Asymmetric learning to avoid heterospecific males in Mesocricetus hamsters

If a female mates with a male of a closely related species, her fitness is likely to decline. Consequently, females may develop behavioral mechanisms to avoid mating with heterospecific males. In some species, one such mechanism is for adult females to learn to discriminate against heterospecific males after exposure to such males. We have previously shown that adult, female Syrian hamsters (Mesocricetus auratus) learn to discriminate against male Turkish hamsters (Mesocricetus brandti) after exposure to a single heterospecific male during 8 days across a wire-mesh barrier. Here we repeated that experiment but this time we exposed female Turkish hamsters to a male Syrian hamster for 8 days and then measured sexual and aggressive behaviors towards that heterospecific male and towards a conspecific male. In contrast to female Syrian hamsters, female Turkish hamsters did not differ in their latency to go into lordosis or in any measure of aggression towards either type of male. Female Turkish hamsters spent less time in lordosis with the heterospecific male, but the percentage of trials in which females copulated with conspecific and heterospecific males did not differ. When comparing females from both species that had been exposed to a heterospecific male for 8days, female Syrian hamsters copulated less and were more aggressive towards the heterospecific male compared to the behavior of female Turkish hamsters. We discuss how this asymmetric response between females of the two species may be due to the much larger geographical range of Turkish hamsters compared to Syrian hamsters.     

Can captivity lead to inter-species mating in two Mesocricetus hamster species?

In two closely related species, females generally prefer conspecific males over heterospecific males. We found that estrous (but not diestrous) female Syrian hamsters Mesocricetus auratus prefer the odors of conspecific males to odors of Turkish hamsters Mesocricetus brandti . However, female Syrian hamsters are not aggressive toward male Turkish hamsters and will readily mate with them. We hypothesize that many generations in captivity led to a reduction in females' ability to avoid inter-species mating, possibly related to the heightened sexual receptivity observed in Mesocricetus hamsters in captivity. To test this hypothesis, we replicated a study carried out with female Turkish hamsters soon after the current laboratory stock of this species was established. In that study, female Turkish hamsters showed lordosis toward male Syrian hamsters in only 20% of interactions and attacked heterospecific males in 80% of the pairings. Using animals descended from that original colony (after many generations in captivity and certain episodes of inbreeding), 100% of female Turkish hamsters mated with heterospecific males and none showed aggression toward heterospecific males. Thus female avoidance of inter-specific mating may be affected by captive rearing conditions.     

Effect of hamster pregnancy on female protein, a homolog of serum amyloid P component.

Pentraxins such as human serum amyloid P component (SAP) and C reactive protein (CRP) represent an ancient family of proteins that are ubiquitous in nature and have evolved with little change in structure or regulation. The pentraxin in the Syrian hamster (Mesocricetus auratus) is unique because it is preferentially expressed in the female at high constitutive levels and accordingly called female protein (FP) or FP(SAP) due to its close homology with human SAP. The high levels of FP in female serum (100-fold greater than male serum) suggested its role in hamster pregnancy, one of the shortest of any eutherian mammal. We determined the serum FP concentration in pregnant Syrian hamsters and found a marked decrease (>80%) at term with the nadir at parturition with subsequent increase. A similar downregulation of FP was found in the normal female Syrian hamster after injury (acute phase response), so in both cases the assumed beneficial effects were achieved with less, rather than more pentraxin, a paradoxical pentraxin response. The fall in serum FP concentration could represent a response to protect the fetus from the high and potentially toxic level of FP normally found in the female, that is harmful because of its association with amyloidosis. An FP that is 97.5% identical to Syrian hamster FP is found in the Turkish hamster (Mesocricetus brandti), although serum levels in females are much lower, and amyloid is very rare. During pregnancy/parturition of Turkish hamsters, the serum level of FP remained remarkably constant. In a more distantly related hamster, the Armenian hamster (Cricetulus migratorius), serum FP actually increased during pregnancy and at parturition in a manner similar to that found in the Armenian hamster during an acute phase response. The heterogeneity of FP kinetics during pregnancy in these three species of hamster indicates pleomorphic gene structure for regulation of their similar FPs, and suggests that this protein may have a different function in the pregnancy of each species.     

Cone pigments in a North American marsupial, the opossum (Didelphis virginiana)

Only two of the four cone opsin gene families found in vertebrates are represented in contemporary eutherian and marsupial species. Recent genetic studies of two species of South American marsupial detected the presence of representatives from two of the classes of cone opsin genes and the structures of these genes predicted cone pigments with respective peaks in the ultraviolet and long-wavelength portions of the spectrum. The Virginia opossum (Didelphis virginiana), a profoundly nocturnal animal, is the only marsupial species found in North America. The prospects for cone-based vision in this species were examined through recordings of the electroretinogram (ERG), a commonly examined retinal response to photic stimulation. Recorded under flickering-light conditions that elicit signals from cone photoreceptors, the spectral sensitivity of the opossum eye is well accounted for by contributions from the presence of a single cone pigment having peak absorption at 561–562 nm. A series of additional experiments that employed various chromatic adaptation paradigms were conducted in a search for possible contributions from a second (short-wavelength sensitive) cone pigment. We found no evidence that such a mechanism contributes to the ERG in this marsupial.     

Photoreceptors and photopigments in a subterranean rodent,the pocket gopher (<Emphasis Type="Italic">Thomomys bottae</Emphasis>)

Pocket gophers (Thomomys bottae) are rodents that spend much of their lives in near-lightless subterranean burrows. The visual adaptations associated with this extreme environment were investigated by making anatomical observations of retinal organization and by recording retinal responses to photic stimulation. The size of the eye is within the normal range for rodents, the lens transmits light well down into the ultraviolet, and the retina conforms to the normal mammalian plan. Electroretinogram recording revealed the presence of three types of photopigments, a rod pigment with a spectral peak of about 495 nm and two types of cone pigment with respective peak values of about 367 nm (UV) and 505 nm (medium-wavelength sensitive). Both in terms of responsivity to lights varying in temporal frequency and in response recovery following intense light adaptation, the cone responses of the pocket gopher are similar to those of other rodents. Labeling experiments indicate an abundance of cones that reach densities in excess of 30,000 mm^–2. Cones containing UV opsin are found throughout the retina, but those containing medium-wavelength sensitive opsin are mostly restricted to the dorsal retina where coexpression of the two photopigments is apparently the rule. Rod densities are lower than those typical for nocturnal mammals.     

Rods are rods and cones cones, and (never) the twain shall meet.

More than 100 photopigment G protein-coupled receptors (opsins) have been sequenced and organized into six classes. Rod photoreceptors in various species have been found to express an opsin from one of the two rhodopsin classes, while cones express an opsin from one of the four remaining classes. It has now been discovered that salamander short-wavelength sensitive cones and green rods express the same opsin, while manifesting other features that classically distinguish rods from cones.     

Visual pigments of marine carnivores: pinnipeds, polar bear, and sea otter

Rod and cone visual pigments of 11 marine carnivores were evaluated. Rod, middle/long-wavelength sensitive (M/L) cone, and short-wavelength sensitive (S) cone opsin (if present) sequences were obtained from retinal mRNA. Spectral sensitivity was inferred through evaluation of known spectral tuning residues. The rod pigments of all but one of the pinnipeds were similar to those of the sea otter, polar bear, and most other terrestrial carnivores with spectral peak sensitivities (λ_max) of 499 or 501 nm. Similarly, the M/L cone pigments of the pinnipeds, polar bear, and otter had inferred λ_max of 545 to 560 nm. Only the rod opsin sequence of the elephant seal had sensitivity characteristic of adaptation for vision in the marine environment, with an inferred λ_max of 487 nm. No evidence of S cones was found for any of the pinnipeds. The polar bear and otter had S cones with inferred λ_max of ∼440 nm. Flicker-photometric ERG was additionally used to examine the in situ sensitivities of three species of pinniped. Despite the use of conditions previously shown to evoke cone responses in other mammals, no cone responses could be elicited from any of these pinnipeds. Rod photoreceptor responses for all three species were as predicted by the genetic data.Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.     

Termination of gonadal refractoriness in Turkish hamsters, Mesocricetus brandti

The Turkish hamster (Mesocricetus brandti) is a photoperiodic species. In this investigation, we characterized the photoperiodic requirements for termination of gonadal refractoriness, defined as the inability of the animal to respond to short-day treatment with gonadal regression. Paired testes weights were reduced to less than 20% of their original weight by 10 wk of 12L:12D treatment. This was followed by spontaneous testicular recrudescence (completed by Week 25 of 12L:12D treatment), the overt indication of refractoriness to short photoperiods. Next, the period of long-day exposure sufficient for termination of refractoriness was determined. Refractory males were exposed to 16L:8D for 5 to 20 wk. Ten weeks of 16L:8D treatment was enough for the animals to regain the sensitivity to a second challenge of 12L:12D treatment. Fifteen weeks of 20L:4D or 16L:8D terminated refractoriness in female Turkish hamsters; 20L:4D therefore was not interpreted as a short day by refractory hamsters. This was unexpected because in photosensitive animals this photoperiod acts like a short day, causing gonadal regression. These results suggest that Turkish hamsters are similar to Syrian hamsters in that both species require two or more months of long days in summer to recover sensitivity to the short days of the following fall.     

Retinal Cone Photoreceptors of the Deer Mouse Peromyscus maniculatus: Development,Topography, Opsin Expression and Spectral Tuning

A quantitative analysis of photoreceptor properties was performed in the retina of the nocturnal deer mouse, Peromyscus maniculatus, using pigmented (wildtype) and albino animals. The aim was to establish whether the deer mouse is a more suitable model species than the house mouse for photoreceptor studies, and whether oculocutaneous albinism affects its photoreceptor properties. In retinal flatmounts, cone photoreceptors were identified by opsin immunostaining, and their numbers, spectral types, and distributions across the retina were determined. Rod photoreceptors were counted using differential interference contrast microscopy. Pigmented P. maniculatus have a rod-dominated retina with rod densities of about 450.000/mm² and cone densities of 3000 - 6500/mm². Two cone opsins, shortwave sensitive (S) and middle-to-longwave sensitive (M), are present and expressed in distinct cone types. Partial sequencing of the S opsin gene strongly supports UV sensitivity of the S cone visual pigment. The S cones constitute a 5-15% minority of the cones. Different from house mouse, S and M cone distributions do not have dorsoventral gradients, and coexpression of both opsins in single cones is exceptional (<2% of the cones). In albino P. maniculatus, rod densities are reduced by approximately 40% (270.000/mm²). Overall, cone density and the density of cones exclusively expressing S opsin are not significantly different from pigmented P. maniculatus. However, in albino retinas S opsin is coexpressed with M opsin in 60-90% of the cones and therefore the population of cones expressing only M opsin is significantly reduced to 5-25%. In conclusion, deer mouse cone properties largely conform to the general mammalian pattern, hence the deer mouse may be better suited than the house mouse for the study of certain basic cone properties, including the effects of albinism on cone opsin expression.     

M opsin phosphorylation in intact mammalian retinas

The deactivation of visual pigments involved in phototransduction is critical for recovering sensitivity after exposure to light in rods and cones of the vertebrate retina. In rods, phosphorylation of rhodopsin by rhodopsin kinase (GRK1) and the subsequent binding of visual arrestin completely terminates phototransduction. Although signal termination in cones is predicted to occur via a similar mechanism as in rods, there may be differences due to the expression of related but distinct gene products. While rods only express GRK1, cones in some species express only GRK1 or GRK7 and others express both GRKs. In the mouse, cone opsin is phosphorylated by GRK1, but this has not been demonstrated in mammals that express GRK7 in cones. We compared cone opsin phosphorylation in intact retinas from the 13-lined ground squirrel (GS) and pig, cone- and rod-dominant mammals, respectively, which both express GRK7. M opsin phosphorylation increased during continuous exposure to light, then declined between 3 and 6 min. In contrast, rhodopsin phosphorylation continued to increase during this time period. In GS retina homogenates, anti-GS GRK7 antibody blocked M opsin phosphorylation by 73%. In pig retina homogenates, only 20% inhibition was observed, possibly due to phosphorylation by GRK1 released from rods during homogenization. Our results suggest that GRK7 phosphorylates M opsin in both of these mammals. Using an in vitro GTPgammaS binding assay, we also found that the ability of recombinant M opsin to activate G(t) was greatly reduced by phosphorylation. Therefore, phosphorylation may participate directly in the termination of phototransduction in cones by decreasing the activity of M opsin.     

The circadian system of the Turkish hamster, Mesocricetus brandti: responses to light

The circadian system of the Turkish hamster controlling wheel-running activity responded to single 1-hr light pulses and to repeated 1-hr pulses in a similar way as that of Syrian hamsters studied previously. At constant light of 100 lx, the period length (tau) of the freerunning activity rhythm of Turkish hamsters was longer and the activity time (alpha) was shorter than that of Syrian hamsters. Among individuals, the ability of the system to be entrained by one 1-hr light pulse per cycle was related to the range (advance plus delay amplitude) of the phase response curve (PRC) derived from single light pulses and to the compression of alpha caused by the pulse Zeitgeber. The data support the hypothesis derived from experiments on Syrian hamsters that the range of the PRC is functionally related with alpha, possibly reflecting the phase relations (coupling) between two oscillators.     

Laboratory assessment of chronic hepatitis in Syrian hamsters.

Clinical chemistry studies in the diagnosis of hamster diseases have received little attention. Although normal values exist for serum constituents, the effects of disease on these values are not well documented. Chronic hepatitis is endemic in several Syrian hamster (Mesocricetus auratus) colonies and is reported mainly through routine histologic examination. We investigated whether any differences in serum clinical chemistries were present in animals with hepatobiliary disease versus unaffected hamsters. Only serum alanine aminotransferase (ALT) and bile acids were significantly elevated in hamsters with chronic hepatitis only. In hamsters that had both chronic hepatitis and biliary disease, the serum ALT, alkaline phosphatase, cholesterol, and bile acids were significantly elevated. The results of this study indicated that serum clinical chemistries may be a useful antemortem diagnostic test for chronic hepatobiliary disease in hamsters.     

Characterization of photoreceptor cell types in the little brown bat Myotis lucifugus (Vespertilionidae)

We report the expression of three visual opsins in the retina of the little brown bat (Myotis lucifugus, Vespertilionidae). Gene sequences for a rod-specific opsin and two cone-specific opsins were cloned from cDNA derived from bat eyes. Comparative sequence analyses indicate that the two cone opsins correspond to an ultraviolet short-wavelength opsin (SWS1) and a long-wavelength opsin (LWS). Immunocytochemistry using antisera to visual opsins revealed that the little brown bat retina contains two types of cone photoreceptors within a rod-dominated background. However, unlike other mammalian photoreceptors, M. lucifugus cones and rods are morphologically indistinguishable by light microscopy. Both photoreceptor types have a thin, elongated outer segment. Using microspectrophotometry we classified the absorption spectrum for the ubiquitous rods. Similar to other mammals, bat rhodopsin has an absorption peak near 500 nm. Although we were unable to confirm a spectral range, cellular and molecular analyses indicate that M. lucifugus expresses two types of cone visual pigments located within the photoreceptor layer. This study provides important insights into the visual capacity of a nocturnal microchiropteran species.     

Functional maturation of the gonads of Turkish hamsters under various photoperiods

The golden hamster, Mesocricetus auratus, is the only photoperiodic rodent to date that has been shown to fail to respond to inhibitory (i.e., short, less than 12.5 h/day) photoperiods until after pubertal onset. In other photoperiodic hamsters, mice, and voles, short photoperiods greatly retard gonadal maturation. The Turkish hamster, Mesocricetus brandti, is a photoperiodic rodent that as an adult is reproductively competent only on photoperiods of 15-17 h of light per day; photoperiods of less than 15 or greater than 17 h of light promote gonadal regression. In this report we addressed two questions: a) are prepubertal M. brandti photoperiodic, and b) if so, is gonadal maturation enhanced or suppressed by exposure to photoperiods of greater than 17 h of light per day? Turkish hamsters were raised on photoperiods of 12, 16, 20, or 24 (= LL) h of light per day. Testicular growth was retarded for 16 wk by 12L:12D. Very long days, 20L:4D, or LL did not retard testicular development. In females, pubertal onset, as indicated by first vaginal estrus, was delayed in young raised on 12L:12D and in 2 of 18 and 4 of 19 young raised on 20L:4D and LL, respectively. These results demonstrate that prepubertal Turkish hamsters are photoperiodic, but respond differently from adults to photoperiods greater than 17 h of light per day.     

Regulation of phototransduction in short-wavelength cone visual pigments via the retinylidene Schiff base counterion.

Short-wavelength visual pigments (SWS1) have lambda(max) values that range from the ultraviolet to the blue. Like all visual pigments, this class has an 11-cis-retinal chromophore attached through a Schiff base linkage to a lysine residue of opsin apoprotein. We have characterized a series of site-specific mutants at a conserved acidic residue in transmembrane helix 3 in the Xenopus short-wavelength sensitive cone opsin (VCOP, lambda(max) approximately 427 nm). We report the identification of D108 as the counterion to the protonated retinylidene Schiff base. This residue regulates the pK(a) of the Schiff base and, neutralizing this charge, converts the violet sensitive pigment into one that absorbs maximally in the ultraviolet region. Changes to this position cause the pigment to exhibit two chromophore absorbance bands, a major band with a lambda(max) of approximately 352-372 nm and a minor, broad shoulder centered around 480 nm. The behavior of these two absorbance bands suggests that these represent unprotonated and protonated Schiff base forms of the pigment. The D108A mutant does not activate bovine rod transducin in the dark but has a significantly prolonged lifetime of the active MetaII state. The data suggest that in short-wavelength sensitive cone visual pigments, the counterion is necessary for the characteristic rapid production and decay of the active MetaII state.     

Alpha transducin is present in blue-, green-, and red-sensitive cone photoreceptors in the human retina

Phototransduction in vertebrate rod and cone photoreceptor cells involves G protein-mediated light stimulation of cGMP hydrolysis. Enzymes of the cGMP hydrolysis cascades of rods and cones are products of different genes. Three different classes of cones in the human retina are maximally sensitive to either blue, green, or red light. Distinct opsin genes are expressed in each type of cone. The distribution of cone types in human retina was determined using anti-peptide antibodies that recognize specific amino acid sequences in green/red opsin and blue opsin. These antibodies together with an anti-peptide antibody against Tc alpha were used in double labeling experiments to demonstrate the presence of the Tc alpha peptide in all types of cones. cDNA clones corresponding to human rod and cone transducin alpha subunit (Tr alpha and Tc alpha) genes were isolated. Southern blot analyses of human genomic DNA suggest that there is only one rod T alpha gene but more than one cone T alpha gene. The multiple Tc alpha genes could be closely related genes or different Tc alpha alleles, or one could be a pseudogene.     

Bat Eyes Have Ultraviolet-Sensitive Cone Photoreceptors

Mammalian retinae have rod photoreceptors for night vision and cone photoreceptors for daylight and colour vision. For colour discrimination, most mammals possess two cone populations with two visual pigments (opsins) that have absorption maxima at short wavelengths (blue or ultraviolet light) and long wavelengths (green or red light). Microchiropteran bats, which use echolocation to navigate and forage in complete darkness, have long been considered to have pure rod retinae. Here we use opsin immunohistochemistry to show that two phyllostomid microbats, Glossophaga soricina and Carollia perspicillata, possess a significant population of cones and express two cone opsins, a shortwave-sensitive (S) opsin and a longwave-sensitive (L) opsin. A substantial population of cones expresses S opsin exclusively, whereas the other cones mostly coexpress L and S opsin. S opsin gene analysis suggests ultraviolet (UV, wavelengths <400 nm) sensitivity, and corneal electroretinogram recordings reveal an elevated sensitivity to UV light which is mediated by an S cone visual pigment. Therefore bats have retained the ancestral UV tuning of the S cone pigment. We conclude that bats have the prerequisite for daylight vision, dichromatic colour vision, and UV vision. For bats, the UV-sensitive cones may be advantageous for visual orientation at twilight, predator avoidance, and detection of UV-reflecting flowers for those that feed on nectar.     

Isolation of Corynebacterium kutscheri from aged Syrian hamsters (Mesocricetus auratus).

Corynebacterium kutscheri was isolated from the oral cavities of 12 male Syrian hamsters (Mesocricetus auratus) which were about 12 months old. At 1, 5, and 9 months after initial isolation of C. kutscheri from the oral cavity, hamsters were euthanatized, and attempts were made to culture C. kutscheri from 13 additional sites. Corynebacterium kutscheri was isolated from nine hamsters, and regardless of the hamsters' ages, the organisms were most frequently isolated from the oral cavity (100%), esophagus (100%), cecal content (100%), and colon and rectum (88.9%). Isolation rates in the nasal cavity were 66.7%, followed by 55.5% in the trachea and 33.3% in the submaxillary lymph nodes. The number of the organisms found in the submaxillary lymph nodes and esophagus was 10(3) to 10(4) CFU/g. The number found in the cecal content and in the colon and rectum was 10(2) to 10(5) CFU/g. The organisms were not isolated from lung, stomach, kidney, spleen, and mesenteric lymph node tissues. The hamsters had neither clinical signs nor lesions. However, 7 of 12 animals had low agglutinating antibody titers. The Syrian hamster can therefore be an asymptomatic carrier of C. kutscheri.