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.     

The inter-spawning interval of the female Three-spined stickleback, Gasterosteus aculeatus

Female Three-spined sticklebacks spawn several times in a breeding season, at intervals of a few days. The changes that take place in females during the interval between successive spawnings were analysed. The average time between spawnings was 87.5 hours. Between spawnings females increased in weight by between 15 and 30%. The bulk of this weight increase was lost when the eggs were spawned. The increase in weight was because of an increase in weight of the ovaries, which showed an increase in both dry matter and water content. After spawning the ovaries formed 8 to 9% of the total body weight, and this increased to up to 24% just prior to the next spawning. The ovaries were maximally hydrated immediately after spawning. There were no significant changes in the calorific value of the ovaries, but the calorific value of the rest of the body was a minimum just after spawning. It was estimated that between spawnings females were making a net gain of energy at an average rate of 2 cal/hour. After spawning, courtship behaviour by the females waned, but recovered over the last half of the interval between spawnings. The inter-spawning interval of the Three-spined stickleback provides a useful situation in which physiological and nutritional aspects of reproduction in a teleost fish can be studied.     

Spawning patterns in the three-spined stickleback (Gasterosteus aculeatus L.): an evaluation by DNA fingerprinting

We analysed a random sample of 10 three-spined stickleback nests by DNA fingerprinting. DNA from the guardian male and a random subsample of LO fry per nest were probed with pYNZ 132, a human single-locus probe for VNTR-loci (variable number of tandem repeats). On average this probe produced DNA fingerprints of 12 scoreable bands. By comparing the bands present in each individual, we calculated band sharing indices (BSIs) between the guardian male and its fry. The BSls varied between 0.40 and 0.77 with an average (± S.D.) of 0.59 ± 0.09. We therefore conclude that the guardian male was the true father of the fry in all these nests. Once the paternal bands in each fry were determined, we compared the maternal bands among the fry of each nest. Based on the BSIs obtained with these comparisons, we found that one guardian male enticed three females to spawn in its nest, six enticed two females and three enticed one female.     

Effect of spawning number and ration on reproductive performance of the batch-spawning three-spined stickleback Gasterosteus aculeatus

An experiment quantified the effect of food ration and spawning number on the breeding season reproductive performance of batch-spawning, female three-spined sticklebacks Gasterosteus aculeatus . Individually housed females were maintained on fixed rations of 2, 4, 8 or 16% of their initial postspawning mass of live enchytraeid worms from immediately after their first spawning until they ceased spawning. Number of spawnings correlated positively with ration. Total breeding season reproductive investment (total wet mass of eggs produced as a percentage of initial postspawning female mass) ranged from 38% at the 2% ration to 147% at the 16% ration. At the lower rations, postspawning mass, batch fecundity and wet and dry masses of the batch declined over successive spawnings, with the rate of decline inversely related to ration. At the highest ration, there was no decline in batch fecundity and postspawning mass increased over successive spawnings. Mean reproductive investment per inter-spawning interval was higher at the highest ration, but at all rations declined over successive spawnings. Mean reproductive effort per inter-spawning interval (wet mass of eggs spawned as a percentage of the wet mass of food consumed over the inter-spawning interval) was inversely related to ration. At the higher rations, reproductive effort showed no trend over successive spawnings. Neither spawning number nor ration had a systematic effect on egg diameter, wet mass per egg, dry mass per egg or total lipid content of the eggs. If the rate of food intake was insufficient, although batch fecundity declined, the main adjustment was a reduction in the number of spawnings in the breeding season.     

Divergence in reproductive ecology of the three-spined stickleback,Gasterosteus aculeatus

An anadromous population (trachurus form) and three freshwater populations (leiurus form) of the three-spined stickleback,Gasterosteus aculeatus, in central Japan were compared with one another in the reproductive traits: body length at maturity, egg size, clutch size, the swell of abdomen and the number of eggs per nest. The anadromous fish which become larger in body size at maturity spawn eggs smaller in size and greater in number than the freshwater fish. The abdomen swell of gravid females expressed by the proportion of abdomen width to body length was greater in the freshwater fish. The anadromous male fish collected a mean of 2,638 eggs with a range of 1,119 to 4,052 eggs from about 6–7 females. In the three freshwater (the Yamayoke, the Tsuya and the Jizo) populations, males must have mated with about 9–22, 7–18 and 4–7 females respectively. It seems that theleiurus form increases its reproductive success by its much more mating opportunities and the parental efforts of nesting males as well as by spawning large eggs. Furthermore, among the freshwater populations, the Jizo one inhabiting the upper stream was clearly larger in body size, in egg size and in clutch size than the Yamayoke and the Tsuya ones which inhabit stable waterbodies with springs. It is possible that the Jizo population adopted the strategy of spawning a few large eggs as an adaptation to its habitat. The causal and functional explanations in reproductive characteristics among the four populations are discussed in regard to differences in the environmental conditions.     

A temperature-dependent growth model for the three-spined stickleback Gasterosteus aculeatus

Specific growth rates of individually reared juvenile three-spined sticklebacks Gasterosteus aculeatus were investigated under laboratory conditions to parameterize a complete temperature-dependent growth model for this species. To test the applicability of experimentally derived optima in growth response rates to natural conditions, the effects of commercial pellets and natural prey on growth rates were investigated. In addition, to test for seasonal effects on growth, laboratory trials were performed in both spring and winter. Growth took place from 5 to 29° C with a temperature for optimum growth reaching a sharp peak at 21° C. Modelled optimal temperature for maximum growth was estimated to be 21.7° C and lower and upper temperatures for growth were estimated to be 3.6 and 30.7° C, respectively. There were no significant differences in growth rates between fish reared on invertebrates or commercial pellets. Seasonal effects on growth were pronounced, with reduced growth rates in the winter despite similar laboratory conditions. On average, 60% higher growth rates were achieved at the optimum temperature in summer compared to the winter. The strong seasonality in the growth patterns of G. aculeatus indicated here reduces the applicability of the model derived in this study to spring and summer conditions.     

Variation in female life-history traits among Alaskan populations of the threespine stickleback, Gasterosteus aculeatus L. (Pisces: Gasterosteidae)

Life-history characteristics of female threespine stickleback (Gasterosteus aculeatus) were examined in 12 populations, 11 freshwater and one anadromous, within the Cook Inlet region of Alaska. Because this area has been deglaciated during the last 20 000 years, the freshwater populations are recently derived, probably independendy, from the local marine or anadromous stickleback. Freshwater threespine stickleback have undergone considerable morphological evolution within this region, apparently in response to environmental factors including predatory regimes and environmental productivity. Our freshwater study populations were selected to sample this range of morphological variation in order to determine whether life-history traits and morphologies have followed similar evolutionary trajectories. Freshwater populations could be categorized generally into one of three ecomorphotypes: those inhabiting relatively productive lakes having one or more piscivorous fishes present, and in which the stickleback exhibit a fully developed pelvic girdle; those inhabiting low-calcium lakes that lack piscivorous fishes, and in which the pelvic structures are incomplete; those living in streams with piscivorous fishes, in which the stickleback have fully developed pelvic girdles. The anadromous population constituted a fourth ecomorphotype that lives in marine waters, and is robusdy armored. The freshwater populations showed considerable variation in all life-history traits assessed, and this variation generally corresponded to our ecomorphological classifications. Nevertheless, within each ecomorphotype there was sufficient variation to suggest that morphological and life-history traits may not always respond in the same manner in response to the same selective regime.     

Phenotypic integration of life history and morphology: an example from three-spined stickleback, Gasterosteus aculeatus L.

Although typically life history and morphology are studied separately, they may evolve most often in concert. Therefore, a full understanding of the evolution of fish life-history patterns may require exploration of the evolutionary interplay between components of life history and other aspects of phenotype. One of the most promising approaches to understanding phenotypic integration is population comparison. This approach is particularly effective when ancestralderived relationships are understood and when multiple populations can be inferred to have evolved derived character states independently. Here we provide an example of this approach using five allopatric populations of freshwater three-spined stickleback ( Gasterosteus aculcatus L.) that have diverged in response to differences in selection regimes among the lakes they inhabit. We demonstrate a relationship between one aspect of reproductive life history, clutch volume and relative body shape. The differences are consistent with those predicted on the basis of differences in trophic habit and overall body form. Finally, we discuss the value of particular groups of fish for use in comparative studies and explore the kinds of evolutionary issues that can be addressed through population comparison.     

Inheritance of vertebral number in the three-spined stickleback (Gasterosteus aculeatus)

Intraspecific variation in the number of vertebrae is taxonomically widespread, and both genetic and environmental factors are known to contribute to this variation. However, the relative importance of genetic versus environmental influences on variation in vertebral number has seldom been investigated with study designs that minimize bias due to non-additive genetic and maternal influences. We used a paternal half-sib design and animal model analysis to estimate heritability and causal components of variance in vertebral number in three-spined sticklebacks (Gasterosteus aculeatus). We found that both the number of vertebrae (h² = 0.36) and body size (h² = 0.42) were moderately heritable, whereas the influence of maternal effects was estimated to be negligible. While the number of vertebrae had a positive effect on body size, no evidence for a genetic correlation between body size and vertebral number was detected. However, there was a significant positive environmental correlation between these two traits. Our results support the generalization-in accordance with results from a review of heritability estimates for vertebral number in fish, reptiles and mammals-that the number of vertebrae appears to be moderately to highly heritable in a wide array of species. In the case of the three-spined stickleback, independent evolution of body size and number of vertebrae should be possible given the low genetic correlation between the two traits.     

Ultraviolet light and visual behaviour in the three-spined stickleback, Gasterosteus aculeatus

The ability of various vertebrates to perceive visual information in the ultraviolet region of the electromagnetic spectrum (300-400 nm) is receiving increasing interest. To date, many of these studies have concentrated on the role of ultraviolet perception in mate choice, yet there are several ways in which the ability to perceive ultraviolet information may affect other behaviours. Until now, it has been widely assumed that colour in the three-spined stickleback can be quantified by methods appropriate to the human visual system. However, evidence does exist that suggests that, in some populations, sticklebacks are capable of perceiving ultraviolet wavelengths. Using a behavioural technique, we tested the ability of the stickleback to perceive ultraviolet light under full-spectrum conditions to establish whether such wavelengths are utilised within their normal behavioural repertoire. We tested this ability by assessing whether subjects could locate hidden food in a foraging task where food position was indicated by the position of landmarks. These landmarks differed only in their ultraviolet content, appearing identical when viewed across the human visible region of the spectrum. We found that sticklebacks were able to use ultraviolet perception to locate a foraging patch under full-spectrum conditions.     

Reduction of sexual dimorphism in stream-resident forms of three-spined stickleback Gasterosteus aculeatus

Sexual dimorphism in geometric body shape and external morphology was compared between marine and stream-resident forms of three-spined stickleback Gasterosteus aculeatus collected from North America and Japan. Some aspects of sexual dimorphism were shared between ecotypes: males had larger heads than females with no significant effect of ecotype on the magnitude of sexual dimorphism. By contrast, a significant sex-by-ecotype interaction was found for body depth. Males tended to have deeper bodies than females in both forms, but the magnitude of sexual dimorphism was reduced in stream-resident forms. Although females were generally larger in standard length and had larger pelvic girdles, significant sexual dimorphism in these traits was not consistently found across populations or ecotypes. These results suggest that some aspects of sexual dimorphism were shared between ecotypes, while others were unique to each population. The results further suggest that ecology may influence the evolution of sexual dimorphism in some external morphological traits, such as body depth.     

The pineal complex of the three-spined stickleback,Gasterosteus aculeatus L.

Summary The pineal complex of the three-spined stickleback (Gasterosteus aculeatus L.) was investigated by light and electron microscopy, as well as fluorescence histochemistry for demonstration of catecholamines and indolamines. The pineal complex of the stickleback consists of a pineal organ and a small parapineal organ situated on the left side of the pineal stalk. The pineal organ, including the entire stalk, is comprised mainly of ependymal-type interstitial cells and photoreceptor cells with well-developed outer segments. Both unmyelinated and myelinated nerve fibres are present in the pineal organ. Nerve tracts from the stalk enter the habenular and posterior commissures. A small bundle of nerve fibres connects the parapineal organ and the left habenular body. The presence of indolamines (5-HTP, 5-HT) was demonstrated in cell bodies of both the pineal body and the pineal stalk, and catecholaminergic nerve fibres surround the pineal complex.     

Dyadic relationships in nesting males of the three-spined stickleback, Gasterosteus aculeatus

Multidimensional scaling analysis of nest site location, nesting interval, and aggressive and mating interactions revealed that male three-spined sticklebacks, Gasterosteus aculeatus, formed nesting clusters comprising five patterns of dyadic relationships. These patterns were defined by intervening variables such as size difference between the two males, nest site locations, synchronization of nesting cycles (egg presence in the nest), distance between two nests, and nest raiding behaviours. Several patterns of dyadic relationships were integrated among nesting males and their constellations indicated an expression of the social structure. Through an understanding the social structure, I described effects of social context or situations on individual reproductive success.     

Cost of egg production in the three-spined stickleback (Gasterosteus aculeatus L.)

In the interval between successive spawnings, female sticklebacks consumed approximately their own wet weight of Tubifex. On average, for 100 cal of food consumed, 26 cal of eggs, 3 cal of somatic growth and 11 cal of faeces were produced. In the absence of somatic growth, the efficiency of egg production was estimated as nearly 30%, and it was predicted that in the absence of egg production, the efficiency of somatic growth would range from 20% for a fish of 0.8 g wet weight to 3% for 2 g fish.
The weight of eggs produced at a spawning was a function of the weight of the female but not of the amount of food consumed. If food consumption was not sufficient to cover the cost of egg production, the fish lost weight. Total production (the summation of egg production and somatic growth) was a function of the amount of food consumed.     

Genetic evidence for male-biased dispersal in the three-spined stickleback (Gasterosteus aculeatus)

Sex-biased dispersal is capable of generating population structure in nonisolated populations and may affect adaptation processes when selective conditions differ among populations. Intrasexual competition for local resources and/or mating opportunities predicts a male-biased dispersal in polygynous species and a female bias in monogamous species. The patterns of sex-biased dispersal in birds and mammals are well explained by their respective mating systems, but the picture emerging from fish studies is still mixed. Using neutral genetic markers, we investigated whether there is any evidence for sex-biased dispersal among Baltic Sea populations of the three-spined stickleback ( Gasterosteus aculeatus ). The null hypothesis of non sex-biased dispersal was rejected in favour of male-biased dispersal in this species. As the three-spined stickleback has a polygynous mating system, the observed male bias in dispersal is consistent with the hypothesis that local mate competition might drive the observed pattern. Although more research both on the proximate and ultimate causes behind the observed pattern is needed, our results serve as a first step towards understanding patterns of sex-biased dispersal in this species.     

Detecting Holocene divergence in the anadromous-freshwater three-spined stickleback (Gasterosteus aculeatus) system

The anadromous-freshwater three-spined stickleback (Gasterosteus aculeatus) system allows for inferring the role of adaptation in speciation with a high level of accuracy because the freshwater ecotype has evolved multiple times from a uniform anadromous ancestor. A cause for concern is that independent evolution among drainages is not guaranteed in areas with a poorly resolved glacial history. This is the case for the west European great rivers, whose downstream valleys flanked the southern limit of the late Pleistocene ice sheet. We tested for independent and postglacial colonization of these valleys hypothesizing that the relationships among anadromous and freshwater sticklebacks correspond to a raceme structure. We compared the reduction in plate number accompanying this colonization to the genetic differentiation using 13 allozyme and five microsatellite loci in 350 individuals. Overall microsatellite differentiation (F(ST) = 0.147) was twice as large as allozyme differentiation (F(ST) = 0.066). Although habitat-specific gene flow may mask the ancestral relationships among both ecotypes, levels of microsatellite differentiation supported the hypothesis of raceme-like divergence, reflecting independent colonizations rather than the presence of two distinct evolutionary clades. Under an infinite alleles model and in the absence of gene flow, the observed freshwater divergence might be reached after 440 (microsatellites) to 4500 (allozymes) generations. Hence, the anadromous-freshwater stickleback system most likely diverged postglacially. We conclude that the reduction in plate number in two freshwater basins probably occurred independently, and that its considerable variation among populations is not in agreement with the time since divergence.     

Phylogeography of isolated freshwater three-spined stickleback Gasterosteus aculeatus populations in the Adriatic Sea basin

Analyses of mitochondrial (mt) DNA and microsatellite variation were carried out to examine the relationships between 10 freshwater populations of three-spined sticklebacks Gasterosteus aculeatus along the eastern coast of the Adriatic Sea. Partial sequences of the mtDNA control region and cytochrome b gene, in addition to 15 microsatellite loci, were used to analyse populations from four isolated river catchments. Results uncovered an Adriatic lineage that was clearly divergent from the European lineage, and confirmed that the most divergent and ancient populations are located within the Adriatic lineage as compared with other European populations. Two northern Adriatic populations formed independent clades within the European mitochondrial lineage, suggesting different colonization histories of the different Adriatic populations. Nuclear marker analyses also indicated deep divergence between Adriatic and European populations, albeit with some discordance between the mtDNA phylogeny of the northern Adriatic populations, further highlighting the strong differentiation among the Adriatic populations. The southern populations within the Adriatic lineage were further organized into distinct clades corresponding to respective river catchments and sub-clades corresponding to river tributaries, reflecting a high degree of population structuring within a small geographic region, concurrent with suggestions of existence of several microrefugia within the Balkan Peninsula. The highly divergent clades and haplotypes unique to the southern Adriatic populations further suggest, in accordance with an earlier, more limited survey, that southern Adriatic populations represent an important reservoir for ancient genetic diversity of G. aculeatus.     

Studies on the toxicity of cadmium to the three-spined stickleback Gasterosteus aculeatus L.

Cadmium was found to be lethal to sticklebacks at all concentrations from 100.0 to 0.001 mg Cd 1^–1, in water of 103–111 mg 1^–1 hardness as CaCO₃. The pattern of mortality as shown by the time-concentration curve suggests that toxicity is not due to a single mechanism but changes with concentration. Fish were found to accumulate cadmium, the whole body levels increasing from 0.90 μg/g fresh weight at 0.001 mg Cd 1^–1 exposure concentration to 51.0 μg/g at 100 mg Cd 1^–1. The concentration factor was shown to decrease with increasing exposure concentration from 0.51 at 100 mg Cd 1^–1 to 511 at 0.001 mg Cd 1^–1. The plerocercoid parasite Schistocephalus solidus in the host's perivisceral cavity contained less cadmium than the tissues of its host.     

Daily growth increments in the otoliths of the three-spined stickleback, Gasterosteus aculeatus L.

Daily increment formation was demonstrated in the sagittae of the three-spined stickleback, Gasterosieus aculeatus L., under both laboratory and field conditions. The onset of daily increment formation coincided with the day of hatching. The main sources of inaccuracy in age determination resulted from difficulties in resolving narrow increments in the sagittae of fish held at low temperatures and the increasing incidence of checks with age. The advantage of daily increments for investigating growth in this species was demonstrated from a comparison between increment-derived age-at-length data and length-at-capture data, since the latter significantly under-estimated early growth rate within a population.