Effect of salinity on nest building behaviour in the nine-spined stickleback Pungitius sinensis

The authors evaluated the adaptability of male nine-spined sticklebacks (Pungitius sinensis) at three salinity levels (0, 5 and 10 psu) by comparing nest building success rates with nest structures. Successful nest building decreased as salinity increased. In addition, nests built in fresh water (i.e., 0 psu) were glued together, whereas those built in brackish water (5 and 10 psu) broke easily and fell from the nest site to the gravel bottom. Based on these findings, the authors suggest that P. sinensis adapts to freshwater environments.     

Parasites of the nine-spined stickleback Pungitius pungitius (L)

Eleven species of parasite are reported from the nine-spined stickleback Pungitius pungitius (L). Nine of these, namely, Trichodina domerguei, T. tenuidens, Vorticella sp., Epistylis?, Diplostomum spathaceum, Cryptocotyle lingua, Proteocephalus filicollis, Schistocephalus solidus and glochidia of Anodonta cygnea, are new host records for Great Britain. Gyrodactylus spp. and Thersitina gasterostei were also found.     

Predation mediated population divergence in complex behaviour of nine‐spined stickleback (Pungitius pungitius)

The proximate and ultimate explanations for behavioural syndromes (correlated behaviours – a population trait) are poorly understood, and the evolution of behavioural types (configuration of behaviours – an individual trait) has been rarely studied. We investigated population divergence in behavioural syndromes and types using individually reared, completely predator‐ or conspecific‐naïve adult nine‐spined sticklebacks (Pungitius pungitius) from two marine and two predatory fish free, isolated pond populations. We found little evidence for the existence of behavioural syndromes, but population divergence in behavioural types was profound: individuals from ponds were quicker in feeding, bolder and more aggressive than individuals from marine environments. Our data reject the hypothesis that behavioural syndromes exist as a result of genetic correlations between behavioural traits, and support the contention that different behavioural types can be predominant in populations differing in predation pressure, most probably as a result of repeated independent evolution of separate behavioural traits.     

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.     

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.     

Development of the lateral line system in the sea bass

Using light and electron microscopy, a study of the development of the lateral line system of the sea bass Dicentrarchus labrax , from embryo to adult, revealed that the first free neuromasts appeared on the head shortly before hatching and multiplied during the larval stage. They were aligned on the head and trunk in a pattern which corresponded to the location of future canals. The transition to the juvenile stage marked the start of important anatomical changes during which head and trunk canals were formed successively. Neuromasts, with a cupula and consisting of standard sensory cells and supporting cells, were characterized by bidirectional polarity. The exact location of the first neuromast formed in the embryo was identified and its differentiation monitored from primordium to eruption. This neuromast was distinguishable from the others by its radial polarity. Correlations were made between the development of the lateral line system and the behaviour of the sea bass.     

Migrations of three-spined stickleback, nine-spined stickleback, and pond smelt in the Chignik catchment, Alaska

Upstream spawning migrations of age-2 three-spined stickleback, nine-spined stickleback, and pond smelt, and subsequent downstream migrations of young-of-the-year and age-1 individuals are documented in Black River of the Chignik catchment, Alaska.     

Habitat-dependent and -independent plastic responses to social environment in the nine-spined stickleback (Pungitius pungitius) brain

The influence of environmental complexity on brain development has been demonstrated in a number of taxa, but the potential influence of social environment on neural architecture remains largely unexplored. We investigated experimentally the influence of social environment on the development of different brain parts in geographically and genetically isolated and ecologically divergent populations of nine-spined sticklebacks (Pungitius pungitius). Fish from two marine and two pond populations were reared in the laboratory from eggs to adulthood either individually or in groups. Group-reared pond fish developed relatively smaller brains than those reared individually, but no such difference was found in marine fish. Group-reared fish from both pond and marine populations developed larger tecta optica and smaller bulbi olfactorii than individually reared fish. The fact that the social environment effect on brain size differed between marine and pond origin fish is in agreement with the previous research, showing that pond fish pay a high developmental cost from grouping while marine fish do not. Our results demonstrate that social environment has strong effects on the development of the stickleback brain, and on the brain''s sensory neural centres in particular. The potential adaptive significance of the observed brain-size plasticity is discussed.     

Morphological and genetic divergence in Swedish postglacial stickleback (Pungitius pungitius) populations

Background

An important objective of evolutionary biology is to understand the processes that govern phenotypic variation in natural populations. We assessed patterns of morphological and genetic divergence among coastal and inland lake populations of nine-spined stickleback in northern Sweden. Coastal populations are either from the Baltic coast (n = 5) or from nearby coastal lakes (n = 3) that became isolated from the Baltic Sea (< 100 years before present, ybp). Inland populations are from freshwater lakes that became isolated from the Baltic approximately 10,000 ybp; either single species lakes without predators (n = 5), or lakes with a recent history of predation (n = 5) from stocking of salmonid predators (~50 ybp).

Results

Coastal populations showed little variation in 11 morphological traits and had longer spines per unit of body length than inland populations. Inland populations were larger, on average, and showed greater morphological variation than coastal populations. A principal component analysis (PCA) across all populations revealed two major morphological axes related to spine length (PC1, 47.7% variation) and body size (PC2, 32.9% variation). Analysis of PCA scores showed marked similarity in coastal (Baltic coast and coastal lake) populations. PCA scores indicate that inland populations with predators have higher within-group variance in spine length and lower within-group variance in body size than inland populations without predators. Estimates of within-group P _ST (a proxy for Q _ST) from PCA scores are similar to estimates of F _ST for coastal lake populations but P _ST > F _ST for Baltic coast populations. P _ST > F _ST for PC1 and PC2 for inland predator and inland no predator populations, with the exception that P _ST < F _ST for body size in inland populations lacking predators.

Conclusions

Baltic coast and coastal lake populations show little morphological and genetic variation within and between groups suggesting that these populations experience similar ecological conditions and that time since isolation of coastal lakes has been insufficient to demonstrate divergent morphology in coastal lake populations. Inland populations, on the other hand, showed much greater morphological and genetic variation characteristic of long periods of isolation. Inland populations from lakes without predators generally have larger body size, and smaller spine length relative to body size, suggesting systematic reduction in spine length. In contrast, inland populations with predators exhibit a wider range of spine lengths relative to body size suggesting that this trait is responding to local predation pressure differently among these populations. Taken together the results suggest that predation plays a role in shaping morphological variation among isolated inland populations. However, we cannot rule out that a causal relationship between predation versus other genetic and environmental influences on phenotypic variation not measured in this study exists, and this warrants further investigation.     

Lactate dehydrogenase isozymes and allozymes of the nine-spined stickleback Pungitius pungitius (L.) (Osteichthyes: Gasterosteidae)

Zymograms indicate the existence of three loci coding for lactate dehydrogenase in the nine-spined stickleback Pungitius pungitius. The skeletal muscle locus is polymorphic for two codominant alleles: Ldh-A(100). and Ldh-A(140). Differences in allele frequencies among nine samples, obtained from eight geographically isolated populations, proved not significant in 28/36 pairwise comparisons. The frequency of Ldh-A(100) varied from 0.426 to 0.715. Significant differences in apparent Km (pyruvate) values were found among the LDH-A allozymes suggesting a functional basis for the selective maintenance of this polymorphism.     

Quantitative genetics of body size and timing of maturation in two nine-spined stickleback (Pungitius pungitius) populations

Due to its influence on body size, timing of maturation is an important life-history trait in ectotherms with indeterminate growth. Comparison of patterns of growth and maturation within and between two populations (giant vs. normal sized) of nine-spined sticklebacks (Pungitius pungitius) in a breeding experiment revealed that the difference in mean adult body size between the populations is caused by differences in timing of maturation, and not by differential growth rates. The fish in small-sized population matured earlier than those from large-sized population, and maturation was accompanied by a reduction in growth rate in the small-sized population. Males matured earlier and at smaller size than females, and the fish that were immature at the end of the experiment were larger than those that had already matured. Throughout the experimental period, body size in both populations was heritable (h² = 0.10–0.64), as was the timing of maturation in the small-sized population (h² = 0.13–0.16). There was a significant positive genetic correlation between body size and timing of maturation at 140 DAH, but not earlier (at 80 or 110 DAH). Comparison of observed body size divergence between the populations revealed that Q _ST exceeded F _ST at older ages, indicating adaptive basis for the observed divergence. Hence, the results suggest that the body size differences within and between populations reflect heritable genetic differences in the timing of maturation, and that the observed body size divergence is adaptive.     

Baiting improves CPUE in nine‐spined stickleback (Pungitius pungitius) minnow trap fishery

Whether or not baiting influences stickleback catch per unit effort (CPUE) remains a matter of debate among stickleback researchers: While the opinions about the impact of baiting on CPUE differ, supporting quantitative data are scarce. The effect of baiting and trap type on nine‐spined stickleback (Pungitius pungitius) CPUE was studied in a field experiment conducted over four consecutive days in a small pond in northeastern Finland. The results show that baited traps yielded better (mean CPUE = 1.24 fish/trap/d) catches than unbaited traps (mean CPUE = 0.66); however, there were also differences in CPUE depending on the type of collapsible trap that was used. The trap type effect on CPUE seemed to differ among age classes – the finer meshed trap caught more young‐of‐the‐year fish than the coarse‐meshed one, whereas the opposite was true for the older and larger individuals. The results agree with those of an earlier more restricted study conducted in the same locality: Together, these results provide strong evidence for the positive impact of baiting on nine‐spined stickleback CPUE.     

History vs. habitat type: explaining the genetic structure of European nine‐spined stickleback (Pungitius pungitius) populations

The genetic structure of contemporary populations can be shaped by both their history and current ecological conditions. We assessed the relative importance of postglacial colonization history and habitat type in the patterns and degree of genetic diversity and differentiation in northern European nine‐spined sticklebacks (Pungitius pungitius), using mitochondrial DNA (mtDNA) sequences and 12 nuclear microsatellite and insertion/deletion loci. The mtDNA analyses identified – and microsatellite analyses supported – the existence of two historically distinct lineages (eastern and western). The analyses of nuclear loci among 51 European sites revealed clear historically influenced and to minor degree habitat dependent, patterns of genetic diversity and differentiation. While the effect of habitat type on the levels of genetic variation (coastal > freshwater) and differentiation (freshwater > coastal) was clear, the levels of genetic variability and differentiation in the freshwater sites were independent of habitat type (viz. river, lake and pond). However, levels of genetic variability, together with estimates of historical effective population sizes, decreased dramatically and linearly with increasing latitude. These geographical patterns of genetic variability and differentiation suggest that the contemporary genetic structure of freshwater nine‐spined sticklebacks has been strongly impacted by the founder events associated with postglacial colonization and less by current ecological conditions (cf. habitat type). In general, the results highlight the strong and persistent effects of postglacial colonization history on genetic structuring of northern European fauna and provide an unparalleled example of latitudinal trends in levels of genetic diversity.     

Morphological divergence of North‐European nine‐spined sticklebacks (Pungitius pungitius): signatures of parallel evolution

Parallel evolution is characterised by repeated, independent occurrences of similar phenotypes in a given habitat type, in different parts of the species distribution area. We studied body shape and body armour divergence between five marine, four lake, and ten pond populations of nine‐spined sticklebacks [Pungitius pungitius (Linnaeus, 1758)] in Fennoscandia. We hypothesized that marine and lake populations (large water bodies, diverse fish fauna) would be similar, whereas sticklebacks in isolated ponds (small water bodies, simple fish fauna) would be divergent. We found that pond fish had deeper bodies, shorter caudal peduncles, and less body armour (viz. shorter/absent pelvic spines, reduced/absent pelvic girdle, and reduced number of lateral plates) than marine fish. Lake fish were intermediate, but more similar to marine than to pond fish. Results of our common garden experiment concurred with these patterns, suggesting a genetic basis for the observed divergence. We also found large variation among populations within habitat types, indicating that environmental variables other than those related to gross habitat characteristics might also influence nine‐spined stickleback morphology. Apart from suggesting parallel evolution of morphological characteristics of nine‐spined sticklebacks in different habitats, the results also show a number of similarities to the evolution of three‐spined stickleback (Gasterosteus aculeatus Linnaeus, 1758) morphology. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 403–416.     

Morphology of the mechanosensory lateral line system in the Atlantic Stingray,Dasyatissabina: The mechanotactile hypothesis

The biological function of anatomical specializations in the mechanosensory lateral line of elasmobranch fishes is essentially unknown. The gross and histological features of the lateral line in the Atlantic stingray, Dasyatis sabina, were examined with special reference to its role in the localization and capture of natural invertebrate prey. Superficial neuromasts are arranged in bilateral rows near the dorsal midline from the spiracle to the posterior body disk and in a lateral position along the entire length of the tail. All dorsal lateral line canals are pored, contain sensory neuromasts, and have accessory lateral tubules that most likely function to increase their receptive field. The pored ventral canal system consists of the lateral hyomandibular canal along the disk margin and the short, separate mandibular canal on the lower jaw. The extensive nonpored and relatively compliant ventral infraorbital, supraorbital, and medial hyomandibular canals form a continuous complex on the snout, around the mouth, and along the abdomen. Vesicles of Savi are small mechanosensory subdermal pouches that occur in bilateral rows only along the ventral midline of the rostrum. Superficial neuromasts are best positioned to detect water movements along the transverse body axis such as those produced by tidal currents, conspecifics, or predators. The pored dorsal canal system is positioned to detect water movements created by conspecifics, predators, or possibly distortions in the flow field during swimming. Based upon the stingray lateral line morphology and feeding behavior, we propose the Mechanotactile Hypothesis, which states that the ventral nonpored canals and vesicles of Savi function as specialized tactile mechanoreceptors that facilitate the detection and capture of small benthic invertebrate prey. J. Morphol. 238:1–22, 1998. © 1998 Wiley-Liss, Inc.     

The origin of pituitary cysts in the rostral pars distalis of the nine-spined stickleback,Pungitius pungitius L.

Summary Pituitary cysts in the nine-spined stickleback, Pungitius pungitius L., develop next to blood vessels passing through the prolactin zone of the rostral pars distalis to the connective tissue capsule at its periphery. Cysts were most frequent when pituitaries were large compared with body lengths. However, the incidence of cysts could not be closely related to body length alone. As the rostral pars distalis is more highly vascularised in fish with large pituitaries, and as there was no evidence of accumulating secretion around these blood vessels, it is suggested that cysts develop when vascular demands (or supplies) become excessive. Associated with the greater vascularity of the rostral pars distalis in large pituitaries was a remarkable development of non-granulated cells. Indeed cysts may originate as enlarged intercellular spaces between such cells, as the latter often surround blood vessels. The non-granulated cells are also important in enlarging cyst cavities (by phagocytosing prolactin-cell debris) and perhaps for maintaining their structural integrity. It is suggested that the macrophages within cyst cavities are derived from the non-granulated cells.     

Fine scale genetic population structure of the freshwater and Omono types of nine-spined stickleback Pungitius pungitius (L.) within the Omono River system, Japan

The fine scale geographic population structure of two types of nine-spined stickleback Pungitius pungitius (the widely distributed freshwater type and a local endemic, the Omono type) within the Omono River system, Japan, was investigated. A principal components analysis of allele frequencies and neighbour-joining tree for pair-wise F _ST values, based on 10 allozyme loci, revealed that the Omono type was comprised of four regional groups with relatively high genetic divergence. This grouping was also supported by hierarchical analysis of molecular variance (AMOVA) with a higher variance component among the regional groups, and by an exact test with significant genotypic differentiation for all sample pairs among the regional groups. Moreover, in the clustering of individuals using the Bayesian method, most of individuals in each regional group were assigned the corresponding cluster. On the other hand, there were less pronounced regional groups of the freshwater type, although AMOVA, exact test for genotypic differentiation and Bayesian analysis indicated genetic divergence between two sampling sites in lower reach of the Omono River and other sites. The results suggest that the Omono type represented an earlier colonization, with subsequent invasion of the freshwater type.     

Phylogeography of ninespine sticklebacks (Pungitius pungitius) in North America: glacial refugia and the origins of adaptive traits

The current geographical distribution of the ninespine stickleback (Pungitius pungitius) was shaped in large part by the glaciation events of the Pleistocene epoch (2.6 Mya–10 Kya). Previous efforts to elucidate the phylogeographical history of the ninespine stickleback in North America have focused on a limited set of morphological traits, some of which are likely subject to widespread convergent evolution, thereby potentially obscuring relationships among populations. In this study, we used genetic information from both mitochondrial DNA (mtDNA) sequences and nuclear microsatellite markers to determine the phylogenetic relationships among ninespine stickleback populations. We found that ninespine sticklebacks in North America probably dispersed from at least three glacial refugia—the Mississippi, Bering, and Atlantic refugia—not two as previously thought. However, by applying a molecular clock to our mtDNA data, we found that these three groups diverged long before the most recent glacial period. Our new phylogeny serves as a critical framework for examining the evolution of derived traits in this species, including adaptive phenotypes that evolved multiple times in different lineages. In particular, we inferred that loss of the pelvic (hind fin) skeleton probably evolved independently in populations descended from each of the three putative North American refugia.     

Organization and physiology of posterior lateral line afferent neurons in larval zebrafish

The lateral line system of larval zebrafish can translate hydrodynamic signals from the environment to guide body movements. Here, I demonstrate a spatial relationship between the organization of afferent neurons in the lateral line ganglion and the innervation of neuromasts along the body. I developed a whole cell patch clamp recording technique to show that afferents innervate multiple direction-sensitive neuromasts, which are sensitive to low fluid velocities. This work lays the foundation to integrate sensory neuroscience and the hydrodynamics of locomotion in a model genetic system.