Lepomis gibbosus and largemouth bass Micropterus salmoides. Future research on the non-native species in the South Caucasus should be conducted both country- and region-wide and should account not only for the high biodiversity, but also for the critical geopolitical situation affecting the study area.

Macro-Habitat Suitability for Threespine Stickleback (Gasterosteus aculeatus L.) Near the Southern Limit of Its Global Distribution: Implications for Species Management and Conservation

The threespine stickleback is a freshwater fish listed as endangered in Portugal, near the southern limit of the species global distribution. However, few measures have been proposed aiming at the conservation of this species in suboptimal environments. From existing databases and specific sampling campaigns, we obtained occurrence data of threespine stickleback for a total of 646 sites. The occurrence data, together with 15 environmental macrohabitat predictors, were used to model the potential distribution of the species using an ensemble of species distribution models. Through the results of our final ensemble, we project that the threespine stickleback occurs predominantly at lower stretches of river systems, where sandy substrate is dominant and flow is higher. Within this region, sticklebacks are also more likely to occur in sites with high levels of rainfall in the driest month, thus avoiding locations with high potential for drying during summer. The species also tends to avoid steep slope areas with high levels of annual precipitation. Based on our results, a map of the species probability of occurrence was generated and river sections were categorized into levels according to their importance for the species’ conservation.

Sexually mediated phenotypic variation within and between sexes as a continuum structured by ecology: The mosaic nature of skeletal variation across body regions in Threespine stickleback (Gasterosteus aculeatus L.).

Ecological character displacement between the sexes, and sexual selection, integrate into a convergent set of factors that produce sexual variation. Ecologically modulated, sexually mediated variation within and between sexes may be a major contributor to the amount of total variation that selection can act on in species. Threespine stickleback (Gasterosteus aculeatus) display rapid adaptive responses and sexual variation in many phenotypic traits. We examined phenotypic variation in the skull, pectoral and pelvic girdles of threespine stickleback from two freshwater and two coastal marine sites on the Sunshine Coast of British Columbia, Canada, using an approach that avoids a priori assumptions about bimodal patterns of variation. We quantified shape and size of the cranial, pectoral and pelvic regions of sticklebacks in marine and freshwater habitats using 3D geometric morphometrics and an index of sexually mediated variation. We show that the expression of phenotypic variation is structured in part by the effects of both habitat marine vs freshwater and the effects of individual sites within each habitat. Relative size exerts variable influence, and patterns of phenotypic variation associated with sex vary among body regions. This fine‐grained quantification of sexually mediated variation in the context of habitat difference and different anatomical structures indicates a complex relationship between genetically inferred sex and environmental factors, demonstrating that the interplay between shared genetic background and sexually mediated, ecologically based selective pressures structures the phenotypic expression of complex traits.

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.

Activity of Enzymes of Energy and Carbohydrate Metabolism in Juveniles of Three-Spined Stickleback Gasterosteus aculeatus (Gasterosteidae) from Different Biotopes of the White Sea

Activity of Enzymes of Energy and Carbohydrate Metabolism in Juveniles of Three-Spined Stickleback Gasterosteus aculeatus (Gasterosteidae) from Different Biotopes of the White Sea

Evolutionary gain and loss of a pathological immune response to parasitism.

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

Extreme intraspecific divergence in mitochondrial haplotypes makes the threespine stickleback fish an emerging evolutionary mutant model for mito-nuclear interactions.

Mitochondrial DNA is primarily maternally inherited in most animals and evolves about 10 times faster than biparentally inherited nuclear DNA. Mitochondrial dysfunction (mt-dys) arises when interactions between the co-evolving mitochondrial and nuclear genomes are perturbed in essential processes like oxidative phosphorylation (OXPHOS). Over time mt-dys can lead to mitochondrial diseases (mt-diseases), which are surprisingly prevalent and include common diseases such as Alzheimer’s, Parkinson’s, and diabetes. Unfortunately, the strong impact that intraspecific mitochondrial and nuclear genetic variation has on mt-disease complicates its study and the development of effective treatments. Animal models have advanced our understanding of mt-disease but their relevance to human conditions is often limited by their relatively low nuclear genetic diversity. Many traditional laboratory models also typically have a single mitochondrial haplotype (mitotype), in stark contrast to over 5,000 mitotypes in humans worldwide. The threespine stickleback fish has an evolutionary history that has made it a favorable evolutionary mutant model (EMM) for studying mito-nuclear interactions and possibly mt-diseases. EMMs are species with naturally evolved states that mimic maladaptive human diseases. In threespine stickleback, a period of isolation followed by introgression of the mitochondrial genome from a sister species resulted in the maintenance of two distinct mitochondrial haplotypes which continue to segregate within many populations of wild stickleback. The existence of two mitogenomes segregating in numerous genetically diverse populations provides a unique system for exploring complex mito-nuclear dynamics. Here we provide the first complete coding region analysis of the two threespine stickleback mitotypes, whose mitogenomic divergence exceeds that of other mammalian models for mitochondrial disease and even that between ancient and modern humans. We find that divergence is not uniform across the mitogenome, but primarily impacts protein coding genes, and significantly impacts proteins in Complex I of OXPHOS. The full characterization of these highly divergent intraspecific mitotypes provides a foundation for the development of threespine stickleback as an EMM for mito-nuclear interactions.

Evolution of stickleback spines through independent cis-regulatory changes at HOXDB

Understanding the mechanisms leading to new traits or additional features in organisms is a fundamental goal of evolutionary biology. We show that HOXDB regulatory changes have been used repeatedly in different fish genera to alter the length and number of the prominent dorsal spines used to classify stickleback species. In Gasterosteus aculeatus (typically ‘three-spine sticklebacks’), a variant HOXDB allele is genetically linked to shortening an existing spine and adding an additional spine. In Apeltes quadracus (typically ‘four-spine sticklebacks’), a variant HOXDB allele is associated with lengthening a spine and adding an additional spine in natural populations. The variant alleles alter the same non-coding enhancer region in the HOXDB locus but do so by diverse mechanisms, including single-nucleotide polymorphisms, deletions and transposable element insertions. The independent regulatory changes are linked to anterior expansion or contraction of HOXDB expression. We propose that associated changes in spine lengths and numbers are partial identity transformations in a repeating skeletal series that forms major defensive structures in fish. Our findings support the long-standing hypothesis that natural Hox gene variation underlies key patterning changes in wild populations and illustrate how different mutational mechanisms affecting the same region may produce opposite gene expression changes with similar phenotypic outcomes.

12. Deadly snack: mortality of a European grass snake Natrix natrix while attempting to feed on a three-spined stickleback Gasterosteus aculeatus

12. Deadly snack: mortality of a European grass snake Natrix natrix while attempting to feed on a three-spined stickleback Gasterosteus aculeatus

Interactive Effects of Lake Morphometry and Sticklebacks on the Trophic Position of Arctic charr, Salvelinus alpinus (L.), across Lakes in Western Greenland

The structure and functioning of Arctic ecosystems have been drastically modified by global warming, with fish species potentially performing habitat shifts such as the northern expansion of generalist and warm-adapted species. The freshwater fish species Arctic charr (Salvelinus alpinus, hereafter charr) plays a key role in Arctic lake food webs, but sticklebacks (Gasterosteus aculeatus) may impact the trophic position (TP) of charr by affecting their habitat choice and food resources. In the present study, we used multiple regression analyses to examine the role of lake morphology (i.e., depth and area) and the influence of sticklebacks on the TP of charr (estimated from δ15N and δ13C) sampled in nine Arctic lakes in Western Greenland between 2011 and 2013. Results showed that charr populations exhibited larger TP values when co-occurring with sticklebacks. Specifically, for larger and deeper lakes, a significant positive effect on TP values was observed for medium-sized (25 to 35 cm) charr. Moreover, the TP of sticklebacks had a null effect on the TP values of the largest charr (> 40 cm), suggesting that the largest-sized charr individuals did not prey on sticklebacks. We conclude that charr undergoes flexible ontogenetic trophic trajectories depending on the species composition of the Arctic fish community structure (here presence or absence of sticklebacks) and abiotic lake features.

Habitat change alters the expression and efficiency of a female ornament.

Anthropogenic habitat changes are disrupting the mate choice process in a range of organisms, with consequences for populations and communities. Research has so far focused on male sexually selected traits and female mate choice, given their conspicuousness, whereas effects on female ornaments and male mate choice have been largely overlooked. Yet, females of many species develop ornaments that males use in mate choice. These ornaments can be costly and reduce female fecundity and viability and, hence, influence population growth rate. Thus, attention should be paid to changes in female ornaments and the consequences the changes have for populations. Here, we show that declining visibility in aquatic ecosystems reduces the investment of female three-spined stickleback in a melanin-based ornament in favor of increased mate search activity. The adjustment appears adaptive as males pay less attention to the ornament under poor visibility, and as melanin-based ornaments are generally physiologically costly. It is likely that past fluctuations in visibility have promoted the evolution of environment-dependent plasticity in female ornamentation. More attention should be paid to changes in female ornaments and their adaptive value, across taxa, given the impact that female investment in ornaments can have on fecundity and population growth rate. Environments are changing at an accelerating rate because of human activities and knowledge of the responses of both males and females is needed to evaluate and predict the ultimate impact on populations and biodiversity.

Intergeneric hybridization of two stickleback species leads to introgression of membrane-associated genes and invasive TE expansion

Interspecific hybridization has occurred relatively frequently during the evolution of vertebrates. This process usually abolishes reproductive isolation between the parental species. Moreover, it results in the exchange of genetic material and can lead to hybridogenic speciation. Hybridization between species has predominately been observed at the interspecific level, whereas intergeneric hybridization is rarer. Here, using whole-genome sequencing analysis, we describe clear and reliable signals of intergeneric introgression between the three-spined stickleback (Gasterosteus aculeatus) and its distant mostly freshwater relative the nine-spined stickleback (Pungitius pungitius) that inhabit northwestern Russia. Through comparative analysis, we demonstrate that such introgression phenomena apparently take place in the moderate-salinity White Sea basin, although it is not detected in Japanese sea stickleback populations. Bioinformatical analysis of the sites influenced by introgression showed that they are located near transposable elements, whereas those in protein-coding sequences are mostly found in membrane-associated and alternative splicing-related genes.

The importance of considering the duration of extreme temperatures when investigating responses to climate change.

The frequency and duration of heatwaves are increasing because of human activities. To cope with the changes, species with longer generation times may have to rely on plastic responses. The probability that their responses are adaptive is higher if the species have experienced temperature fluctuations also in their evolutionary past. However, experimental studies investigating responses to heatwaves often use exposure times that are significantly shorter than recent heatwaves. We show that this can lead to faulty conclusions and that the duration of higher temperature has to be considered in experimental designs. We recorded the response of threespine stickleback to prolonged duration of higher temperature during the breeding season, using a population that has experienced large fluctuations in temperature in its past and, hence, is expected to endure temperature changes well. We found males to adaptively adjust their reproductive behaviours to short periods of higher temperature, but not to longer periods that extended across two breeding cycles. Males initially increased their reproductive activities-nest building, courtship and parental care-which ensured high reproductive success during the first breeding cycle, but decreased their reproductive activities during the second breeding cycle when exposed to sustained high temperature. This reduced their courtship success and resulted in fewer offspring. Thus, a species expected to cope well with higher temperature suffers fitness reductions when the duration of high temperature is prolonged. The results stress the importance of considering the duration of extreme environmental conditions when investigating the impact that human activities have on species. Responses to short-term exposures cannot be extrapolated to assess responses to longer periods of extreme conditions.

Round-the-World Voyage of the Threespine Stickleback (Gasterosteus aculeatus): Phylogeographic Data Covering the Entire Species Range

A total of 205 COI sequences and 310 cyt b sequences of the threespine stickleback (Gasterosteus aculeatus) from basins of all seas throughout the vast range of this species were analyzed. Median networks of haplotypes constructed in this study, combined with the results of reconstruction of paleogeographic conditions, led to the conclusion that the threespine stickleback emerged as a species in the Pacific Ocean basin and spread to Europe from the south, populating the system of water bodies that existed in the Oligocene. The main water body was the Paratethys Ocean (Sea), which existed 5–34 Mya. In the area of the modern North Sea, stickleback populations, part of which later migrated to the eastern and western coasts of North America, gave rise to the group of haplotypes that has the widest distribution in northern Europe. The stickleback populations belonging to the lineage that dispersed along the Arctic and western coasts of North America displaced the carriers of the haplotypes of the ancient phylogenetic lineage that inhabited the Pacific coast. The ancestors of G. wheatlandi dispersed from the Pacific to the Atlantic Ocean via the Arctic to meet G. aculeatus, which circled the globe from east to west.

Laboratory measures of boldness correlate with ecological niche in threespine stickleback

AbstractResearch on among individual variation in behavior has increased rapidly in recent years. It is intuitively appealing that variation in the behavior of individuals has ecological consequences, for example, on trophic niche. Bold individuals, with a tendency to be explorative and risk‐tolerant, can be less likely to alter their foraging behavior based on context and, therefore, forage more consistently. Stable isotopes are a useful tool to retrospectively estimate ecological niche and have been found to correlate with foraging behavior in the wild and can be used to extend studies to further examine the ecological or evolutionary relevance of animal personality measured in the laboratory. We examined if common behavioral traits related to ecological niche in the wild using a rapid behavioral assay and δ13C and δ15N stable isotopes from fin and muscle, reflecting ecological niche for the previous weeks and months. We found that bolder stickleback (and females) were enriched in δ13C compared with shyer stickleback (and males) but the covariation of gender and stable isotope values complicate inferences. Nevertheless, the current results highlight the long‐term ecological importance of among individual variation in behavior and are among the first to support a correlation between laboratory measures of behavior and ecological niche in the wild and to document gender differences in stable isotope values of fish.