Character displacement of male nuptial colour in threespine sticklebacks (Gasterosteus aculeatus)

To study the isolation mechanism of two commonly intermingled louseworts, Pedicularis rhinanthoides and Pedicularis longiflora , pollination biology in three mixed populations with the two species was investigated during a 3-year project. The results indicated that higher flowering density could help to enhance pollinator activity, and thus increase reproductive output. Bumblebees are the exclusive pollinator for the two louseworts and are essential for their reproductive success. Reproductive isolation between the two species is achieved by a combination of pre- and postzygotic isolation mechanisms. Although both species are pollinated by bumblebees, the present study indicates they successfully avoid interspecific pollen transfer due to floral isolation. Mechanical isolation is achieved by the stigma in the two species picking up pollen from different parts of the pollinator's body, whereas ethological isolation occurs due to flower constancy. Additionally, strong postzygotic isolation was demonstrated by non seed set after artificial cross-pollination even with successful pollen tube growth. We describe the hitherto unreported role of variation in the tightness and direction of the twist of the corolla beak in maintaining mechanical isolation between Pedicularis species. Although floral isolation in Pedicularis is incomplete, it is considered to be an important mechanism in maintaining species boundaries in the genus.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 37–48.     

Rate of food consumption in a population of threespine sticklebacks,Gasterosteus aculeatus,estimated from the faecal production

Synopsis The daily rate of faecal production by threespine sticklebacks living in a small lake was measured at monthly intervals. Laboratory experiments yielded a regression model which allowed the prediction of the rate of food consumption from faecal production. It was estimated that the annual rate of consumption was 12,800 mg per fish. The highest rate of food consumption was in early summer. The experiments also showed that the absorption efficiency was greater at higher temperatures and for heavier fish.Address all correspondence to R.J. Wootton     

Habitat-specific morphological variation among threespine sticklebacks (Gasterosteus aculeatus) within a drainage basin

Habitat-specific morphological variation, often corresponding to resource specialization, is well documented in freshwater fishes. In this study we used landmark based morphometric analyses to investigate morphological variation among threespine sticklebacks (Gasterosteus aculeatus L.) from four interconnected habitat types within a single lowland drainage basin in eastern England. These included the upper and lower reaches of the river, the estuary, a connected ditch network and a coastal salt marsh. We found significant habitat-specific differences in morphology, with three axes of variation describing differences in orbit diameter, body depth, caudal peduncle shape and pectoral fin positioning as well as variation in relative dorsal and pelvic spine size. Interestingly, the ditch system, an artificial and heavily managed habitat, is populated by sticklebacks with a characteristic morphology, suggesting that human management of habitats can in some circumstances lead to morphological variation among the animals that inhabit them. We discuss the mechanisms that conceivably underlie the observed morphological variation and the further work necessary to identify them. Finally, we consider the implications of habitat-specific body shape variation for the behavioural ecology of this ecologically generalist species.     

Risk of predation as a promoting factor of species divergence in threespine sticklebacks (Gasterosteus aculeatus L.)

Icelandic freshwater systems are geologically young and contain only six species of freshwater fish. As these species colonized Icelandic fresh waters they were presented with a diversity of unique, uncontested habitats and food resources, promoting the evolution of new behaviour strategies crucial to the formation of new morphs and speciation. To determine the likelihood that predation threat could affect the antipredator behaviour and possibly the sympatric divergence of prey populations, we analysed antipredator behaviour of seven groups of Icelandic threespine sticklebacks ( Gasterosteus aculeatus ): two marine groups, one group from a lake without piscine predators, and two polymorphic lake populations, each with two groups occupying unique habitats. Shoaling cohesion, school formation and duration, and vigilance in predator inspection/avoidance behaviour varied greatly among groups. The differences appeared to be related to the risk of predation as well as to opportunities and constraints set by the different habitats. Antipredator behaviour was especially pronounced and differed extensively in two polymorphic forms from the lake Thingvallavatn, where predation risk is very high. By keeping the two morphs separate in their respective habitats, high predation risk may be a contributing factor in promoting the habitat-specific divergence of G. aculeatus seen in the lake. This suggests that in situations where refuge habitats are spatially separated, the risk of predation may contribute to the evolution of separate sympatric forms of small fish such as G. aculeatus .  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 189–203.     

Interacting evolutionary constraints in pelvic reduction of threespine sticklebacks, Gasterosteus aculeatus (Pisces, Gasterosteidae)

The pelvic girdle of Gasterosteus aculeatus is normally a complex and robust structure that varies moderately among and within populations, but in several populations it occurs as a vestigial series. Based on 14 Recent and fossil populations from North America and Scotland, three general patterns of intrapopulation variation of vestigial pelvic structures can be recognized. In most cases of pelvic reduction, the size and complexity of the pelvic girdle are reduced mostly by progressive truncation of distal structures, but two patterns of distal truncation occur. Paedomorphosis appears to play a role in all cases of pelvic reduction, but in a fossil assemblage and one extant population it accounts for most of the structural simplification.
Pelvic reduction in populations of Gasterosteus depends on an interaction between natural selection, which appears to determine whether or not pelvic reduction occurs, and phylogenetic constraint (especially developmental constraint), which strongly influences the form of pelvic vestiges. The empirical difficulty of discriminating between phylogenetic constraint and effects of natural selection, and the potential for phylogenetic constraint to produce homoplasy are discussed. Pelvic reduction apparently has been a recurrent phenomenon in Gasterosteus since at least the early Pliocene, but it has not resulted in evolution of a separate lineage of 'pelvicless' sticklebacks because such populations are restricted to lakes, which are ephemeral over evolutionary time. Rapid phyletic pelvic reduction coupled with selective extinction of populations with vestigial pelvic structures has resulted in phylogenetic stasis.     

Global analysis of genes involved in freshwater adaptation in threespine sticklebacks (Gasterosteus aculeatus)

Examples of parallel evolution of phenotypic traits have been repeatedly demonstrated in threespine sticklebacks (Gasterosteus aculeatus) across their global distribution. Using these as a model, we performed a targeted genome scan--focusing on physiologically important genes potentially related to freshwater adaptation--to identify genetic signatures of parallel physiological evolution on a global scale. To this end, 50 microsatellite loci, including 26 loci within or close to (<6 kb) physiologically important genes, were screened in paired marine and freshwater populations from six locations across the Northern Hemisphere. Signatures of directional selection were detected in 24 loci, including 17 physiologically important genes, in at least one location. Although no loci showed consistent signatures of selection in all divergent population pairs, several outliers were common in multiple locations. In particular, seven physiologically important genes, as well as reference ectodysplasin gene (EDA), showed signatures of selection in three or more locations. Hence, although these results give some evidence for consistent parallel molecular evolution in response to freshwater colonization, they suggest that different evolutionary pathways may underlie physiological adaptation to freshwater habitats within the global distribution of the threespine stickleback.     

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.     

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     

Energetics of the annual reproductive cycle in female sticklebacks, Gasterosteus aculeatus L.

Laboratory studies on the thrce-spined stickleback provided predictive equations for the relationships between food consumption, faecal production and growth, and between respiration rate and body weight. These equations were used to estimate the energy income and expenditure at monthly intervals during the annual reproductive cycle of females of mean length from two populations. In winter only a small percentage of the energy income was invested in ovarian or somatic growth, and the latter was negative in some cases. Routine respiration and faecal losses accounted for a high proportion of the energy income. In spring a higher proportion of the energy income was partitioned into somatic and ovarian growth while routine respiration accounted for a smaller proportion of the energy income.     

Water temperature,not fish morph,determines parasite infections of sympatric Icelandic threespine sticklebacks (Gasterosteus aculeatus)

Parasite communities of fishes are known to respond directly to the abiotic environment of the host, for example, to water quality and water temperature. Biotic factors are also important as they affect the exposure profile through heterogeneities in parasite distribution in the environment. Parasites in a particular environment may pose a strong selection on fish. For example, ecological differences in selection by parasites have been hypothesized to facilitate evolutionary differentiation of freshwater fish morphs specializing on different food types. However, as parasites may also respond directly to abiotic environment the parasite risk does not depend only on biotic features of the host environment. It is possible that different morphs experience specific selection gradients by parasites but it is not clear how consistent the selection is when abiotic factors change. We examined parasite pressure in sympatric morphs of threespine stickleback (Gasterosteus aculeatus) across a temperature gradient in two large Icelandic lakes, Myvatn and Thingvallavatn. Habitat‐specific temperature gradients in these lakes are opposite. Myvatn lava rock morph lives in a warm environment, while the mud morph lives in the cold. In Thingvallavatn, the lava rock morph lives in a cold environment and the mud morph in a warm habitat. We found more parasites in fish living in higher temperature in both lakes, independent of the fish morph, and this pattern was similar for the two dominating parasite taxa, trematodes and cestodes. However, at the same time, we also found higher parasite abundance in a third morph living in deep cold–water habitat in Thingvallavatn compared to the cold‐water lava morph, indicating strong effect of habitat‐specific biotic factors. Our results suggest complex interactions between water temperature and biotic factors in determining the parasite community structure, a pattern that may have implications for differentiation of stickleback morphs.     

A comparison of the behavioural responses of parasitized and non-parasitized three-spined sticklebacks, Gasterosteus aculeatus L., to progressive hypoxia

Eighty sticklebacks (32 parasitized, 48 uninfected) were subjected to a serial reduction in dissolved oxygen (DO) concentration until they showed continuous aquatic surface respiration for longer than 10s (> 10s ASR). An analysis of results showed that (1) parasitized adult male and female sticklebacks reacted to low DO significantly earlier than non-parasitized controls; (2) severity of parasite infection was significantly correlated with DO at which > 10s ASR occurred; (3) gravid, non-parasitized females show ASR at a relatively high DO, with a threshold response similar to that of parasitized fish.
It is suggested that the metabolic respiratory demand of the parasitic tapeworm larvae causes the stickleback to modify its behaviour at lowered DO. This behavioural modification causes the fish to surface, where they are likely to be at risk from predatory birds. Field data on DO levels at the study site show that environmental conditions in the shallow lake margins approach the range required to affect the behaviour of heavily parasitized sticklebacks.     

Oxygen consumption by sticklebacks (Gasterosteus aculeatus L.) exposed to zinc

The rate of oxygen consumption by sticklebacks has been studied by long-term continuous-flow respirometry. Exposure to 1 p.p.m. zinc in calcium-free water causes wide variations in individual responses, but oxygen uptake tends to rise and then become extremely erratic, before declining as death approaches. Behavioural abnormalities such as increased ventilation rate, loss of balance, and long periods of inactivity alternating with spasmodic swimming also occur. Exposure to 6.5 p.p.m. zinc in high-calcium water generally causes a rise in oxygen consumption, followed by fluctuations in the rate of uptake, but no behavioural abnormalities occur and deaths are rare even after exposure for 400 h. If restored to zinc-free water after 40 h exposure to zinc, recovery is generally complete, although fluctuating rates of oxygen uptake persist. These results are discussed in relation to previous work on the effects of heavy metals on fish respiration.     

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.     

Inbreeding and developmental stability in three-spined sticklebacks (Gasterosteus aculeatus L.)

Fluctuating asymmetry, small non-directional departures from perfect symmetry in bilateral traits, results from the inability of individuals to buffer development against genetic and environmental perturbations. Fluctuating asymmetry is a widely used measure of developmental stability, and developmental stability has been hypothesised to be inversely related to heterozygosity. We compared male three-spined sticklebacks (Gasterosteus aculeatus L.) that had been inbred for one generation to outbred control males with respect to the asymmetry of a set of bilateral morphometric traits. Inbred fish developed significantly more asymmetric pectoral fins than their outbred counterparts, whereas neither the magnitude of asymmetry for pelvic spines nor for gill covers significantly responded to the treatment. Our results conform to a pattern of heterogeneity amongst traits in their tendency to develop asymmetrically in response to stress.     

Population biology of three-spined sticklebacks, Gasterosteus aculeatus, in Scotland

The age of maturation, longevity and aspects of anti-predator morphology were studied for seven Gasterosteus aculeatus L. populations in Scotland during 1978 and 1979. All seven populations are annual with less than 1% of adults surviving a second year. At the four mainland study sites, breeding adult sticklebacks were larger than at any of the three Hebridean sites. Adult females were larger than adult males at all sites, except Lennox Castle where parasitism may account for the lack of sexual dimorphism. Two of the Hebridean sites, Loch Fada and Loch a Bharpa have spine-deficient G. aculeatus populations which are morphologically unprotected from predation. In the five normally spined populations, some aspects of defensive morphology (index of increase in critical dimension, ventral spine size) are associated with predation risk, while others (lateral plate number) are not. These data are discussed in relation to the current stickleback literature.     

Metabolic correlates of burst swimming capacity of juvenile and adult threespine stickleback (Gasterosteus aculeatus)

The relationship between burst swimming performance and muscle metabolic capacities was examined in juvenile and adult threespine sticklebacks (Gasterosteus aculeatus). The absolute burst speed measured during startle responses increased markedly with growth of juveniles, but this positive allometry did not continue in adults. The allometry of phosphofructokinase (PFK), lactate dehydrogenase, creatine phosphokinase activities and protein concentrations was positive in juveniles and became negative in adults. The lower activities in adults may reflect the mobilization of muscle proteins for reproduction. In juveniles, absolute burst swimming and muscle glycolytic capacity show a similar allometry. However, when the influence of factors such as size and age was removed by calculating residuals from multiple regressions, variation in muscle enzyme activities in juveniles did not explain variation in their swimming capacity. In adults, interindividual variation in PFK and cytochrome C oxidase activities was correlated with variation in the burst swimming capacity. Apparently, mobilization of muscle proteins in support of reproduction may lead muscle enzyme levels to limit burst performance. Accepted: 9 November 1998