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.     

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.     

Fecundity of the three-spined stickleback, Gasterosteus aculeatus (L.)

The number of eggs spawned by female three-spined sticklebacks Gasterosteus aculeatus (L.) was highly correlated with the size of the fish expressed either as total length or as weight after spawning. There were no significant correlations between the size of the eggs measured either as wet weight per egg or as dry weight per egg, and the size of the fish. Nor were there significant correlations between the calorific value of the eggs and the length or weight of the fish. Regressions relating egg production to the length and the weight of the fish are given. These results and an analysis of previous studies on the fecundity of the stickleback suggest that variations in fecundity are primarily a reflection of variation in the size of the fish at maturity, and that this size is related to the race of the stickleback and to environmental conditions such as food supply which influence the growth of sticklebacks.     

A three-spined stickleback, Gasterosteus aculeatus L. from the North Atlantic

An unusual occurrence of a three-spined stickleback, Gasterosteus aculeatus , is described from Ocean Weather Station India in the North-east Atlantic. Previous records of G. aculeatus caught well offshore are summarised and reasons for these occurrences are suggested. Mention is made of the possibility of sticklebacks breeding in the open ocean.     

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.     

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.     

Comparative study of the olfactory epithelium of the three-spined stickleback (Gasterosteus aculeatus) and the nine-spined stickleback (Pungitius pungitius)

Summary The olfactory epithelium of the three-spined stickleback (Gasterosteus aculeatus) and the nine-spined stickleback (Pungitius pungitius) has been studied with a conventional histochemical and a novel immunological staining technique. In both species, the sensory epithelium is arranged in folds separated by non-sensory epithelial tissue. In the nine-spined stickleback, intrinsic folds consisting of non-sensory cells are found in the apical part of the sensory epithelium where they divide the surface of the sensory epithelium into small islets. These non-sensory cells are non-ciliated, flattened and piled on top of each other; they contain numerous electron-translucent vesicles. The intrinsic folds are absent from the sensory epithelium of the three-spined stickleback. In both species, axons of receptor cells form a layer of fibers in the sensory epithelium immediately above the basal cells. In the three-spined stickleback, thick branches of the olfactory nerve are frequently found in this layer. These branches are only occasionally observed in the sensory epithelium of the nine-spined stickleback. Thus, the three-spined stickleback and the nine-spined stickleback show considerable differences in the organization of the sensory regions of the olfactory epithelium.     

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.     

Mitochondrial DNA phylogeography of the three-spined stickleback (Gasterosteus aculeatus) in Europe-evidence for multiple glacial refugia

An analysis of mitochondrial DNA sequence variation in 172 three-spined sticklebacks (Gasterosteus aculeatus) sampled across the European distribution range revealed three major evolutionary lineages occupying relatively large and separate geographic areas. The trans-Atlantic lineage comprised of populations spanning from the East Coast of USA to the continental Europe and was basal group to the other European lineages in the phylogeny. The European lineage included populations located in the Western and Eastern Europe, British Isles, Scandinavia as well as some parts of the Mediterranean region. The third lineage was specific to the Black Sea drainages. The within lineage structure was characterized by significant excess of low frequency haplotypes and star-like mtDNA genealogies, which suggest a recent population expansions to the formerly glaciated marine and freshwater environments. A coalescent-based method dated the splits between the major lineages to have occurred during the Saalian and Weichselian glaciations in the late Pleistocene, depending on the molecular clock calibration. The coalescent simulations further indicate high degree of genetic diversity within the lineages and a substantial increase in the genetic diversity in the European lineage relative to the ancestral level. In addition to the three major lineages, the freshwater populations in R. Neretva and L. Skadar in the Adriatic Sea coast region harboured unique and highly divergent haplotypes suggesting long independent histories of these populations. Evidence from mtDNA analyses suggests that these populations deserve a status of an evolutionary significant unit.     

LHRH-immunoreactive cells in the brain of the three-spined stickleback,Gasterosteus aculeatus L. (Gasterosteidae)

Summary Cells immunoreactive with an anti-LHRH serum were visualized in the brain of the three-spined stickleback, Gasterosteus aculeatus, by means of the PAP technique. Positive cells were found in a periventricular position in the nucleus praeopticus pars magnocellularis, the nucleus dorsomedialis thalami, the nucleus ventromedialis thalami, the nucleus periventricularis posterior, and in the periventricular dorsomedian tegmentum. These cells were frequently observed to contact the CSF.     

Female mate choice and male red coloration in a natural three-spined stickleback (Gasterosteus aculeatus) population

Under laboratory conditions, female three-spined sticklebacks(Gasterosteus aculeatus L.) show a mating preference for intenselyred-colored males. We verified this female choice in the fieldby observing a freshwater stickleback population in its naturalhabitat. During the egg collection phase, individual courtingmales were localized with the aid of a dummy of a ripe female,caught and photographed under standardized conditions, and released.After males had stopped collecting eggs, we counted the numberof eggs in the nests. The more intense a male's red breedingcoloration, the more eggs he received. Simultaneous female choiceexperiments in the laboratory suggested that ripe females ofthis population preferred redder males. Breeding activitiesof the males in the field were clustered and seem to be synchronizedwithin clusters. At one of the breeding sites, more intensered males were in better physical condition, but this was notthe case at another site. Although several synchronized breedingcycles were observed, the majority of males seem to completeonly one breeding cycle.     

Shyness and boldness differences across contexts in juvenile three-spined stickleback Gasterosteus aculeatus from an anadromous population

To examine if a behavioural syndrome is present in juvenile three-spined stickleback Gasterosteus aculeatus from anadromous populations, individuals were repeatedly exposed to a variety of conditions to assess behavioural consistency and determine if a shyness-boldness syndrome occurred. The degree of exploration in a novel environment was positively correlated with boldness in all other test conditions. Activity level in all contexts, foraging, predator inspection and shoaling were found to be repeatable while other behaviours such as latency to respond appeared more plastic. Both similarities and differences were found for behavioural correlations within and across contexts when compared to prior studies on freshwater populations of G. aculeatus. This suggests that selection pressures may vary across ontogeny and environments.     

Calcium and salinity as selective factors in plate morph evolution of the three-spined stickleback (Gasterosteus aculeatus)

Identifying the causal factors underlying natural selection remains a key challenge in evolutionary biology. Although the genetic basis for the plate morph evolution of three-spined stickleback (Gasterosteus aculeatus) is well described, the environmental variables that form the basis for different morphs are not understood. We measured the effects of dissolved calcium and salinity on the growth of sticklebacks with different plate morphs from Scotland and Poland. There was a significant interaction of calcium with plate morph for fish from both regions, with complete morph sticklebacks growing more slowly at low calcium concentrations and low morph sticklebacks showing divergent responses to calcium concentration. A Scottish anadromous population showed evidence of local adaptation to high salinity, which was independent of plate morph. Polish and Scottish populations diverged in their response to salinity, suggesting a difference in osmotic regulation. The results implicate a role for calcium in selecting for plate morph evolution in sticklebacks, possibly as a limiting element in skeletal growth.     

Identifying footprints of directional and balancing selection in marine and freshwater three-spined stickleback (Gasterosteus aculeatus) populations

Natural selection is expected to leave an imprint on the neutral polymorphisms at the adjacent genomic regions of a selected gene. While directional selection tends to reduce within-population genetic diversity and increase among-population differentiation, the reverse is expected under balancing selection. To identify targets of natural selection in the three-spined stickleback ( Gasterosteus aculeatus ) genome, 103 microsatellite and two indel markers including expressed sequence tags (EST) and quantitative trait loci (QTL)-associated loci, were genotyped in four freshwater and three marine populations. The results indicated that a high proportion of loci (14.7%) might be affected by balancing selection and a lower proportion (2.8%) by directional selection. The strongest signatures of directional selection were detected in a microsatellite locus and two indel markers located in the intronic regions of the Eda-gene coding for the number of lateral plates. Yet, other microsatellite loci previously found to be informative in QTL-mapping studies revealed no signatures of selection. Two novel microsatellite loci ( Stn12 and Stn90 ) located in chromosomes I and VIII, respectively, showed signals of directional selection and might be linked to genomic regions containing gene(s) important for adaptive divergence. Although the coverage of the total genomic content was relatively low, the predominance of balancing selection signals is in agreement with the contention that balancing, rather than directional selection is the predominant mode of selection in the wild.     

Induction of diploid gynogenesis in an evolutionary model organism, the three-spined stickleback (Gasterosteus aculeatus)

Background

X-linked alpha thalassemia, mental retardation syndrome in humans is a rare recessive disorder caused by mutations in the ATRX gene. The disease is characterised by severe mental retardation, mild alpha-thalassemia, microcephaly, short stature, facial, skeletal, genital and gonadal abnormalities.

Results

We examined the expression of ATRX and ATRY during early development and gonadogenesis in two distantly related mammals: the tammar wallaby (a marsupial) and the mouse (a eutherian). This is the first examination of ATRX and ATRY in the developing mammalian gonad and fetus. ATRX and ATRY were strongly expressed in the developing male and female gonad respectively, of both species. In testes, ATRY expression was detected in the Sertoli cells, germ cells and some interstitial cells. In the developing ovaries, ATRX was initially restricted to the germ cells, but was present in the granulosa cells of mature ovaries from the primary follicle stage onwards and in the corpus luteum. ATRX mRNA expression was also examined outside the gonad in both mouse and tammar wallaby whole embryos. ATRX was detected in the developing limbs, craniofacial elements, neural tissues, tail and phallus. These sites correspond with developmental deficiencies displayed by ATR-X patients.

Conclusions

There is a complex expression pattern throughout development in both mammals, consistent with many of the observed ATR-X syndrome phenotypes in humans. The distribution of ATRX mRNA and protein in the gonads was highly conserved between the tammar and the mouse. The expression profile within the germ cells and somatic cells strikingly overlaps with that of DMRT1, suggesting a possible link between these two genes in gonadal development. Taken together, these data suggest that ATRX has a critical and conserved role in normal development of the testis and ovary in both the somatic and germ cells, and that its broad roles in early mammalian development and gonadal function have remained unchanged for over 148 million years of mammalian evolution.