The aberrant stickleback Gasterosteus aculeatus in the Karlskrona archipelago, SE Sweden

The aberrant stickleback in the Karlskrona archipelago is probably a completely new form within the three‐spined stickleback Gasterosteus aculeatus complex. Males of this type differ from sympatric, normal stickleback males by being smaller and by having less striking nuptial coloration. They also build nests in algae above the bottom, whereas normal stickleback males build their nest at the bottom. Moreover, observations suggest that aberrant stickleback males have emancipated from most of the care of nest and offspring as they appear to transport fertilized eggs from the nest to the surroundings where they are left unattended. Whether this can be explained by sex‐specific reproductive strategies or by any other means is investigated. Preliminary results suggest the aberrant stickleback to be genetically distinct from regular morphs. The project will investigate this further and hopefully clarify whether the aberrant type has evolved in the Karlskrona archipelago, thus probably in sympatry with normal sticklebacks, or if it is of allopatric origin. With reproductively important morphological and behavioural deviations, our first guess would be that isolation is mediated through sexual selection. If this is true, isolation may have been relatively rapid making a sympatric origin less unlikely. The aberrant form is very rare and endangered. Presently, it is only found at two sites, both of which are threatened by an impending ferry terminal construction. A major aim of the project is to help preserve the aberrant stickleback. Most importantly, aberrants will be collected for captive breeding and introduction to new localities.     

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.     

Occurrence of Schistocephalus solidus in anadromous threespine stickleback

Plerocercoids of the cestode Schistocephalus solidus are reported for the first time from the body cavity of anadromous threespine stickleback inhabiting Mud Lake, Alaska. Most infected stickleback harbored a single large plerocerciod (mean weight = 0.447 g, range = 0.228-0.716 g). The overall prevalence of plerocercoids across genders and 2 yr of samples was 1.4%, but prevalence was significantly greater in males than in females. Because of the large size of the plerocercoids, anadromous stickleback were probably infected as juveniles before leaving the lake, suggesting that plerocercoids can live in the body cavity of oceanic stickleback for several years.     

Heterospecific aggression and adaptive divergence in brook stickleback (Culaea inconstans)

Agonistic behavior between heterospecifics, in which individuals of one species attack another, may cause a subordinate species to shift resource or habitat use. Subsequent evolutionary responses to selection may mimic shifts expected under ecological character displacement, but with no role played by exploitative competition. Alternatively, aggressive behavior can evolve when fitness is improved by excluding members of a coexisting species from a defendable resource through interference. We tested whether heterospecific agonistic behavior has evolved in brook stickleback (Culaea inconstans) by comparing replicate allopatric populations to those sympatric with ninespine stickleback (Pungitius pungitius). We also tested for heritable variation in heterospecific aggressive behavior by rearing family groups in a common environment. Allopatric populations of brook stickleback were more aggressive than ninespine stickleback, suggesting that pre-existing aggression in brook stickleback contributed to niche shifts by ninespine stickleback. In addition, sympatric adult brook stickleback were more aggressive toward ninespine stickleback than brook stickleback from allopatric populations. Overt heterospecific aggressive behaviors were heritable, and aggression in juvenile brook stickleback increased with age in sympatric but not in allopatric populations reared in a common environment. Brook stickleback have evolved increased aggression when they coexist with ninespine stickleback. These stickleback communities have been structured by both evolved and pre-existing variation in heterospecific aggressive behavior in brook stickleback.     

Intraguild predation drives evolutionary niche shift in threespine stickleback

Intraguild predation--competition and predation by the same antagonist--is widespread, but its evolutionary consequences are unknown. Intraguild prey may evolve antipredator defenses, superior competitive ability on shared resources, or the ability to use an alternative resource, any of which may alter the structure of the food web. We tested for evolutionary responses by threespine stickleback to a benthic intraguild predator, prickly sculpin. We used a comparative morphometric analysis to show that stickleback sympatric with sculpin are more armored and have more limnetic-like body shapes than allopatric stickleback. To test the ecological implications of this shift, we conducted a mesocosm experiment that varied sculpin presence and stickleback population of origin (from one sympatric and one allopatric lake). Predation by sculpin greatly increased the mortality of allopatric stickleback. In contrast, sculpin presence did not affect the mortality of sympatric stickleback, although they did have lower growth rates suggesting increased nonpredatory effects of sculpin. Consistent with their morphology, sympatric stickleback included more pelagic prey in their diets, leading to depletion of zooplankton in the mesocosms. These findings suggest that intraguild prey evolution has altered food web structure by reducing both predation by the intraguild predator and diet overlap between species.     

Adaptation and constraint in a stickleback radiation

The evolution of threespine sticklebacks in freshwater lakes constitutes a well‐studied example of a phenotypic radiation that has produced numerous instances of parallel evolution, but the exact selective agents that drive these changes are not yet fully understood. We present a comparative study across 74 freshwater populations of threespine stickleback in Norway to test whether evolutionary changes in stickleback morphology are consistent with adaptations to physical parameters such as lake depth, lake area, lake perimeter and shoreline complexity, variables thought to reflect different habitats and feeding niches. Only weak indications of adaptation were found. Instead, populations seem to have diversified in phenotypic directions consistent with allometric scaling relationships. This indicates that evolutionary constraints may have played a role in structuring phenotypic variation across freshwater populations of stickleback. We also tested whether the number of lateral plates evolved in response to lake calcium levels, but found no evidence for this hypothesis.     

Diversification and adaptive evolution of putative sweet taste receptors in threespine stickleback

The threespine stickleback Gasterosteus aculeatus is known to include several morphologically and ecologically divergent forms. Its phenotypic traits related to feeding vary among forms, and are considered to be a result of adaptations to various environments to find foods effectively. To examine whether the diversification of feeding modes in the stickleback involves genetic changes of the sense of taste, taste receptor family 1 (T1R) genes in stickleback were analyzed and compared with those in other model fishes. Ten T1R genes and 2 pseudogenes were identified from the stickleback genomic sequences. In particular, putative sweet taste receptors (T1R2s) highly increased in number in stickleback (8 genes and 2 pseudogenes) compared to other fishes (2-3 genes). Maximum likelihood estimations of nonsynonymous-synonymous nucleotide substitution rate have indicated that stickleback T1R2 are under positive selection. Expression analysis by RT-PCR revealed that most stickleback T1R genes were expressed in the taste organs; however, at least two T1R2 genes were not expressed in the taste organs, suggesting that the expression levels of these T1R2 genes may be fluctuated through the life history. In addition, sequencing analysis showed that several T1R2 genes in an anadromous form stickleback individual collected from the western Pacific (Japan) were substantially different from those in genomic data derived from a freshwater form individual collected in North America. This suggested that intra-specific variations of stickleback T1R2 genes were considerably large. Our results imply that, in stickleback, T1R2s have diversified through adaptation to various environments, probably to perceive substances important for its survival and reproduction.     

Life-history plasticity in female threespine stickleback

The postglacial adaptive radiation of the threespine stickleback fish (Gasterosteus aculeatus) has been widely used to investigate the roles of both adaptive evolution and plasticity in behavioral and morphological divergence from the ancestral condition represented by present-day oceanic stickleback. These phenotypes tend to exhibit high levels of ecotypic differentiation. Population divergence in life history has also been well studied, but in contrast to behavior and morphology, the extent and importance of plasticity has been much less well studied. In this review, we summarize what is known about life-history plasticity in female threespine stickleback, considering four traits intimately associated with reproductive output: age/size at maturation, level of reproductive effort, egg size and clutch size. We envision life-history plasticity in an iterative, ontogenetic framework, in which females may express plasticity repeatedly across each of several time frames. We contrast the results of laboratory and field studies because, for most traits, these approaches give somewhat different answers. We provide ideas on what the cues might be for observed plasticity in each trait and, when possible, we inquire about the relative costs and benefits to expressed plasticity. We end with an example of how we think plasticity may play out in stickleback life history given what we know of plasticity in the ancestor.     

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.     

Isolation between sympatric anadromous and resident threespine stickleback species in Mud Lake,Alaska

A sympatric pair of anadromous and resident freshwater threespine stickleback species (Gasterosteus aculeatus species complex) occurs in Mud Lake in the Matanuska-Susitna Valley, Alaska. The two forms differ in an array of morphological traits, including traits associated with predator defense (e.g., spine lengths) and trophic ecology (e.g., number of gill rakers). Mud Lake is only the third lake reported to have anadromous stickleback (which have a complete row of lateral plates) coexisting with low-plated resident stickleback in the absence of intermediate partially plated fish. Microhabitat and seasonal isolation appear to contribute to reproductive isolation between the two forms.     

Intraguild predation leads to genetically based character shifts in the threespine stickleback

Intraguild predation is a common ecological interaction that occurs when a species preys upon another species with which it competes. The interaction is potentially a mechanism of divergence between intraguild prey (IG‐prey) populations, but it is unknown if cases of character shifts in IG‐prey are an environmental or evolutionary response. We investigated the genetic basis and inducibility of character shifts in threespine stickleback from lakes with and without prickly sculpin, a benthic intraguild predator (IG‐predator). Wild populations of stickleback sympatric with sculpin repeatedly show greater defensive armor and water column height preference. We laboratory‐raised stickleback from lakes with and without sculpin, as well as marine stickleback, and found that differences between populations in armor, body shape, and behavior persisted in a common garden. Within the common garden, we raised stickleback half‐families from multiple populations in the presence and absence of sculpin. Although the presence of sculpin induced trait changes in the marine stickleback, we did not observe an induced response in the freshwater stickleback. Behavioral and morphological trait differences between freshwater populations thus have a genetic basis and suggest an evolutionary response to intraguild predation.     

Genetic divergence in morphology-performance mapping between Misty Lake and inlet stickleback

Different environments should select for different aspects of organismal performance, which should lead to correlated divergence in morphological traits that influence performance. The result should be genetic divergence in aspects of performance, morphology and associations ('maps') between morphology and performance. Testing this hypothesis requires quantifying performance and morphology in multiple populations after controlling for environmental differences, but this is rarely attempted. We used a common-garden experiment to examine morphology and several aspects of swimming performance within and between the lake and inlet populations of threespine stickleback (Gasterosteus aculeatus) from the Misty system, Vancouver Island, Canada. Controlling for body size, lake stickleback had shallower bodies, larger caudal fins and smaller pelvic girdles. With or without morphological covariates, lake stickleback showed greater performance in both sustained and burst swimming. In contrast, inlet stickleback showed greater manoeuverability than did lake stickleback in some analyses. Morphology-performance relationships were decoupled when considering variation within vs. between populations. Moreover, morphology-performance mapping differed between the two populations. Based on these observations, we advance a hypothesis for why populations adapting to different environments should show adaptive genetic divergence in morphology-performance mapping.     

Parallel evolution? Microsatellite variation of recently isolated marine and freshwater three-spined stickleback

Variation at nine microsatellite loci, four of which are linked to phenotypic traits (spine length and lateral plate morphology) in Canadian three-spined stickleback Gasterosteus aculeatus , are used to test for selection on marine and freshwater three-spined stickleback morphs in Iceland. There are indications of strong selection on loci linked to dorsal spine length, providing another potential example of parallel divergence at the genomic level in three-spined stickleback.     

Studies of threespine stickleback developmental evolution: progress and promise

A promising route for understanding the origin and diversification of organismal form is through studies at the intersection of evolution and development (evo-devo). While much has been learned over the last two decades concerning macroevolutionary patterns of developmental change, a fundamental gap in the evo-devo synthesis is the integration of mathematical population and quantitative genetics with studies of how genetic variation in natural populations affects developmental processes. This micro-evo-devo synthesis requires model organisms with which to ask empirical questions. Threespine stickleback fish (Gasterosteus aculeatus), long a model for studying behavior, ecology and evolution, is emerging as a prominent model micro-evo-devo system. Research on stickleback over the last decade has begun to address the genetic basis of morphological variation and sex determination, and much of this work has important implications for understanding the genetics of speciation. In this paper we review recent threespine stickleback micro-evo-devo results, and outline the resources that have been developed to make this synthesis possible. The prospects for stickleback research to speed the micro-(and macro-) evo-devo syntheses are great, and this workhorse model system is well situated to continue contributing to our understanding of the generation of diversity in organismal form for many more decades.     

A comparative analysis of experimental selection on the stickleback pelvis

Mechanisms of natural selection can be identified using experimental approaches. However, such experiments often yield nonsignificant effects and imprecise estimates of selection due to low power and small sample sizes. Combining results from multiple experimental studies might produce an aggregate estimate of selection that is more revealing than individual studies. For example, bony pelvic armour varies conspicuously among stickleback populations, and predation by vertebrate and insect predators has been hypothesized to be the main driver of this variation. Yet experimental selection studies testing these hypotheses frequently fail to find a significant effect. We experimentally manipulated length of threespine stickleback (Gasterosteus aculeatus) pelvic spines in a mesocosm experiment to test whether prickly sculpin (Cottus asper), an intraguild predator of stickleback, favours longer spines. The probability of survival was greater for stickleback with unclipped pelvic spines, but this effect was noisy and not significant. We used meta‐analysis to combine the results of our mesocosm experiment with previously published experimental studies of selection on pelvic armour. We found evidence that fish predation indeed favours increased pelvic armour, with a moderate effect size. The same approach found little evidence that insect predation favours reduced pelvic armour. The causes of reduced pelvic armour in many stickleback populations remain uncertain.     

Life cycle and structure of populations of three-spined stickleback <Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis> (Fam. Gasterosteidae) in rivers of northwestern Kamchatka (with reference to the Utkholok River)

From the end of May to mid-August 2005 and 2006, the dynamics of migrations and spawning, as well as specific features of development, growth, and feeding migration of the three-spined stickleback Gasterosteus aculeatus in the salmon river Utkholok of the mountain-tundra type were studied. Morphological characteristics, age, fecundity, dates of reproduction and spawning biotopes, structure of spawning groups, and specific features of feeding were investigated. On the basis of the obtained data, it was concluded that the riverine and migratory forms of three-spined sticklebacks from the Utkholok River belong to a single population. Biological specific features of spawners with high (2005) and low (2006) numbers of the migratory form were compared. For comparison, we also used our own data on the morphology and biological analysis of the migratory three-spined stickleback from the Kol River salmon of the mountain type.     

Phenotypic divergence among threespine stickleback that differ in nuptial coloration

By studying systems in their earliest stages of differentiation, we can learn about the evolutionary forces acting within and among populations and how those forces could contribute to reproductive isolation. Such an understanding would help us to better discern and predict how selection leads to the maintenance of multiple morphs within a species, rather than speciation. The postglacial adaptive radiation of the threespine stickleback (Gasterosteus aculeatus) is one of the best‐studied cases of evolutionary diversification and rapid, repeated speciation. Following deglaciation, marine stickleback have continually invaded freshwater habitats across the northern hemisphere and established resident populations that diverged innumerable times from their oceanic ancestors. Independent freshwater colonization events have yielded broadly parallel patterns of morphological differences in freshwater and marine stickleback. However, there is also much phenotypic diversity within and among freshwater populations. We studied a lesser‐known freshwater “species pair” found in southwest Washington, where male stickleback in numerous locations have lost the ancestral red sexual signal and instead develop black nuptial coloration. We measured phenotypic variation in a suite of traits across sites where red and black stickleback do not overlap in distribution and at one site where they historically co‐occurred. We found substantial phenotypic divergence between red and black morphs in noncolor traits including shape and lateral plating, and additionally find evidence that supports the hypothesis of sensory drive as the mechanism responsible for the evolutionary switch in color from red to black. A newly described third “mixed” morph in Connor Creek, Washington, differs in head shape and size from the red and black morphs, and we suggest that their characteristics are most consistent with hybridization between anadromous and freshwater stickleback. These results lay the foundation for future investigation of the underlying genetic basis of this phenotypic divergence as well as the evolutionary processes that may drive, maintain, or limit divergence among morphs.     

Evolutionary diversification of opercle shape in Cook Inlet threespine stickleback

We investigated the evolution of a large facial bone, the opercle (OP), in lake populations of the threespine stickleback that were founded by anadromous ancestors, in Cook Inlet, Alaska. Recent studies characterized OP variation among marine and lake populations and mapped a quantitative trait locus with a large influence on OP shape. Using populations from diverse environments and independent evolutionary histories, we examined divergence of OP shape from that of the anadromous ancestor. We report preliminary evidence for divergence between benthic and generalist lake ecotypes, necessitating further investigation. Furthermore, rapid divergence of OP shape has occurred in a lake population that was founded by anadromous stickleback in the 1980s, which is consistent with divergence of other phenotypic traits and with OP diversification in other lake populations. By contrast, there has been limited evolution of OP shape in a second lake population that may have experienced a genetic bottleneck early in its history and lacks genetic variation for OP divergence. Taken together, the results obtained from these two populations are consistent with studies of other stickleback phenotypic traits that implicate ancestral variation in postglacial adaptive radiation of threespine stickleback in fresh water.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 832–844.     

A meso-predator release of stickleback promotes recruitment of macroalgae in the Baltic Sea

In the Baltic Sea, increased populations of the three-spined stickleback are invading the coastal zone in summer, following declines in large predatory fish such as cod, pike, and perch. Here, we explore the consequences of such a meso-predator release on a near-natural scale, by manipulating stickleback densities in four large 600 m² enclosures: two ‘removal’ and two ‘addition’ enclosures. Higher densities of stickleback resulted in a three times higher recruitment of ephemeral green macroalgae. At the same time we found higher abundances of the dominating invertebrate grazers with lower stickleback densities: higher numbers of both amphipods and smaller gastropods were found in one stickleback ‘removal’ enclosure and higher numbers of large gastropods occurred in the other ‘removal’ enclosure. Grazer abundances also depended on the macrophyte species that dominated the enclosures. Nutrient enrichment had no statistically significant effect on algal recruitment, although the mean number of algal recruits was almost doubled under enriched conditions. Our results indicate that a meso-predator release of stickleback may dramatically shift coastal food web constitution towards increased abundances of ephemeral macroalgae through a trophic cascade.