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.     

Frequency of Ectodysplasin alleles and limited introgression between sympatric threespine stickleback populations

The threespine stickleback (Gasterosteus aculeatus) is primitively an anadromous or resident marine species but has repeatedly colonized fresh water, where predictable phenotypic divergence usually occurs rapidly. A conspicuous element of this divergence is change of the number and position of lateral armor plates from about 33 that cover the entire flank (complete) to <10 anterior plates (low). This difference is caused primarily by variation at the Ectodysplasin (Eda) locus. The low Eda allele appears to be rarer in two geographically adjacent anadromous populations from Cook Inlet, Alaska than in most marine or anadromous populations reported from elsewhere, and there is no evidence of elevated gene flow for Eda between anadromous and resident lake threespine stickleback populations that breed in sympatry. However, the two anadromous populations are divergent for the frequencies of two complete Eda alleles. It is not clear how monomorphic low-plated freshwater populations in Cook Inlet have almost invariably acquired ancestral low Eda alleles from anadromous ancestors in which this allele appears to be extremely rare.     

Parasite burdens differ between sympatric three-spined stickleback species

The ecological theory of adaptive radiation states that differences in ecological circumstances among local populations are the cause of divergence that leads to speciation. The role of parasites in contributing to divergence has seldom been considered, despite their ubiquity and known selective effects. The potential for parasites to contribute to divergence between closely related taxa was examined by quantifying the variation in parasite burdens between sympatric three-spined stickleback species ( Gasterosteus aculeatus complex) in two lakes in coastal British Columbia, Canada. In doing so the relative importance of geographical differences between lakes and trophic or microhabitat differences between species within lakes were evaluated. The entire metazoan parasite burdens of a total of 255 limnetic and benthic sticklebacks in Paxton and Priest lakes were assayed over five time points between spring and autumn. Despite their sympatric distributions, there were large differences in parasite burdens between benthic and limnetic sticklebacks within lakes and these were consistent across both lakes. In particular, limnetics suffered greater burdens of the parasites Schistocephalus solidus and Diplostomum scudderi and benthics had much higher burdens of parasitic glochidia (mollusc larvae). Parasite burdens also differed quantitatively between lakes, but in general such differences were less pronounced than those between the stickleback species. The documented differences in parasite burdens between stickleback species have potential to contribute to divergent selection on life history, immunological and secondary sexual characters that could contribute to reproductive isolation between the species.     

Genetic divergence in adaptive characters between sympatric species of stickleback

This study explored the genetic basis of phenotypic differences between two sympatric species of ecologically and morphologically divergent sticklebacks (Gasterosteus aculeatus complex). The aim was to understand how many loci determine the differences and to what extent the differences are due to additive or nonadditive gene action. I reared the two parental species, F1 and F2 hybrids, and both backcrosses in the laboratory and measured the following quantitative characters: gill raker number and length (both involved in feeding), lateral plate number and pelvic spine length (both involved in predator defense), and growth (a fitness component). I then applied joint-scaling regression models to estimate composite additive, dominance and epistatic effects, and their contribution to divergence of parental lines. A simple additive model was sufficient for gill raker number and growth; additive and dominance effects contributed significantly to divergence in plate number and pelvic spine length; and additive, dominance, and epistatic effects contributed significantly to divergence in gill raker length. Wright's estimator for the number of loci for the four morphological characters ranged from 1 to 50. My results suggest that adaptive divergence between limnetic and benthic sticklebacks has taken place through a variety of genetic mechanisms specific to different traits. Though interspecific hybrids are completely fertile and viable in the laboratory, they are selected against in the wild. The pattern of inheritance for the traits examined here directly influences how well hybrids can exploit the two major resource environments in the wild.     

Modelling sympatric speciation by means of biologically plausible mechanistic processes as exemplified by threespine stickleback species pairs

We investigate the plausibility of sympatric speciation through a modelling study. We built up a series of models with increasing complexity while focussing on questioning the realism of model assumptions by checking them critically against a particular biological system, namely the sympatric benthic and limnetic species of threespine stickleback in British Columbia, Canada. These are morphologically adapted to their feeding habits: each performs better in its respective habitat than do hybrids with intermediate morphology. Ecological character displacement through disruptive selection and competition, and reinforcement through mating preferences may have caused their divergence. Our model assumptions include continuous morphological trait(s) instead of a dimorphic trait, and mating preferences based on the same trait(s) as selected for in food competition. Initially, morphology is intermediate. We apply disruptive selection against intermediates, frequency-dependent resource competition, and one of two alternative mating preference mechanisms. Firstly, preference is based on similarity where mating preference may result from “imprinting” on conspecifics encountered in their preferred foraging habitat. Here, speciation occurs easily—ecological hybrid inferiority is not necessary. Hybrid inferiority reinforces the stringency of assortative mating. Secondly, individual preferences exist for different trait values. Here, speciation occurs when linkage disequilibrium between trait and preference develops, and some hybrid inferiority is required. Finally, if the morphology subject to disruptive selection, frequency-dependent competition, and mate choice, is coded for by two loci, linkage disequilibrium between the two loci is required for speciation. Speciation and reinforcement of stringency of choosiness are possible in this case too, but rarely. Results demonstrate the contingency of speciation, with the same starting point not necessarily producing the same outcome. The study resulted in flagging issues where models often lack in biological realism and issues where more empirical studies could inform on whether assumptions are likely valid.     

Phenotypic divergence and reproductive isolation between sympatric forms of Japanese threespine sticklebacks

The threespine stickleback ( Gasterosteus aculeatus ) species complex is well suited for identifying the types of phenotypic divergence and isolating barriers that contribute to reproductive isolation at early stages of speciation. In the present study, we characterize the patterns of genetic and phenotypic divergence as well as the types of isolating barriers that are present between two sympatric pairs of threespine sticklebacks in Hokkaido, Japan. One sympatric pair consists of an anadromous and a resident freshwater form and shows divergence in body size between the forms, despite the lack of genetic differentiation between them. The second sympatric pair consists of two anadromous forms, which originated before the last glacial period and are currently reproductively isolated. These two anadromous forms have diverged in many morphological traits as well as in their reproductive behaviours. Both sexual isolation and hybrid male sterility contribute to reproductive isolation between the anadromous species pair. We discuss the shared and unique aspects of phenotypic divergence and reproductive isolation in the Japanese sympatric pairs compared with postglacial stickleback species pairs. Further studies of these divergent species pairs will provide a deeper understanding of the mechanisms of speciation in sticklebacks.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 671–685.     

Sequential mate choice and sexual isolation in threespine stickleback species

Sequential mate choice strategies predict how females should alter their choosiness based on the availability of attractive males. There are many studies on sequential mate choice within species, but few have asked whether females apply these strategies to interactions between species and how these strategies may affect hybridization. We tested how previous interactions with conspecific and heterospecific males affect mate preference and sexual isolation in two threespine stickleback species (benthics and limnetics: Gasterosteus spp.). Consistent with previous work, we found that within species, stickleback females gauge male attractiveness relative to previously encountered males. If females extend these decision rules between species, we predicted that previous interactions with conspecifics should make heterospecifics less attractive, whereas interactions with heterospecifics should make conspecifics more attractive. However, females found heterospecifics less attractive after prior experience, largely independent of the species of male first encountered. Thus, sequential mate choice strategies are used within but not between species in sticklebacks. Further, learning from prior courtship interactions acts to enhance existing sexual isolation between species.     

Colour plasticity and background matching in a threespine stickleback species pair

Examining differences in colour plasticity between closely‐related species in relation to the heterogeneity of background colours found in their respective habitats may offer important insight into how cryptic colour change evolves in natural populations. In the present study, we examined whether nonbreeding dorsal body coloration has diverged between sympatric species of stickleback along with changes in habitat‐specific background colours. The small, limnetic species primarily occupies the pelagic zone and the large, benthic species inhabits the littoral zone. We placed benthic and limnetic sticklebacks against extremes of habitat background colours and measured their degree of background matching and colour plasticity. Benthics matched the littoral background colour more closely than did the limnetics, although there was no difference between species in their resemblance to the pelagic background colour. Benthics were able to resemble both background colours by exhibiting greater directional colour plasticity in their dorsal body coloration than limnetics, which may be an adaptive response to the greater spectral heterogeneity of the littoral zone. The present study highlights how habitat‐specific spectral characteristics may shape cryptic coloration differences between stickleback species. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 902–914.     

Divergence in drought‐response traits between sympatric species of Mimulus

Differential adaptation to local environmental conditions is thought to be an important driver of speciation. Plants, whose sedentary lifestyle necessitates fine‐tuned adaptation to edaphic conditions such as water availability, are often distributed based on these conditions. Populations occupying water‐limited habitats may employ a variety of strategies, involving numerous phenotypes, to prevent and withstand desiccation. In sympatry, two closely related Mimulus species—M. guttatus and M. nasutus—occupy distinct microhabitats that differ in seasonal water availability. In a common garden experiment, we characterized natural variation within and between sympatric M. guttatus and M. nasutus in the ability to successfully set seed under well‐watered and drought conditions. We also measured key phenotypes for drought adaptation, including developmental timing, plant size, flower size, and stomatal density. Consistent with their microhabitat associations in nature, M. nasutus set seed much more successfully than M. guttatus under water‐limited conditions. This divergence in reproductive output under drought was due to differences in mortality after the onset of flowering, with M. nasutus surviving at a much higher rate than M. guttatus. Higher seed set in M. nasutus was mediated, at least in part, by a plastic increase in the rate of late‐stage development (i.e., fruit maturation), consistent with the ability of this species to inhabit more ephemeral habitats in the field. Our results suggest adaptation to water availability may be an important factor in species maintenance of these Mimulus taxa in sympatry.     

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.     

Responses to simulated winter conditions differ between threespine stickleback ecotypes

Abiotic factors can act as barriers to colonization and drive local adaptation. During colonization, organisms may cope with changes in abiotic factors using existing phenotypic plasticity, but the role of phenotypic plasticity in assisting or hindering the process of local adaptation remains unclear. To address these questions, we explore the role of winter conditions in driving divergence during freshwater colonization and the effects of plasticity on local adaptation in ancestral marine and derived freshwater ecotypes of threespine stickleback (Gasterosteus aculeatus). We found that freshwater‐resident stickleback had greater tolerance of acute exposure to low temperatures than marine stickleback, but these differences were abolished after acclimation to simulated winter conditions (9L:15D photoperiod at 4 °C). Plasma chloride levels differed between the ecotypes, but showed a similar degree of plasticity between ecotypes. Gene expression of the epithelial calcium channel (ECaC) differed between ecotypes, with the freshwater ecotype demonstrating substantially greater expression than the marine ecotype, but there was no plasticity in this trait under these conditions in either ecotype. In contrast, growth (assessed as final mass) and the expression of an isoform of the electroneutral Na⁺/H⁺ exchanger (NHE3) exhibited substantial change with temperature in the marine ecotype that was not observed in the freshwater ecotype under the conditions tested here, which is consistent with evolution of these traits by a process such as genetic assimilation. These data demonstrate substantial divergence in many of these traits between freshwater and marine stickleback, but also illustrate the complexity of possible relationships between plasticity and local adaptation.     

Distinct spawning migration patterns in sympatric Japan Sea and Pacific Ocean forms of threespine stickleback Gasterosteus aculeatus

Spawning migration patterns were compared between sympatric populations of the anadromous Japan Sea (JS) form and Pacific Ocean (PO) form of the threespine stickleback Gasterosteus aculeatus in the Lake Akkeshi–Bekanbeushi River system, eastern Hokkaido, Japan. In Akkeshi Bay and Lake Akkeshi, the JS form had longer collecting peak periods and more collection peaks than the PO form. Furthermore, although the PO form migrated upstream in freshwater habitats, the greater part of the JS form stayed in brackish waters before breeding. These findings suggest that the 2 forms have distinctly different spawning migration patterns and breeding grounds.     

Ecological divergence and habitat isolation between two migratory forms of Japanese threespine stickleback (Gasterosteus aculeatus)

When two closely related species migrate to divergent spawning sites, divergent use of spawning habitats can directly reduce heterospecific mating. Furthermore, adaptations to divergent spawning habitats can promote speciation as a by‐product of ecological divergence. Here, we investigated habitat isolation and ecological divergence between two anadromous forms of threespine stickleback (Gasterosteus aculeatus), the Japan Sea and Pacific Ocean forms. In several coastal regions of eastern Hokkaido, Japan, these forms migrate to the same watershed to spawn. Our field surveys in a single watershed revealed that segregation of distinct spawning sites between the two forms was maintained within the watershed across multiple years. These spawning sites diverged in salinity and predator composition. Morphological and physiological divergence between the forms also occurs in the direction predicted by ecological differences between the spawning sites. Our data indicate that migration into divergent spawning habitats can be an important mechanism contributing to speciation and phenotypic divergence in anadromous fishes.     

Ecological causes of sex-biased parasitism in threespine stickleback

Males and females can differ in levels of parasitism and such differences may be mediated by the costs of sexual selection or by ecological differences between the genders. In threespine stickleback, Gasterosteus aculeatus , males exhibit paternal care and territorial nest defence and the costs of reproduction may be particularly high for males relative to females. We monitored levels of parasitism for 15 years in a population of stickleback infected by four different parasite species. Consistent with general predictions, overall parasite prevalence (total parasitism) was greater in males than in females. However, this excess did not occur for each species of parasite. Males had higher prevalence of a cestode Cyathocephalus truncatus and a trematode Bunodera sp. relative to females, while females had higher prevalence of a cestode Schistocephalus solidus and nematodes. This suggested ecological sources to differences in parasitism rather than reproductive costs and therefore we examined diet of unparasitized stickleback, predicting that differences in dietary niche would influence relative parasitism. This was partially confirmed and showed that female stomach contents had increased frequency of pelagic items, the major habitat for the primary host of S. solidus whereas males exhibited increased frequency of benthic items, the dominant habitat of C. truncatus and Bunodera. Temporal shifts in the extent and direction of differential parasitism among years between the sexes were associated with temporal shifts in dietary differences. Our results, combined with those in the literature, suggest that ecological differences between genders could be a more important component to patterns of parasitic infection in natural populations than currently appreciated.     

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.     

Microhabitat contributes to microgeographic divergence in threespine stickleback

Since the New Synthesis, most migration-selection balance theory has predicted that there should be negligible differentiation over small spatial scales (relative to dispersal), because gene flow should erode any effect of divergent selection. Nevertheless, there are classic examples of microgeographic divergence, which theory suggests can arise under specific conditions: exceptionally strong selection, phenotypic plasticity in philopatric individuals, or nonrandom dispersal. Here, we present evidence of microgeographic morphological variation within lake and stream populations of threespine stickleback (Gasterosteus aculeatus). It seems reasonable to assume that a given lake or stream population of fish is well-mixed. However, we found this assumption to be untenable. We examined trap-to-trap variation in 34 morphological traits measured on stickleback from 16 lakes and 16 streams. Most traits varied appreciably among traps within populations. Both between-trap distance and microhabitat characteristics such as depth and substrate explained some of the within-population morphological variance. Microhabitat was also associated with genotype at particular loci but there was no genetic isolation by distance, implying that heritable habitat preferences may contribute to microgeographic variation. Our study adds to growing evidence that microgeographic divergence can occur across small spatial scales within individuals’ daily dispersal neighborhood where gene flow is expected to be strong.     

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.     

Directional asymmetry of pelvic vestiges in threespine stickleback

Extensive reduction of the size and complexity of the pelvic skeleton (i.e., pelvic reduction) has evolved repeatedly in Gasterosteus aculeatus. Asymmetrical pelvic vestiges tend to be larger on the left side (i.e., left biased) in populations studied previously. Loss of Pitx1 expression is associated with pelvic reduction in G. aculeatus, and pelvic reduction maps to the Pitx1 locus. Pitx1 knockouts in mice have reduced hind limbs, but the left limb is larger. Thus left-biased directional asymmetry of stickleback pelvic vestiges may indicate the involvement of Pitx1 in pelvic reduction. We examined 6,356 specimens from 27 Cook Inlet populations of G. aculeatus with extensive pelvic reduction. Samples from 20 populations exhibit the left bias in asymmetrical pelvic vestiges expected if Pitx1 is involved, and three have a slight, non-significant left bias. However, samples from three populations have a significant right bias, and one large sample from another population has equal frequencies of specimens with larger vestiges on the left or right side. A sample of fossil threespine stickleback also has significantly left-biased pelvic vestiges. These results suggest that silencing of Pitx1 or the developmental pathway in which it functions in the pelvis is the usual cause of pelvic reduction in most Cook Inlet populations of G. aculeatu, and that it caused pelvic reduction at least 10 million years ago in a stickleback population. A different developmental genetic mechanism is implicated for three populations with right-biased pelvic vestiges and for the population without directional asymmetry.     

A comparison of sex steroid hormone excretion and metabolism by psittacine species

The metabolism, excretory rates, and excretory patterns of carbon 14 (¹⁴C) radiolabeled estradiol (E₂) and testosterone (T) were studied in female budgerigars (Melopsittacus undulatus) and orange‐winged Amazon parrots (Amazona amazonica). Radiolabeled E₂ and T were injected intramuscularly into six budgerigars and two orange‐winged Amazon parrots. Serial fecal/urine samples were collected for 168 h post‐radiolabel injection. Peak radiolabeled E₂ excretion was observed at 4 h post‐injection, and by 24 h, 93.3 ± 6.3 and 65.9% (range, 59.1–72.7%) of the injected radiolabel was recovered in the fecal/urine matter of budgerigars and orange‐winged Amazon parrots, respectively. Similarly, peak radiolabeled T excretion was observed at 4 h post‐injection with 92.7± 3.6 and 66.2% (range, 57.5–75.2%) of the injected radiolabel recovered in the fecal/urine matter by 24 h in the budgerigars and orange‐winged Amazon parrots, respectively. High‐performance liquid chromatography (HPLC) analysis of the fecal/urine material revealed that both parrot species excreted >80% of the radiolabel in the form of complex steroid conjugates. Immunoreactive E₂ and T metabolites were detected using estrone (E₁) and C‐21/C‐19 conjugate enzyme immunoassays, respectively. Hydrolysis of the E₂ metabolites and HPLC analysis of the ether extracts revealed that E₂ and E₁ were the major steroid moieties. Hydrolysis of the T metabolites and HPLC analysis of the ether extracts revealed two and three major unconjugated peaks for the budgerigars and the orange‐winged Amazon parrots, respectively. Zoo Biol 18:247–260, 1999. © 1999 Wiley‐Liss, Inc.