Trying to See Red Through Stickleback Photoreceptors: Functional Substitution of Receptor Sensitivities

A key to understanding animal behavior is knowledge of the sensory information animals extract from their environment. For visually motivated tasks, the information animals obtain through their eyes is often assumed to be essentially the same as that perceived by humans. However, known differences in structure and processing among the visual systems of different animals clearly indicate that the world seen by each is different. A well‐characterized difference between human and other animal visual systems is the number of types and spectral sensitivities of their photoreceptors. We are developing a technique, functional substitution, that exploits knowledge of these differences to portray for human subjects, colors as they would appear through the photoreceptors of another animal. In a specific application, we ask human subjects to rank hues of male threespine stickleback (Gasterosteus aculeatus) throats viewed through stickleback photopigments. We compare these ranks to ranks of the same throat hues viewed through normal human photoreceptors. We find essentially no difference between the two sets of rankings. This suggests that any differences in human and stickleback rankings of such hues would result from differences in post‐receptoral neural processing. Using a previously developed model of stickleback neural processing, we established another ranking of the hues which was again essentially the same as the rankings produced by the human subjects. A growing literature indicates that stickleback do rank such hues in the evaluation of males as potential mates or threats. Although our results do not demonstrate that humans and stickleback use the same mechanisms to assess color, our experiments significantly failed to show that stickleback and human rankings of throat hues should be different. Nevertheless, a comparison of all these rankings to ranks derived from subjective color scoring by human observers suggests that color scoring may utilize other cues and should thus be used cautiously.     

Conspicuous Female Ornamentation and Tests of Male Mate Preference in Threespine Sticklebacks (Gasterosteus aculeatus)

Sexual selection drives the evolution of exaggerated male ornaments in many animal species. Female ornamentation is now acknowledged also to be common but is generally less well understood. One example is the recently documented red female throat coloration in some threespine stickleback (Gasterosteus aculeatus) populations. Although female sticklebacks often exhibit a preference for red male throat coloration, the possibility of sexual selection on female coloration has been little studied. Using sequential and simultaneous mate choice trials, we examined male mate preferences for female throat color, as well as pelvic spine color and standard length, using wild-captured threespine sticklebacks from the Little Campbell River, British Columbia. In a multivariate analysis, we found no evidence for a population-level mate preference in males, suggesting the absence of directional sexual selection on these traits arising from male mate choice. Significant variation was detected among males in their preference functions, but this appeared to arise from differences in their mean responsiveness across mating trials and not from variation in the strength (i.e., slope) of their preference, suggesting the absence of individual-level preferences as well. When presented with conspecific intruder males, male response decreased as intruder red throat coloration increased, suggesting that males can discriminate color and other aspects of phenotype in our experiment and that males may use these traits in intrasexual interactions. The results presented here are the first to explicitly address male preference for female throat color in threespine sticklebacks.     

Evolution and assessment of colour patterns in stream-resident and anadromous male threespine stickleback Gasterosteus aculeatus from three regions

We compared the colour patterns of free swimming, reproductively active male threespine stickleback Gasterosteus aculeatus of the anadromous and stream ecotypes from three geographically distinct regions. Consistent with the hypothesis of environmentally mediated selection, our results indicate ecologically replicated differences in G. aculeatus coloration between anadromous and stream-resident populations, and that G. aculeatus probably have the visual acuity to discriminate colour pattern differences between anadromous and stream-resident fish.     

Colour vision in the passeriform bird,Leiothrix lutea: correlation of visual pigment absorbance and oil droplet transmission with spectral sensitivity

The visual receptors in the retina of the passeriform bird Leiothrix lutea were examined microspectro-photometrically. The rods had a maximum absorbance close to 500 nm. Four spectrally different classes of single cone were identified with typical combinations of photopigments and oil droplets: a long-wave sensitive cone with a photopigment P568 and a droplet with a cut-off wavelength at 564 nm, a middle-wave sensitive cone with a P499 and a droplet with a cut-off at 506 nm, a short-wave sensitive cone with a P454 and a droplet with maximum absorbance below 410nm and an ultraviolet sensitive cone with a P355 and a transparent droplet. Double cones possessed a P568 in both the principal and accessory members. A pale droplet with variable absorbance (maximal at about 420 nm) was associated with the principal member whereas the ellipsoid region of the accessory member contained only low concentrations of carotenoid. The effective spectral sensitivities of the different cone classes were calculated from the characteristic combinations of oil droplets and photopigments and corrected for the absorbance of the ocular media. Comparison of these results with the behavioural spectral sensitivity function of Leiothrix lutea suggests that the increment threshold photopic spectral sensitivity of this avian species is mediated by the 4 single cone classes modified by neural opponent mechanisms.Abbreviations LWS long wave sensitive - MWS middle wave sensitive - SWS short wave sensitive (cones)     

Handling does not affect reproductive signals of male threespine stickleback

We examined the affect of handling on reproductive signal expression in male threespine stickleback, Gasterosteus aculeatus. Spectrophotometric techniques have become popular methods for measuring fish color, but the measurements require handling of the subjects in order to make measurements. Fish can undergo rapid physiological color change in response to stress. As such, handling fish may induce color changes and measured colour may not be representative of signal appearance under non-stressful conditions. We measured the reflectance characteristics of the opercular, ventro-lateral and dorso-lateral areas of 41 reproductive males from Hotel Lake, BC, Canada using spectroradiometry immediately upon capture and again at 2, 3, 4, 5, 10, 15, and 20 min post-capture. Repeated measures ANOVA revealed that post-capture handling did not affect opercular or ventro-lateral reflectance characteristics over the 20 min period. However, we did observe a change in dorso-lateral reflectance characteristics of parental males over the experiment. The results of our study show that handling does not influence reflective properties of two key components of stickleback reproductive signals during a time frame that is reasonable for taking field measurements of signal color.     

Reflectance characteristics are correlated with male condition in a population of threespine stickleback (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>) that has lost the species typical nuptial signal

Several populations of threespine stickleback (Gasterosteus aculeatus) on the Pacific Coast of North America remain drab during courtship and become melanic during parental care rather than adopt the species typical red signal. Male signal redness is an honest signal of male physiological condition. Here, I test the prediction that reflectance characteristics of drab males also honestly indicate male condition. I located, observed and captured nesting stickleback from Brannen Lake, British Columbia, Canada. I measured reflectance characteristics of each male’s signal right after capture and later measured its wet weight and total length to calculate Fulton’s condition index, K. Males in better condition, higher K, had lower total reflectance (i.e. were darker) than males in poorer condition. The principals underlying honest signaling appear to be operating despite the possession of a novel nuptial signal in Brannen Lake stickleback.     

Color vision of the budgerigar (<Emphasis Type="Italic">Melopsittacus undulatus</Emphasis>): hue matches,tetrachromacy, and intensity discrimination

Budgerigars, Melopsittacus undulatus, were trained to discriminate monochromatic lights from mixtures of two comparison lights. The addition of small amounts of UV (365 nm) to blue or yellow lights dramatically changed the color for the birds. Hue matches showed the birds to be dichromatic both at long wavelengths (only P565 and P508 active) and at short wavelengths (only P370 and P445 active because of screening of P508 and P565 by cone oil droplets). In mid-spectrum (only P445 and P508 active), a hue match was achieved, but the results were more complicated because two opponent neural processes were activated. All observed hue matches were in quantitative agreement with calculations of relative quantum catch in the pairs of participating single cones and point to the presence of a minimum of three opponent neural processes. For the hue matches at mid- and short wavelengths, the calculations also predict peak values of absorbance of the cone oil droplets associated with P508 and P445. Relative intensity of the training light affected difficult matches at long but not short wavelengths, likely due to achromatic signals from the double cones. With suitable training, birds could make intensity discriminations at short wavelengths, where the double cones have diminished sensitivity.     

Reversed brain size sexual dimorphism accompanies loss of parental care in white sticklebacks

Uncovering factors that shape variation in brain morphology remains a major challenge in evolutionary biology. Recently, it has been shown that brain size is positively associated with level of parental care behavior in various taxa. One explanation for this pattern is that the cognitive demands of performing complex parental care may require increased brain size. This idea is known as the parental brain hypothesis (PBH). We set out to test the predictions of this hypothesis in wild populations of threespine stickleback (Gasterosteus aculeatus). These fish are commonly known to exhibit (1) uniparental male care and (2) sexual dimorphism in brain size (males>females). To test the PBH, we took advantage of the existence of closely related populations of stickleback that display variation in parental care behavior: common marine threespine sticklebacks (uniparental male care) and white threespine sticklebacks (no care). To begin, we quantified genetic differentiation among two common populations and three white populations from Nova Scotia. We found overall low differentiation among populations, although F_ST was increased in between‐type comparisons. We then measured the brain weights of males and females from all five populations along with two additional common populations from British Columbia. We found that sexual dimorphism in brain size is reversed in white stickleback populations: males have smaller brains than females. Thus, while several alternatives need to be ruled out, the PBH appears to be a reasonable explanation for sexual dimorphism in brain size in threespine sticklebacks.     

LOSS OF NUPTIAL COLOR IN THREESPINE STICKLEBACKS (GASTEROSTEUS ACULEATUS)

Loss of conspicuous nuptial color in Gasterosteus aculeatus (threespine stickleback) has been reported from several localities in western North America and is ascribed to increased rates of predation or to convergent threat displays. I have examined 66 populations of G. aculeatus from the Queen Charlotte Archipelago and found extensive variation in the expression of red nuptial color. Males in 31 of the populations lack red throats, while males in five populations have major expression of red nuptial color. I test two hypotheses for nuptial-color loss: that the loss results from increased predation rates and that it involves differences in water spectra (relative transmission at 400 nm). Results, which are consistent with the second hypothesis, show that the greatest expression of red pigment occurs in habitats with the highest water clarity, while loss of red nuptial color is generally found in heavily stained waters. There is no correlation between nuptial-color loss and presence or absence of vertebrate predators. Two new hypotheses for these associations are proposed: signal-masking in spectrally restricted habitats and carotenoid deficiencies in the diet. Previous studies of red nuptial color and its loss in Gasterosteus merit additional attention, given the associations with underwater spectra.     

Advancing breeding in stickleback (Gasterosteus aculeatus) to produce two reproductive cycles per year

The effects of photoperiod and temperature manipulation on reproductive cycles in threespine stickleback Gasterosteus aculeatus were examined. The experimental “advanced group” conditions were adjusted to simulate two reproductive seasons within a calendar year by adjusting light and temperature cycles. G. aculeatus subject to advanced conditions had two reproductive cycles per year, grew at normal rates and suffered little additional mortality. The research of many stickleback scientists would benefit from faster generation times and our methods could potentially shorten the time required to produce fish for genetic, behavioural and morphological work.     

Empirical Modelling of the Population Dynamics of a Small Population of the Threespine Stickleback, <Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>

Synopsis We estimated the abundance of a small population of threespine stickleback, Gasterosteus aculeatus, by mark-recapture over a 21 year period. Length-frequency analysis showed that the population in October consisted almost entirely of young-of-the-year. The per capita annual rate of increase was inversely related to abundance in October. Time series analysis suggested the presence of a cycle of abundance with a period of about 6 years. There was a significant inverse relationship between abundance in year t and in year t + 3. A simple, empirical, deterministic model based on this inverse relationship and run for 100 years predicted that population abundance showed damped oscillations leading to a stable abundance. When a stochastic component was added to the model, seven of 10 runs included a component with a period of about 6 years. These simulations suggest that the dynamics of this population are driven by an interaction between a deterministic (density-dependent) component and a stochastic component. We compare these results with time series of abundance of threespine stickleback obtained from the Thames Estuary in south-east England and Loch Lomond in Scotland.     

Female‐specific increase in primordial germ cells marks sex differentiation in threespine stickleback (Gasterosteus aculeatus)

Gonadal sex differentiation is increasingly recognized as a remarkably plastic process driven by species‐specific genetic or environmental determinants. Among aquatic vertebrates, gonadal sex differentiation is a frequent endpoint in studies of endocrine disruption with little appreciation of underlying developmental mechanisms. Work in model organisms has highlighted the diversity of master sex‐determining genes rather than uncovering any broad similarities prompting the highly conserved developmental decision of testes versus ovaries. Here we use molecular genetic markers of chromosomal sex combined with traditional histology to examine the transition of the bipotential gonads to ovaries or testes in threespine stickleback (Gasterosteus aculeatus). Serially‐sectioned threespine stickleback fry were analyzed for qualitative and quantitative indications of sexual differentiation, including changes in gonadal morphology, number of germ cells and the incidence of gonadal apoptosis. We show that threespine stickleback sampled from anadromous and lacustrine populations are differentiated gonochorists. The earliest sex‐specific event is a premeiotic increase in primordial germ cell number followed by a female‐specific spike in apoptosis in the undifferentiated gonad of genetic females. The data suggest that an increase in PGC number may direct the undifferentiated gonad toward ovarian differentiation. J. Morphol., 2008. © 2007 Wiley‐Liss, Inc.     

PARTIAL REPRODUCTIVE ISOLATION OF A RECENTLY DERIVED RESIDENT‐FRESHWATER POPULATION OF THREESPINE STICKLEBACK (GASTEROSTEUS ACULEATUS) FROM ITS PUTATIVE ANADROMOUS ANCESTOR

We used no‐choice mating trials to test for assortative mating between a newly derived resident‐freshwater population (8–22 generations since founding) of threespine stickleback (Gasterosteus aculeatus) in Loberg Lake, Alaska and its putative anadromous ancestor as well as a morphologically convergent but distantly related resident‐freshwater population. Partial reproductive isolation has evolved between the Loberg Lake population and its ancestor within a remarkably short time period. However, Loberg stickleback readily mate with morphologically similar, but distantly related resident‐freshwater stickleback. Partial premating isolation is asymmetrical; anadromous females and smaller resident‐freshwater males from Loberg Lake readily mate, but the anadromous males and smaller Loberg females do not. Our results indicate that premating isolation can begin to evolve in allopatry within a few generations after isolation as a correlated effect of evolution of reduced body size.     

Genetics of osteal plate polymorphism and microevolution of threespine stickleback (Gasterosteus aculeatus L.)

Summary The results of genetical studies of osteal plate polymorphism of threespine stickleback Gasterosteus aculeatus reported to date (Munzing 1959; Hagen and Gilbertson 1973; Avise 1976) are discussed and proposed inheritance models are considered. Results of crosses between the morphs of G. aculeatus from the White Sea are presented. An attempt has been made by the author to devise a unifying model for the inheritance of plate morphs within the whole range of G. aculeatus. The role of polymorphism in the microevolutionary processes taking place within this complex species is discussed.     

Tending a complex microbiota requires major immune complexity

Animals maintain complex microbial communities within their guts that fill important roles in the health and development of the host. To what degree a host's genetic background influences the establishment and maintenance of its gut microbial communities is still an open question. We know from studies in mice and humans that external factors, such as diet and environmental sources of microbes, and host immune factors play an important role in shaping the microbial communities (Costello et al. 2012 ). In this issue of Molecular Ecology, Bolnick et al. ( 2014a ) sample the gut microbial community from 150 genetically diverse stickleback isolated from a single lake to provide evidence that another part of the adaptive immune response, the major histocompatibility complex class II (MHCII) receptors of antigen‐presenting cells, may play a role in shaping the gut microbiota of the threespine stickleback, Gasterosteus aculeatus (Bolnick et al. 2014a ). Bolnick et al. ( 2014a ) provide insight into natural, interindividual variation in the diversity of both stickleback MHCII alleles and their gut microbial communities and correlate changes in the diversity of MHCII receptor alleles with changes in the microbiota.     

Habitat‐specific trends in ontogeny of body shape in stickleback from coastal archipelago: Potential for rapid shifts in colonizing populations

We investigated ontogenetic trends in body shape of 54 freshwater (48 lake, seven stream) and six anadromous populations of threespine stickleback (Gasterosteus aculeatus L.) from the Haida Gwaii archipelago off the west coast of Canada. Multivariate analysis of covariance on the partial warp scores generated from 12 homologous landmarks on 1,958 digital images of subadult and adult male stickleback indicated that there was considerable variability of population ontogenetic slopes. We used discriminant function analysis to quantify body shape and determined that anadromous stickleback, which are ancestral to the freshwater populations, have a strongly negative ontogenetic slope (?5.62; increased streamlining with increased size). All freshwater populations exhibit a more positive slope (91% differed significantly from the marine slope), with the differences being most accentuated in populations from ponds and streams. In pristine lakes, ontogenetic slope could be predicted by lake volume as well as multivariate measures of habitat. Evidence from field transplant experiments of one of the intact populations indicates a rapid change (5 years) from allometric to isometric growth, equivalent to about half of the total slope variation among intact populations on the archipelago. We interpret this shift as developmental plasticity and suggest this may comprise the precursor for selection of optimal body shapes in these stickleback populations. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

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.     

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.     

Haem—haem interactions in cytochrome aa3 during the anaerobic-aerobic transition

A biphasic response is seen at both 445 and 605 nm as the ascorbate—cytochrome c—cytochrome aa₃ system is taken slowly from the anaerobic to the aerobic state. At low oxygen tensions the 445 nm band is more reduced while at high oxygen tensions the 605 nm band is more reduced. It is suggested that the redox potential for cytochrome a (contributing 70% at 605–630 nm and 50% at 445–455 nm) is a function of the redox state of cytochrome a₃. This model can account for both the aerobic/anaerobic data and for observations of interactions in the anaerobic system alone (Leigh, Jr, J.S., Wilson, D.F., Owen, C.S. and King, T.E. (1974) Arch. Biochem. Biophys. 160, 476–486).