The tale of the bad stepfather: male three-spined sticklebacks Gasterosteus aculeatus L. recognize foreign eggs in their manipulated nest by egg cues alone

The ability to discriminate between own and foreign eggs was investigated in brood-caring male three-spined sticklebacks Gasterosteus aculeatus . Males totally cannibalized clutches that contained both foreign and their own eggs significantly more often than sham-manipulated control clutches that only contained their own eggs. These results show that caring males are able to recognize the presence of foreign eggs by egg cues alone.     

棕色田鼠幼仔对父鼠的早期识别及条件位置偏爱

群居性动物的幼仔对亲本的识别有利于获得最大化的亲本抚育。雄性棕色田鼠对幼仔具有较高水平的父本投资,那么幼仔在断乳前是否能够识别父鼠并形成条件位置偏爱(Conditioned place preference,CPP)呢?本研究通过双向选择测试、社会互作测试以及CPP 测试探讨了这一问题。双向选择结果显示,与陌生雄鼠相比,出生后14 d 和21 d 的幼仔对父鼠访问的持续时间及潜伏期有显著性差异(P < 0.05);社会互作结果表明,14 d幼仔对父鼠的跟随行为较陌生雄鼠多,但探究行为及亲密行为没有显著性差异(P > 0.05),21 d 幼仔对父鼠的探究行为较少、跟随行为和亲密行为较多(P < 0.05)。CPP 结果表明,在连续4 d (出生后13 ～ 16 d;19 ～ 22 d)的父鼠强化后,第17 d 和第23 d 的幼仔不能形成对父鼠的位置偏爱(P > 0.05)。这些结果说明断乳前的棕色田鼠幼仔已能够识别父鼠和陌生雄鼠,但不能形成对父鼠的位置偏爱。     

Three‐spined sticklebacks Gasterosteus aculeatus as a model for exploring behavioural biology

Niko Tinbergen chose the three‐spined stickleback Gasterosteus aculeatus for his classic behavioural studies because they are small, robust, common and easy to house in the laboratory under reasonably natural conditions and also because their behaviour, while sufficiently simple to be tractable, is still sufficiently complex to be interesting. An analysis of citation records shows that this was an inspired choice. Research on these small fish has addressed all four of Tinbergen's famous questions (causation, development, functions and evolution) and has contributed to the understanding of many different behavioural systems. The G. aculeatus literature is used here to explore several themes in fundamental behavioural biology (diet choice, shoaling, behavioural syndromes and sexual signalling) and the extent to which research using G. aculeatus has informed both fundamental and applied behavioural biology, the latter in the context of aquaculture research.     

Body size and food-patch finding in a stickleback shoal

In mixed shoals of small and large three-spined sticklebacks Gasterosteus aculeatus , there were no differences between small and large fish in the probability of finding a food patch, nor in the time of their patch discovery.     

Evaluation of ovum fixation and storage in three-spined stickleback

Ripe eggs removed from three-spined sticklebacks stored in 50% isopropyl alcohol showed significantly Sower mean masses than those stored in 10% formalin. These results are considered in relationship to preservation techniques for stickleback.     

Evolution and assessment of colour patterns in stream-resident and anadromous male threespine stickleback Gasterosteus aculeatus from three regions

We compared the colour patterns of free swimming, reproductively active male threespine stickleback Gasterosteus aculeatus of the anadromous and stream ecotypes from three geographically distinct regions. Consistent with the hypothesis of environmentally mediated selection, our results indicate ecologically replicated differences in G. aculeatus coloration between anadromous and stream-resident populations, and that G. aculeatus probably have the visual acuity to discriminate colour pattern differences between anadromous and stream-resident fish.     

Schooling affects growth in the three-spined stickleback, Gasterosteus aculeatus

Three-spined stickleback fry (mean length 20 mm, mean weight 14 mg) were reared for 14 days alone and in groups of six in a constant per capita water volume. The fish originated from two habitats (rock-pools, sea) of different predation pressure. The fry were fed nauplii of Artemia and commercial aquarium fish food ad libitum. Specific growth rates of solitary and schooling fry differed and were also affected by their origin. The specific growth rates of solitary fry from the sea averaged 1.0% day⁻¹ (length) and 6.0% day⁻¹ (weight) and those of solitary rock-pool fry 1.1 and 6.7%, respectively. For group-reared fish the corresponding values were 1.2% (length) and 6.6% (weight), and 1.3% (length) and 7.6% (weight). The finding that schooling sticklebacks grow faster than solitary ones implies that grouping enhances fitness in stickleback fry under the conditions of our experiments.     

Genetic relationships among marine and freshwater populations of the European three-spined stickleback (Gasterosteus aculeatus) revealed by microsatellites

To assess the population genetic structure of the three-spined stickleback, Gasterosteus aculeatus, variability at 18 microsatellite loci was examined in 1724 individuals from 74 locations covering most of the species distribution range in Europe. The results revealed high overall degree of differentiation (F(ST) = 0.21) but contrasting level of divergence and genetic variability between habitat types. Marine populations were genetically relatively uniform even across great geographical distances as compared to substantial differentiation among freshwater populations. Analysis of molecular variance indicated low but significant (2.7%) variation in allele frequencies between geographical regions, but a negligible effect of habitat type (0.2%). The phylogenetic pattern was not explained by habitat type, but a weak signal of populations clustering according to geographical or water system origin was found. The results support the view that three-spined stickleback marine ancestors colonized northern European fresh waters during the postglacial marine submergence c. 10,000 years ago, whereas in the Mediterranean region colonization probably dates back to the Pleistocene. The independent origins of river and lake populations indicate that they originate from multiple colonizations rather than sharing common ancestry. In the continuous marine environment, the low degree of differentiation among populations can be explained by gene flow among subpopulations and large effective population size buffering divergence in neutral markers. In contrast, among postglacially established freshwater populations differentiation appears to be driven by genetic drift and isolation. The stepwise mutations appear to have contributed to the population differentiation in the southern part of the three-spined stickleback distribution range.     

“Micropersonality” traits and their implications for behavioral and movement ecology research

1. Many animal personality traits have implicit movement‐based definitions and can directly or indirectly influence ecological and evolutionary processes. It has therefore been proposed that animal movement studies could benefit from acknowledging and studying consistent interindividual differences (personality), and, conversely, animal personality studies could adopt a more quantitative representation of movement patterns.
2. Using high‐resolution tracking data of three‐spined stickleback fish (Gasterosteus aculeatus), we examined the repeatability of four movement parameters commonly used in the analysis of discrete time series movement data (time stationary, step length, turning angle, burst frequency) and four behavioral parameters commonly used in animal personality studies (distance travelled, space use, time in free water, and time near objects).
3. Fish showed repeatable interindividual differences in both movement and behavioral parameters when observed in a simple environment with two, three, or five shelters present. Moreover, individuals that spent less time stationary, took more direct paths, and less commonly burst travelled (movement parameters), were found to travel farther, explored more of the tank, and spent more time in open water (behavioral parameters).
4. Our case study indicates that the two approaches—quantifying movement and behavioral parameters—are broadly equivalent, and we suggest that movement parameters can be viewed as “micropersonality” traits that give rise to broad‐scale consistent interindividual differences in behavior. This finding has implications for both personality and movement ecology research areas. For example, the study of movement parameters may provide a robust way to analyze individual personalities in species that are difficult or impossible to study using standardized behavioral assays.

     

The three-spined stickleback as an environmental sentinel: effects of stressors on whole-body physiological indices

Indicators of a generalized stress response (changes in cortisol, glucose, RNA: DNA ratio and total protein) when measured in whole-body preparations of individual three-spined sticklebacks Gasterosteus aculeatus displayed significant alterations in response to acute (hours) and chronic (days) disturbances and food withdrawal. In addition, changes in alkali-labile phosphorous, a specific biomarker of exposure to oestrogenic contaminants, could be detected in whole-body preparations of oestrogen-exposed three-spined sticklebacks confirming that the measurement of biomarkers normally assessed in a specific tissue can be equally possible in whole fish.     

No sibling odor preference in juvenile three-spined sticklebacks

Laboratory-bred juvenile three-spined sticklebacks from 11 sibshipsdid not prefer to shoal with their siblings when they were offeredthe choice between odor from unfamiliar siblings and non-kinin a fluviarium, although the power for finding a significantpreference was very high (0.99). The test fish preferred theside where odor from the heavier shoal was supplied; this shows thatthey could appreciate odor cues from conspecifics in our apparatusand should have preferred their siblings if such a preferenceexists. Our results are compatible with theoretical predictionsbut are at variance with previous findings by other authors.We used independent replicates in a blind protocol with strictrandomization of fish and procedures.     

Body condition and reproductive status in sticklebacks exposed to a single wave of Schistocephalus solidus infection

This paper describes the results of a study of the effects of Schistocephalus solidus on one of its intermediate hosts, the stickleback Gasterosteus aculeatus , in an annual population in which infection is known to occur in one major wave in autumn. Weight, as a function of length, was lower in infected sticklebacks compared with uninfected fish during autumn and spring; in winter and summer, both categories of fish were in equally poor condition. In early autumn, the hepatosomatic indices of newly infected fish were higher than those of uninfected fish, perhaps due to a pathological response. Thereafter, relative liver size of uninfected and infected sticklebacks was comparable until spring, when it increased sharply in uninfected sticklebacks but remained stable at a low level in infected sticklebacks. Few infected fish reached maturity. The only males to attain maturity whilst sustaining an infection of S. solidus were in particularly good condition. Nuptial coloration, kidney hypertrophy and testes size were unimpaired in these mature infected males, but whether they were capable of successful reproduction remains debatable.     

Ancestral Plasticity and Allometry in Threespine Stickleback Fish Reveal Phenotypes Associated with Derived, Freshwater Ecotypes

For over a century, evolutionary biologists have debated whether and how phenotypic plasticity impacts the processes of adaptation and diversification. The empirical tests required to resolve these issues have proven elusive, mainly because it requires documentation of ancestral reaction norms, a difficult prospect where many ancestors are either extinct or have evolved. The threespine stickleback radiation is not limited in this regard, making it an ideal system in which to address general questions regarding the role of plasticity in adaptive evolution. As retreating ice sheets have exposed new habitats, oceanic stickleback founded innumerable freshwater populations, many of which have evolved parallel adaptations to their new environments. Because the founding oceanic population is extant, we can directly evaluate whether specific patterns of ancestral phenotypic expression in the context of novel environments (plasticity), or over ontogeny, predisposed the repeated evolution of "benthic" and "limnetic" ecotypes in shallow and deep lakes, respectively. Consistent with this hypothesis, we found that oceanic stickleback raised in a complex habitat and fed a macroinvertebrate diet expressed traits resembling derived, benthic fish. Alternatively, when reared in a simple environment on a diet of zooplankton, oceanic stickleback developed phenotypes resembling derived, limnetic fish. As fish in both treatments grew, their body depths increased allometrically, as did the size of their mouths, while their eyes became relatively smaller. Allometric trajectories were subtly but significantly impacted by rearing environment. Thus, both environmental and allometric influences on development, along with their interactive effects, produced variation in phenotypes consistent with derived benthic and limnetic fish, which may have predisposed the repeated genetic accommodation of this specific suite of traits. We also found significant shape differences between marine and anadromous stickleback, which has implications for evaluating the ancestral state of stickleback traits.     

Otolith development in wild populations of stickleback: Jones & Hynes method does not apply to most populations

This paper critiques Jones & Hynes (1950) findings by analysing sequential samples of otoliths from three wild populations of Gasterosteus aculeatus from North Uist, Scotland and Nottingham, England. Contrary to Jones & Hynes (1950), but coincident with the finding of later researchers, our results showed that no true translucent ring formed in the otolith of G. aculeatus during their first summer. The first translucent ring was probably starting to be formed by the end of summer and was completed by the end of their first winter. There was no second opaque ring in the otoliths of G. aculeatus before they passed their first winter. The second opaque ring was just starting to appear by early April of the second year in the southern population i.e. Nottingham, but later, by May, in the northern populations i.e. North Uist. Formation of the opaque ring in G. aculeatus mostly occurs in spring and summer, with younger fish starting earlier. In contrast, the formation of translucent rings is mostly during autumn and winter, but can be more widespread through the year, possibly as a result of reproductive investment.     

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.     

Female stickleback prefer shallow males: Sexual selection on nest microhabitat

Sexual selection is most often thought of as acting on organismal traits, such as size or color. However, individuals’ habitat use may also affect mating success. Here, we show that, in threespine stickleback, nest depth can be a target of sexual selection. In postglacial lakes in British Columbia, male threespine stickleback nest in a narrow range of depths. Prior studies revealed heritable variation in males’ preferred nest microhabitat. We surveyed four natural populations, finding that male stickleback with shallower nests were more successful at breeding. Indeed, nest depth was a much stronger predictor of male mating success than more commonly studied targets of sexual selection in stickleback (size, condition, shape, color, infection status). This selection on nest depth means that variance in fitness changed predictably across microhabitats, altering the opportunity for sexual selection to act on other traits. Accordingly, we show that sexual selection on other male traits is strongest where variance in nesting success is highest (at intermediate nest depths in some lakes). We conclude that males’ choice of nesting microhabitat is an especially important target of sexual selection, resulting in fine‐scale spatial variation in sexual selection on other traits.     

Morphological and physiological traits of Mediterranean sticklebacks living in the Camargue wetland (Rhone river delta)

Three-spined sticklebacks (Gasterosteus aculeatus L.) living at the southern limit of the species distribution range could possess specific morphological and physiological traits that enable these fish to live at the threshold of their physiological capacities. Morphological analysis was carried out on samples of sticklebacks living in different saline habitats of the Camargue area (Rhone delta, northern Mediterranean coast) obtained from 1993 to 2017. Salinity acclimation capacities were also investigated using individuals from freshwater-low salinity drainage canals and from mesohaline–euryhaline lagoons. Fish were maintained in laboratory conditions at salinity values close to those of their respective habitats: low salinity (LS, 5‰) or seawater (SW, 30‰). Fish obtained from a mesohaline brackish water lagoon (BW, 15‰) were acclimated to SW or LS. Oxygen consumption rates and branchial Na⁺/K⁺-ATPase (NKA) activity (indicator of fish osmoregulatory capacity) were measured in these LS or SW control fish and in individuals subjected to abrupt SW or LS transfers. At all the studied locations, only the low-plated “leiurus” morphotype showed no spatial or temporal variations in their body morphology. Gill rakers were only longer and denser in fish sampled from the LS–freshwater (FW) drainage canals. All fish presented similar physiological capacities. Oxygen consumption rates were not influenced by salinity challenge except in SW fish transferred to LS immediately and 1 h after transfer. However, and as expected, gill NKA activity was salinity dependent. Sticklebacks of the Camargue area sampled from habitats with contrasted saline conditions are homogenously euryhaline, have low oxygen consumption rates and do not appear to experience significantly greater metabolic costs when challenged with salinity. However, an observed difference in gill raker length and density is most probably related to the nutritional condition of their habitat, indicating that individuals can rapidly acclimatize to different diets.     

Genetic variation in MHC class II expression and interactions with MHC sequence polymorphism in three-spined sticklebacks

Genes of the major histocompatibility complex (MHC) have been studied for several decades because of their pronounced allelic polymorphism. Structural allelic polymorphism is, however, not the only source of variability subjected to natural selection. Genetic variation may also exist in gene expression patterns. Here, we show that in a natural population of three-spined sticklebacks (Gasterosteus aculeatus) the expression of MHC class IIB genes was positively correlated with parasite load, which indicates increased immune activation of the MHC when infections are frequent. To experimentally study MHC expression, we used laboratory-bred sticklebacks that were exposed to three naturally occurring species of parasite. We found strong differences in MHC class IIB expression patterns among fish families, which were consistent over two generations, thus demonstrating a genetic component. The average number of MHC class IIB sequence variants within families was negatively correlated to the MHC expression level suggesting compensatory up-regulation in fish with a low (i.e. suboptimal) MHC sequence variability. The observed differences among families and the negative correlation with individual sequence diversity imply that MHC expression is evolutionary relevant for the onset and control of the immune response in natural populations.     

Effects of genetics and light environment on colour expression in threespine sticklebacks

The genetic basis of traits that are under sexual selection and that are involved in recognizing conspecific mates is poorly known, even in systems in which the phenotypic basis of these traits has been well studied. In the present study, we investigate genetic and environmental influences on nuptial colour, which plays important roles in sexual selection and sexual isolation in species pairs of limnetic and benthic threespine sticklebacks ( Gasterosteus aculeatus species complex). Previous work demonstrated that colour differences among species correlate to differences in the ambient light prevalent in their mating habitat. Red fish are found in clear water and black fish in red-shifted habitats. We used a paternal half-sib split-clutch design to investigate the genetic and environmental basis of nuptial colour. We found genetic differences between a red and a black stickleback population in the expression of both red and black nuptial colour. In addition, the light environment influenced colour expression, and genotype by environment interactions were also present. We found evidence for both phenotypic and genetic correlations between our colour traits; some of these correlations are in opposite directions for our red and black populations. These results suggest that both genetic change and phenotypic plasticity underlie the correlation of male colour with light environment.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 663–673.