Migratory history of the threespine stickleback Gasterosteus aculeatus

 The migratory history of two highly divergent forms (the Japan Sea and Pacific Ocean forms) of the threespine stickleback Gasterosteus aculeatus collected from Japanese brackish water (seawater) and freshwater was studied by examining strontium (Sr) and calcium (Ca) concentrations in their otoliths using wavelength dispersive X-ray spectrometry on an electron microprobe. The Sr : Ca ratios in the otoliths changed with salinity of the habitat. The otolith Sr : Ca ratios of the freshwater resident-type samples of the Pacific Ocean form showed consistently low Sr : Ca ratios, averaging 0.85–0.96 × 10⁻³ from the core to the edge. In contrast, the otolith Sr : Ca ratios of the anadromous type of both the Japan Sea and Pacific Ocean forms fluctuated strongly along the life history transects in accordance with their migration patterns from seawater to freshwater. The higher ratios in the anadromous type, averaging 5.4 × 10⁻³, in the otolith region from the core to 200 μm, corresponded to the seagoing period, suggesting that otolith Sr : Ca ratios are affected by ambient water salinity. These findings clearly indicate that otolith Sr : Ca ratios reflect individual life histories, and that these two highly divergent forms of stickleback have a flexible migration strategy. Received: May 23, 2002 / Revised: July 29, 2002 / Accepted: August 19, 2002 Acknowledgments We are grateful to Dr. S. Mori of Gifu Keizai University, and Miss M. Yamada and Messrs. M. Kume and T. Kitamura of Hokkaido University, for their assistance in sampling. This work was supported in part by Grant-in-Aid No. 13760138 from the Ministry of Education, Culture, Sports, Science and Technology, Japan. Correspondence to:Takaomi Arai     

Armor morphology and reproductive output in threespine stickleback,Gasterosteus aculeatus

Synopsis The threespine stickleback, Gasterosteus aculeatus, is an extensively armored fish inhabiting both marine and fresh waters across its holarctic distribution. Marine fish nearly always possess a full complement of bony lateral plates running from just behind the head to the tail, and a robust pelvic girdle complex. These armor features appear to constrain lateral and ventral abdominal distention, and therefore clutch volume. Freshwater populations in many areas exhibit variable reduction in lateral plate number, and in some regions the pelvic girdle is also reduced or lost. Freshwater populations also vary in the degree of abdominal distention exhibited by gravid females. We tested whether reduction in armoring might be correlated with increased clutch volume using five populations from the Cook Inlet area of Alaska. The hypothesis that populations having reduced pelvic girdle complexes would have greater size-adjusted clutch volumes was not supported. In fact, our two full-pelvic populations as a group had larger volumes. Similarly, size-adjusted clutch volumes were not related to pelvic phenotype within either of our two pelvic-reduced populations, nor to lateral plate morph within a fifth population. Other factors that may explain the interpopulation differences in clutch volume in threespine stickleback include body shape, food quantity and quality, intensity of predation, and even behavior. Except for a preliminary analysis of body shape, these possibilities remain unexplored. The concept of phenotypic integration suggests that these factors should be analyzed as a suite rather than individually.     

Heritability of DNA methylation in threespine stickleback (Gasterosteus aculeatus)

Epigenetic mechanisms underlying phenotypic change are hypothesized to contribute to population persistence and adaptation in the face of environmental change. To date, few studies have explored the heritability of intergenerationally stable methylation levels in natural populations, and little is known about the relative contribution of cis- and trans-regulatory changes to methylation variation. Here, we explore the heritability of DNA methylation, and conduct methylation quantitative trait loci (meQTLs) analysis to investigate the genetic architecture underlying methylation variation between marine and freshwater ecotypes of threespine stickleback (Gasterosteus aculeatus). We quantitatively measured genome-wide DNA methylation in fin tissue using reduced representation bisulfite sequencing of F1 and F2 crosses, and their marine and freshwater source populations. We identified cytosines (CpG sites) that exhibited stable methylation levels across generations. We found that additive genetic variance explained an average of 24–35% of the methylation variance, with a number of CpG sites possibly autonomous from genetic control. We also detected both cis- and trans-meQTLs, with only trans-meQTLs overlapping with previously identified genomic regions of high differentiation between marine and freshwater ecotypes. Finally, we identified the genetic architecture underlying two key CpG sites that were differentially methylated between ecotypes. These findings demonstrate a potential role for DNA methylation in facilitating adaptation to divergent environments and improve our understanding of the heritable basis of population epigenomic variation.     

Morphological segregation of Icelandic threespine stickleback (Gasterosteus aculeatus L).

Icelandic threespine sticklebacks show parallel sympatric morphological differences related to different substrate habitats in four Icelandic lakes. The level of morphological diversification varies among the lakes, ranging from a population with a wide morphological distribution to a population with clear resource morphs, where morphological diversification was reflected in diet differences. These differences in morphological divergence are closely related to the differences in the ecological surroundings of each population. This appears to be resource polymorphism, which may lead to population differentiation and speciation. Trophically related sexual dimorphism was also common in these sticklebacks, which is possibly the result of sexual selection or habitat segregation by the sexes. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 247–257.     

Genetic basis of sexual dimorphism in the threespine stickleback Gasterosteus aculeatus

Sexual dimorphism (SD) in morphological, behavioural and physiological features is common, but the genetics of SD in the wild has seldom been studied in detail. We investigated the genetic basis of SD in morphological traits of threespine stickleback (Gasterosteus aculeatus) by conducting a large breeding experiment with fish from an ancestral marine population that acts as a source of morphological variation. We also examined the patterns of SD in a set of 38 wild populations from different habitats to investigate the relationship between the genetic architecture of SD of the marine ancestral population in relation to variation within and among natural populations. The results show that genetic architecture in terms of heritabilities, additive genetic variances and covariances (as well as correlations) is very similar in the two sexes in spite of the fact that many of the traits express significant SD. Furthermore, population differences in threespine stickleback body shape and armour SD appear to have evolved despite constraints imposed by genetic architecture. This implies that constraints for the evolution of SD imposed by strong genetic correlations are not as severe and absolute as commonly thought.     

Seasonal changes in carotenoid and lipid storage by threespine stickleback, Gasterosteus aculeatus

Total body astaxanthin and lipid concentrations in threespine stickleback (Gasterosteus aculeatus) collected from fall through the start of the breeding season were correlated; concentrations of each increased between fall and spring and decrease during the pre-breeding season. Individual tissues (skin, muscle, viscera, carcass, and gonads) showed a decrease between the spring and pre-breeding seasons; beta-carotene also decreased in all tissues except the skin, where there was an increase. Unlike previous studies, beta-carotene, but not astaxanthin, was deposited in the skin prior to nesting, suggesting that that beta-carotene is the carotenoid responsible for creating the nuptial signal in this wild population.     

Two morphotypes of lacustrine threespine stickleback,Gasterosteus aculeatus, in Benka Lake, Alaska

Synopsis Within freshwater fishes, a common pattern of diversification of body form and trophic structure has recently been recognized. Two different suites of co-occurring characters appear to allow fish to efficiently forage on either benthic invertebrates or plankton. For threespine stickleback,Gasterosteus aculeatus, these suites of characters have been labeled benthic and limnetic. The forms differ in several morpholoical traits, with the limnetic having a more fusiform shape, larger eyes, longer and more numerous gill rakers, and a smaller more tubular mouth. Benthic and limnetic threespine stickleback are usually found in allopatry or parapatry, and less frequently in sympatry. Within the range of the threespine stickleback, which comprises perhaps tens of thousands of lacustrine populations, the sympatric occurrence of the benthic and limnetic forms has only been established for six lakes within a small region of the Strait of Georgia, British Columbia. We present the first evidence for the presence of sympatric morphotypes of threespine stickleback outside of British Columbia. We examine the nature and extent of this diversification, and present possible explanations for the sympatric occurrence of these morphotypes. We also explore possible reasons for the small number of documented sympatric benthic and limnetic forms of threespine stickleback despite the existence of thousands of apparently suitable lakes.     

Phenotypic plasticity drives a depth gradient in male conspicuousness in threespine stickleback,Gasterosteus aculeatus

Signal evolution is thought to depend on both a signal's detectability or conspicuousness (signal design) as well as any extractable information it may convey to a potential receiver (signal content). While theoretical and empirical work in sexual selection has largely focused on signal content, there has been a steady accrual of evidence that signal design is also important for trait evolution. Despite this, relatively little attention has been paid to spatial variation in the conspicuousness of a given signal, especially over small spatial scales (relative to an organism's dispersal distance). Here, we show that visual signals of male threespine stickleback vary in conspicuousness, depending on a male's nest depth within a given lake. Deeper nesting males were typically more chromatically conspicuous than shallow nesting males. This trend is partly because all male stickleback are more conspicuous in deep optical environments. However, deep males are even more conspicuous than environmentally driven null expectations, while shallow males tend to be disproportionally cryptic. Experimental manipulation of male nesting depth induced plastic changes in nuptial color that replicated the natural gradients in conspicuousness. We discuss a number of potential mechanisms that could produce depth gradients in conspicuousness in male stickleback, including concomitant depth gradients in diet, predation pressure, male/female density, female preference, and opportunity for sexual selection.     

Evolutionary interplay between ecology,morphology and reproductive behavior in threespine stickleback,Gasterosteus aculeatus

Synopsis Throughout its range, freshwater populations in the Gasterosteus aculeatus species complex display remarkable differentiation of morphology and behavior, much of which reflects differences in ecological conditions among habitats. We first describe the ecological conditions that have led to morphological and behavioral divergence in two common lake types in British Columbia, Canada. Deep, oligotrophic lakes have favored the evolution of slender fish well adapted for feeding on plankton (limnetic, sensu McPhail 1984), whereas shallow, more eutrophic lakes with extensive littoral zones favor fish that are deeper-bodied and well adapted for feeding on benthic invertebrates. The latter forage in large groups that attack nests guarded by males and cannibalize the young within. Courtship in these lakes is relatively inconspicuous, a feature that apparently enhances nest survivorship. In limnetic populations, this form of cannibalism is usually absent and courtship is conspicuous. Because benthic populations tend to have larger bodies and hence, larger gapes than do limnetic fish we suggest that cannibalism may be facilitated by large body size or a correlated trait. We test this by comparing the morphology of populations exhibiting both group cannibalism and a second kind of cannibalism in which solitary females court males, gain access to nests as a consequence, and then cannibalize eggs without spawning. Our results suggest that differences in body size cannot explain variation among populations in cannibalistic tendencies but that body size may affect the effectiveness of cannibalism by females within populations.     

A new model of lateral plate morph inheritance in the threespine stickleback,Gasterosteus aculeatus

The threespine stickleback,Gasterosteus aculeatus, is polymorphic for the arrangement of lateral bony plates. It is confirmed in this paper that four morphs (not three) should be distinguished in this species: low plated, low plated with a keel, partially plated and completely plated. A new model is proposed to explain the inheritance of these morphs which involves one major gene with three alleles displaying a dominance hierarchy withA (completely plated) dominant toa (low plated) which is dominant toa _k (low plated with keel). The dominance of theA allele is modified to semidominance by a dominant alleleC at a second locus. This scheme explains all the results of relevant breeding experiments published so far. Field data also fulfill predictions derived from this model.     

Family origin and the response of threespine stickleback, Gasterosteus aculeatus, to thermal acclimation

To establish whether family origin affects the response of the threespine stickleback (Gasterosteus aculeatus) to thermal acclimation, we examined the rates of feeding, growth, and food conversion, relative tissue and organ masses and activities of a mitochondrial and a glycolytic enzyme in pectoral and axial muscle of individually housed fish from six families during acclimation to 8 degrees C and 23 degrees C. Feeding rates differed among families but were consistently higher in warm-acclimated than cold-acclimated fish. Growth rates differed among families. In four families growth was greater at 8 degrees C; these families generally had higher conversion efficiencies at 8 degrees C than 23 degrees C. For two families, growth was greater at 23 degrees C than 8 degrees C and conversion efficiencies did not differ between 8 degrees C and 23 degrees C. Relative tissue and organ masses (percent axial muscle, hepatosomatic, gut and kidney indices) differed with gender and among families (hepatosomatic, gut and kidney indices) but little with acclimation status. In all families and in both muscles, activities of the mitochondrial enzyme, citrate synthase (CS), were increased by cold acclimation. Axial muscle levels of the glycolytic enzyme, lactate dehydrogenase (LDH), were not affected by thermal acclimation or family origin, but were strongly correlated with the hepatosomatic index and axial muscle protein content. Pectoral muscle levels of LDH were affected by family origin which also influenced the response to thermal acclimation. Similar patterns were observed for specific activities and total muscle contents of these enzymes. Stickleback family origin influenced rates of feeding and growth and the thermal sensitivity of growth rates but not the compensatory increase in muscle CS levels with cold acclimation. The differing thermal sensitivities of growth could reflect distinct strategies for the timing of juvenile growth.     

Male aggression and female mate choice in the threespine stickleback,Gasterosteus aculeatus L.*

A laboratory study of female G. aculeatus revealed no conclusive evidence of active female mate choice on the basis of male aggression levels. However, highly aggressive males failed in 95% of all choice tests. The less aggressive ‘chosen’ males were generally successful again in subsequent trials with the same female, and certain males were consistently successful with different females. Females exhibited an increased readiness to spawn at the end of the reproductive season, although the same males were usually selected again.     

Genetics of osteal plate polymorphism and microevolution of threespine stickleback (Gasterosteus aculeatus L.)

Summary The results of genetical studies of osteal plate polymorphism of threespine stickleback Gasterosteus aculeatus reported to date (Munzing 1959; Hagen and Gilbertson 1973; Avise 1976) are discussed and proposed inheritance models are considered. Results of crosses between the morphs of G. aculeatus from the White Sea are presented. An attempt has been made by the author to devise a unifying model for the inheritance of plate morphs within the whole range of G. aculeatus. The role of polymorphism in the microevolutionary processes taking place within this complex species is discussed.     

Genetically isolated sympatric forms of threespine stickleback,Gasterosteus aculeatus,in Lake Azabachije (Kamchatka-peninsula,USSR)

Synopsis Two sympatric morphs of threespine stickleback Gasterosteus aculeatus are found in Lake Azabachije (Kamchatka, USSR); resident low-plated leiurus and completely plated trachurus, migrating from the Bering sea into the Lake to spawn. The absence of the intermediate morph semiarmatus and significant differences in a number of characters are indicative of reproductive isolation. The results show that the leiurus morph is common in the regions other than those with mild climate and small seasonal fluctuations of temperature.     

Intraspecific variation of spectral sensitivity in threespine stickleback (Gasterosteus aculeatus) from different photic regimes

To examine the influence of the spectral characteristics of underwater light on spectral sensitivity of the ON and OFF visual pathways, compound action potential recordings were made from retinal ganglion cells of threespine stickleback from different photic regimes. In fish from a red-shifted photic regime (P₅₀ 680 nm for downwelling light at 1m), peak sensitivity of both the ON and OFF pathways was limited to long wavelength light (_max 600–620). In contrast, the ON pathway of fish from a comparatively blue-shifted (P₅₀ 566 nm) photic regime exhibited sensitivity to medium (_max 540–560) and long (_max 600 nm) wavelengths, while the OFF pathway exhibited peak sensitivity to only medium (_max 540 nm) wavelength light. In a third population, where the the ambient light is moderately red-shifted (P₅₀ 629 nm), the ON pathway once again exhibited only a long wavelength sensitivity peak at 620 nm, while the OFF pathway exhibited sensitivity to both medium (_max 560 nm) and long (_max 600–620 nm) wavelength light. These findings suggest that the photic environment plays an integral role in shaping spectral sensitivity of the ON and OFF pathways.