Colour perception in three-spined sticklebacks: sexes are not so different after all

Sexual selection theory implies a tight coupling between the evolution of male sexual display and the sensory capabilities of the female. In sexually dimorphic species it is proposed that this might lead to sex differences in a species’ perceptive abilities. However, supporting evidence for this is rare, and to date there is only one example; three-spined sticklebacks, Gasterosteus aculeatus. Here, the female’s visual system is reported to become more red-sensitive during the summer breeding season; a time when sexually mature males display a red throat and belly to potential mates. In contrast, a shift in sensitivity is not apparent in males. These results, although commonly quoted, are surprising because previous observations suggest that both sexes may benefit from the detection of the male’s red colour patch; in females the intensity of red coloration can influence the choice of mate, and in males the conspicuous red colouration can aid the detection of rival males. To investigate this paradox we repeated the original optomotor experiment using a fully controlled design. In contrast to the earlier result, we found that both males and females exhibit a shift in their sensitivity to red during the reproductive period. These new data therefore do not support the hypothesis that sex differences in perceptual abilities occur in sexually dimorphic species.     

Food selection in juvenile three-spined sticklebacks studied in relation to size,abundance and biomass of prey

The food selection and diet of juvenile three-spined sticklebacks (Gasterosteus aculeatus L.) was studied in the littoral of a brackish-water sea area. The sampling stations were located in a eutrophicated area, where the plankton was characterized by rotifers, in a noneutrophicated zone, where copepods predominated, and in the intermediate zone, characterized by cladocerans. In all areas the fish preferred microcrustaceans to rotifers, but they did not feed strictly according to the size-selection hypothesis. Nor did they take the most abundant prey species. With some exceptions the species chiefly eaten by and also selected by fish, were those which had the largest biomass in the plankton.     

Variation in the reproductive potential of Schistocephalus infected male sticklebacks is associated with 11-ketotestosterone titre

Parasites can impact host reproduction by interfering with host endocrine systems, but the adaptive nature of such effects is disputed. Schistocephalus solidus plerocercoids are parasites of three-spined sticklebacks Gasterosteus aculeatus that are often associated with impaired host reproduction. Here, we relate reproductive behavior and physiology to levels of the androgen 11-ketotestosterone (11KT) in naturally infected and non-infected male sticklebacks from two UK populations. In one population infected males harbored heavy infections and showed uniformly reduced 11KT titres and kidney spiggin (nesting glue protein) content compared to non-infected fish. However in a second population infection levels were more variable and males with smaller infections recorded 11KT and spiggin titres that overlapped those of non-infected fish; among infected males from this population 11KT and kidney spiggin also both correlated negatively with infection severity. Male reproductive behavior correlated closely with 11KT titre in both populations, and infected males with high 11KT levels exhibited normal reproductive behavior. Our results suggest that Schistocephalus infection per se does not block reproductive development in male sticklebacks, and that some male fish may have the ability to breed whilst infected. Our results are not consistent with the hypothesis that Schistocephalus adaptively castrates male hosts via endocrine disruption; rather they support the hypothesis that reproductive disruption is a side effect of the energetic costs of infection.     

The breeding colouration of male three-spined sticklebacks (Gasterosteus aculeatus) as an indicator of energy investment in vigour

Summary A necessary condition of most models of intersexual selection requires that secondary sexual traits are costly so that cheating is prevented. If the conspicuous breeding colouration of male three-spined sticklebacks (Gasterosteus aculeatus L.) is such a handicap, it must involve costs. I examined the energetic costs of the breeding colouration by varying the energy contents of the daily food supply among five groups of sticklebacks over a 10 week period. The nutritional carotenoid level, i.e. the colour pigment used in the breeding colouration, was constant for all fish. Both the increase of their condition factor and the condition level they finally achieved correlated positively with the food ration of the groups. Individuals whose condition increased during the experiment developed a more intensive red colouration. However, a direct correlation between food quantity and the red breeding colouration reached at the end of the experiment did not exist. Nevertheless, given the limitation of pigment availability, there was still variation in the breeding colouration and the costs for the metabolism of the colouration were sufficient to render it an honest signal: a female stickleback can assess a male's condition and condition change over the past few weeks by the intensity of the colour of his blue eyes (which is not based on carotenoids and whose pigments were therefore not controlled in the food) and his red jaw, respectively. How much an individual male fish invests in increase of length and increase of condition (which correlate negatively with each other) seems to be, at least partly, his own strategic decision, which could have important consequences in the competition for female mates. It is eventually this decision that a male stickleback seems to signal with his red jaw.     

Shoaling behaviour of sticklebacks infected with the microsporidian parasite, <Emphasis Type="Italic">Glugea anomala</Emphasis>

We compared the shoaling behaviour of three-spined sticklebacks, Gasterosteus aculeatus, infected with the microsporidian, Glugea anomala, to that of non-infected conspecifics. Infected fish lost significantly more weight than non-infected fish during a period of food deprivation, suggesting a metabolic cost to parasitism. In binary shoal choice tests, non-infected test fish showed an association preference for a shoal of non-infected over a shoal of infected conspecifics; infected test fish displayed no preference. Infected fish, however, showed a higher overall tendency to shoal than non-parasitised fish. Furthermore, infected fish occupied front positions within a mixed school. We consider the behavioural differences between infected and uninfected fish in the context of their potential benefits to the fish hosts and the parasites.     

Effects of freshwater and marine overwintering environments on life histories of threespine sticklebacks: evidence for adaptive variation between anadromous and resident freshwater populations

Summary Life history theory predicts that migratory fishes should delay reproduction, be larger at first reproduction, and have higher fecundities than nonmigrants. We tested this hypothesis by comparing life histories of anadromous (estuary) and resident freshwater (upstream) threespine sticklebacks (Gasterosteus aculeatus L.) from the Navarro River, California, USA. Using a split-brood, two-environment breeding design, families from cach population were divided and reared in both freshwater and seawater overwintering environments. In both treatments, the more migratory estuary sticklebacks were larger at first reproduction and had large initial clutch sizes; in the freshwater treatment, the estuary sticklebacks matured later than the upstream fish. Population means varied little across treatments, indicating that the average effects of the different overwintering conditions were slight. The responses of individual families to a given overwintering treatment were highly variable in both populations, as reflected in significant family x treatment effects for all traits. Phenotypic correlations among life history traits were significant and positive for most traits, and were similar in magnitude in both populations. Differences in the relative degree of specialization for migration may in part explain variation in life history between these populations.     

Innate versus adaptive immunity in sticklebacks: evidence for trade-offs from a selection experiment

In vertebrates, the immune system consists of two arms of different characteristics: the innate and the acquired immune response. Parasites that are only shortly exposed to the immune system are most efficiently attacked by fast, constitutive innate immune mechanisms. Here, we experimentally selected within four fish families for high innate resistance versus susceptibility of three-spined sticklebacks (Gasterosteus aculeatus) against infection with the eye-fluke (Diplostomum pseudospathacaeum), a parasite whose metacercariae are protected from the immune system within the eye lens. We predicted that in families with high susceptibility, the adaptive immune system would be upregulated when challenged with infection. In accordance, we found that MHC class IIB expression is increased by approximately 50% in those lines selected for higher parasite load (i.e. low innate response). This suggests extensive genetic correlations between innate and adaptive immune system and/or crosstalk between both lines of defense. An efficient, specific innate immune response might reduce overall activation of the immune system and potentially alleviate associated effects of immunopathology.     

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

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

Migration and life histories of the threespine stickleback: evidence for adaptive variation in growth rate between populations

Synopsis Migratory fishes should exhibit higher growth rates and larger body size than nonmigrants. To test this hypothesis, laboratory reared threespine sticklebacks,Gasterosteus aculeatus, representing three populations from a single drainage in northern California, U.S.A. were compared. These populations differ in their migratory patterns, ranging from highly migratory anadromous forms to nonmigratory freshwater residents. The nonmigratory inland population was significantly smaller in standard length at most ages, with correspondingly reduced growth rates compared to the more migratory upstream and estuary populations. Von Bertalanffy growth functions described the growth trajectories of these fish well, accounting for approximately 99% of the variance in body size exhibited by these populations. Broad sense heritability estimates for body size were significant for all three populations at age 60 days but were significant only for the inland population at later ages. The results of this study provide evidence of genetically-based variation in growth rate and body size among these stickleback populations, and these differences are consistent with the hypothesis that adaptation to different migratory lifestyles has occurred.     

Recent duplication and inter-locus gene conversion in major histocompatibility class II genes in a teleost,the three-spined stickleback

Using a bacterial artificial chromosome (BAC) library, we analysed a 99.5 kb genomic segment containing the major histocompatibility class II genes of a teleost, the three-spined stickleback Gasterosteus aculeatus. Experiments with G. aculeatus have provided direct evidence for balancing selection by pathogens and mate choice driving MH class II beta polymorphism. Two sets of paralogous class II alpha genes and beta genes in a tandem arrangement were identified, designated Gaac-DAA/DAB and Gaac-DBA/DBB. Expression analysis of the beta genes using single-strand conformation polymorphism revealed that both gene copies are expressed. Based on an analysis of pairwise nucleotide polymorphisms, we estimate that the duplication into two paralogous class II loci occurred only 1.2–2.4 million years ago, 1–2 orders of magnitude more recently than in other fish, bird or mammalian species. At the 3-direction of the classical MH loci, we identified another seven genes or gene fragments, two of which (small inducible cytokine, complement regulatory factor) are related to immune function in other vertebrates. None of these genes were associated with MH class II genes in zebrafish, suggesting a markedly different organisation of the MH class II region in sticklebacks, and presumably, across bony fishes. When the nucleotide substitution pattern of the novel class II beta genes was analysed together with a representative sequence sample isolated from fish in northern Germany (n=27), we found that the peptide binding region of the Gaac-DAB and Gaac-DBB loci had undergone an inter-locus gene conversion (P=0.007). In accordance, we found a 10- to 20-fold higher frequency of CpG-islands on the MH class II segment compared to other species, a feature that may be conducive for inter-locus recombination.     

Sticklebacks from streams are more bold than sticklebacks from ponds

Risk-taking behaviour has important consequences for fitness. Here, we show that risk-taking behaviour in sticklebacks consistently varies according to the habitat of origin. We compared the risk-taking behaviour of individual sticklebacks from three pond and three stream populations. Specifically, we measured willingness to forage under predation risk following a simulated attack by a model heron predator. Sticklebacks from stream populations were more willing to forage under predation risk than fish from pond populations. Sticklebacks from streams resumed eating after the simulated attack faster and spent more time eating compared to sticklebacks from ponds. We discuss these findings in terms of differences in life history and predation pressure in the two habitat types.     

No sibling odor preference in juvenile three-spined sticklebacks

Laboratory-bred juvenile three-spined sticklebacks from 11 sibshipsdid not prefer to shoal with their siblings when they were offeredthe choice between odor from unfamiliar siblings and non-kinin a fluviarium, although the power for finding a significantpreference was very high (0.99). The test fish preferred theside where odor from the heavier shoal was supplied; this shows thatthey could appreciate odor cues from conspecifics in our apparatusand should have preferred their siblings if such a preferenceexists. Our results are compatible with theoretical predictionsbut are at variance with previous findings by other authors.We used independent replicates in a blind protocol with strictrandomization of fish and procedures.     

Habitat segregation in a salt marsh among adult sticklebacks (Gasterosteidae)

Synopsis The spatial distribution, seasonal abundance and diel activity of four sticklebacks,Gasterosteus aculeatus, G. wheatlandi, Pungitius pungitius, andApeltes quadracus. coexisting in a St. Lawrence salt marsh were examined to see how these closely related species share their habitat. While all four species breed in the Riviè des Vases, a tidal creek, only three species are found in the adjacent salt marsh pools,A. quadracus being absent. Results are interpreted in terms of avoidance of interspecific competition for space during the relatively short breeding season at this latitude.