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Oxygen consumption and carbon dioxide production in male prairie deermice (Peromyscus maniculatus bairdii) in different reproductive conditions and group densities.

Natural and laboratory populations of Peromyscus exhibit a profound but reversible reproductive inhibition related to population density. Our earlier studies described the endocrine physiology of inhibited animals which resembles a condition of delayed puberty, but they did not reveal a primary mechanism for the induction and maintenance of the inhibition. These studies indicated that reproductive inhibition could be associated with an overall change in general metabolism. To test this hypothesis, oxygen consumption (VO2) and carbon dioxide production (VCO2) were measured in three groups of Peromyscus maniculatus males that were: 1) reproductively-proven, 2) reproductively-inhibited, or 3) recovered from inhibition. We found that the mean of the 2-hr period with the lowest VO2 (the Resting Metabolic Rate, or RMR) was significantly lower, and the mean Respiratory Exchange Ratio (RER) was significantly higher in reproductively-inhibited males compared with reproductively-proven males. In addition, previously inhibited males allowed to recover reproductive function had a significantly higher mean VO2, while the mean RER was not different from reproductively-proven males. Moreover, and contrary to some studies with other species, increasing the ambient carbon dioxide concentration or the caging densities to as high as six animals did not significantly affect oxygen consumption when compared with the corresponding values for individuals. Taken together, these findings indicate that the reproductive inhibition observed in P. maniculatus laboratory populations is causally associated with a significant reduction in general metabolism and that this metabolic reduction which is associated with reproductive-inhibition is not induced by a CO2 signal or induced by absolute density, per se.

Animals↗

Genomic imprinting is disrupted in interspecific Peromyscus hybrids.

Genomic imprinting, the unequal expression of gene alleles on the basis of parent of origin, is a major exception to mendelian laws of inheritance. By maintaining one allele of a gene in a silent state, imprinted genes discard the advantages of diploidy, and for this reason the rationale for the evolution of imprinting has been debated. One explanation is the parent-offspring conflict model, which proposes that imprinting arose in polyandrous mammals as the result of a parental conflict over the allocation of maternal resources to embryos. This theory predicts that there should be no selection for imprinting in a monogamous species. Crosses between the monogamous rodent species Peromyscus polionotus and the polyandrous Peromyscus maniculatus yield progeny with parent-of-origin growth defects that could be explained if imprinting was absent in the monogamous species. We find, however, that imprinting is maintained in P. polionotus, but there is widespread disruption of imprinting in the hybrids. We suggest that the signals governing genomic imprinting are rapidly evolving and that disruptions in the process may contribute to mammalian speciation.

Animals↗

Comparison of the reservoir competence of medium-sized mammals and Peromyscus leucopus for Anaplasma phagocytophilum in Connecticut.

In the northeastern United States, Anaplasma phagocytophilum, the agent of human granulocytic ehrlichiosis (HGE), is transmitted by the tick vector Ixodes scapularis. The white-footed mouse Peromyscus leucopus is a competent reservoir for this agent, but the reservoir competence of non-Peromyscus hosts of I. scapularis has not been studied. Here, we report data confirming reservoir competence of medium-sized mammals for A. phagocytophilum. Raccoons, Virginia opossums, gray squirrels, and striped skunks were live-trapped in June-August of 1998-1999 at two locations in Connecticut. Captured animals were kept for several days at the laboratory in wire-mesh cages over water to allow naturally attached ticks to drop off. Samples of blood and serum were taken from each animal prior to its release at the site of capture. Engorged ticks collected from each animal were allowed to molt. Resulting I. scapularis nymphs and adults were tested for the presence of A. phagocytophilum DNA by polymerase chain reaction, as were the blood samples from the animals. A. phagocytophilum DNA was detected in the blood of >10% of the raccoons tested. Raccoons, opossums, squirrels, and skunks produced adult I. scapularis infected with the agent of HGE. Prevalence of infection was the highest in adult ticks fed as nymphs upon raccoons (23%) and the lowest in those fed upon skunks and opossums (5-7%). The agent was present in nymphal I. scapularis fed as larvae upon raccoons and squirrels, but not in ticks fed upon skunks or opossums. We also tested the ability of I. scapularis to transmit A. phagocytophilum to laboratory-reared white-footed mice after acquiring it from medium-sized mammals. Ticks that acquired the agent from raccoons and squirrels successfully transmitted it to mice. Thus, raccoons and gray squirrels are reservoir-competent for the agent of HGE-they become naturally infected, and are capable of transmitting the infection to feeding ticks.

Anaplasma phagocytophilum↗

Molecular evolution of two lineages of L1 (LINE-1) retrotransposons in the california mouse, Peromyscus californicus.

The large number of L1 [long interspersed elements (LINE)-1] sequences found in the genome is due to the insertion of copies of the retrotransposon over evolutionary time. The majority of copies appear to be replicates of a few active, or "master" templates. A continual replacement of master templates over time gives rise to lineages distinguishable by their own unique set of shared-sequence variants. A previous analysis of L1 sequences in deer mice, Peromyscus maniculatus and P. leucopus, revealed two active L1 lineages, marked by different rates of evolution, whose most recent common ancestor predates the expansion of the Peromyscus species. Here we exploit lineage-specific, shared-sequence variants to reveal a paucity of Lineage 2 sequences in at least one species, P. californicus. The dearth of Lineage 2 copies in P. californicus suggests that Lineage 2 may have been unproductive until after the most recent common ancestor of P. californicus and P. maniculatus. We also show that Lineage 1 appears to have a higher rate of evolution in P. maniculatus relative to either P. californicus or P. leucopus. As a phylogenetic tool, L1 lineage-specific variants support a close affinity between P. californicus and P. eremicus relative to the other species examined.

Animals↗

Evolution of MHC class II E beta diversity within the genus Peromyscus.

Progress in understanding the evolution of variation at the MHC has been slowed by an inability to assess the relative roles of mutation vs. intragenic recombination in contributing to observed polymorphism. Recent theoretical advances now permit a quantitative treatment of the problem, with the result that the amount of recombination is at least an order of magnitude greater than that of mutation in the history of class II genes. We suggest that this insight allows progress in evaluating the importance of other factors affecting the evolution of the MHC. We investigated the evolution of MHC class II E beta sequence diversity in the genus Peromyscus. We find evidence for extensive recombination in the history of these sequences. Nevertheless, it appears that intragenic recombination alone is insufficient to account for evolution of MHC diversity in Peromyscus. Significant differences in silent variation among subgenera arose over a relatively short period of time, with little subsequent change. We argue that these observations are consistent with the effects of historical population bottleneck(s). Population restrictions may explain general features of MHC evolution, including the large amount of recombination in the history of MHC genes, because intragenic recombination may efficiently regenerate allelic polymorphism following a population constriction.

Amino Acid Sequence↗

Systematic implications of chromosomal data from two insular species of Peromyscus from the Gulf of California.

G- and C-banded karyotypes for two insular species of deer mice, Peromyscus slevini and P. sejugis, are described and analyzed relative to the evolutionary relationship of these species to and their inclusion within the P. maniculatus species group. The chromosomal phenotype of P. slevini is unique among all banded karyotypes reported for Peromyscus, and comparison with published karyotypes suggests that P. slevini has systematic affinities with either the P. boylii or P. mexicanus species groups. The karyotypic data for P. sejugis clearly align these mice with P. maniculatus and provide a diagnostic character that supports the specific distinction between these taxa.

Animals↗

Genealogical concordance and the specific status of Peromyscus sejugis.

Peromyscus sejugis, a peripheral isolate of Peromyscus maniculatus, is a threatened taxon endemic to 2 small islands in the Sea of Cortés. Although its insularity makes the specific recognition of P. sejugis inherently problematic, resolution of this problem has important conservation implications. To evaluate the specific validity and evolutionary history of P. sejugis, we compared sequence variation (ND3/ND4L/ND4) in mtDNA for both island populations of P. sejugis with that for 8 populations of P. maniculatus from mainland Baja California. Each island population of P. sejugis had a single haplotype (0.7% sequence divergence), whereas 11 different haplotypes (mean sequence divergence = 0.68%) were obtained for the populations of P. maniculatus. The mean sequence divergence between the populations of the 2 species was 2.0%. Nested clade analysis supports the conclusion that P. sejugis is an insular isolate of P. maniculatus from mainland Baja California. Although our analysis confirms a low level of mtDNA divergence between P. sejugis and P. maniculatus from Baja California, the genealogical concordance of morphological, chromosomal, microsatellite, and mtDNA haplotype distinctiveness supports the conclusion that the 2 island populations of P. sejugis constitute independent evolutionarily significant units and together represent a phylogenetic species distinct from the P. maniculatus from Baja California.

Animals↗

Mys retrotransposons in Peromyscus leucopus and transgenic Mus musculus.

The mys family of retrotransposons exhibits an interesting phylogenetic distribution with 500-1000 copies per haploid genome in the white-footed mouse Peromyscus leucopus and no copies detectable in the house mouse Mus musculus, even though most other repeated sequences are shared by these two species. Comparison of the DNA sequences from the 3' ends of five mys elements show that insertion occurs just upstream of a well-conserved 11 bp target sequence. Transcription patterns of the elements in brain, liver, heart, kidneys and gonads in Peromyscus leucopus are analyzed. Transcripts are found in all tissues examined, but they are remarkably heterogeneous in size. When four cloned elements are introduced into transgenic Mus musculus, however, discrete patterns of expression are revealed. Furthermore, a study of the structure of the concatemers of mys elements in the transgenic mice demonstrates that recircularization of injected linear molecules is an important event in concatemer generation.

Animals↗

Coat color genetics of Peromyscus: III. Golden-nugget--a recessive trait in the white-footed mouse, P. leucopus.

A novel pelage color variant appeared in a laboratory colony of white-footed mice (Peromyscus leucopus) from Massachusetts. The mature adult coat color of this variant exhibits a rich golden tan appearance on the dorsum with white underparts. The trait is inherited as an autosomal recessive. Phenotypic comparisons with other rodents suggest that the trait is attributable to an allele at the brown (b) locus. Under laboratory conditions homozygous or heterozygous golden-nugget Peromyscus do not differ significantly from the wild type in litter size, litter survival, nest defense, or body weight. The possibility that the allele confers some adaptive value in nature is considered. The trait is given the tentative designation bgn (golden-nugget).

Animals↗

Geographic differences for delay of sexual maturation in Peromyscus leucopus: effects of photoperiod, pinealectomy, and melatonin.

Effects of short-day photoperiod, pinealectomy, and melatonin on sexual maturation were tested in Peromyscus leucopus from either Connecticut (CT) or Georgia (GA). Laboratory reared-stocks from CT and GA were exposed to short daylength (photoperiod) from birth or 25 days of age. At 12 wk of age, delay in sexual maturation was indicated in most CT mice by decreased testis length, combined testes weight, and seminal vesicle weight. Conversely, GA animals did not delay sexual maturation when exposed to short-day photoperiod from either birth or 25 days of age. These results indicate that responses to short daylengths differ for juvenile CT and GA populations. In a second experiment, pinealectomized or sham-operated CT males were exposed to short-day (9L:15D) or long-day (16L:8D) photoperiod from birth. Pinealectomy blocked the effect of short daylength on reproduction. Therefore, the pineal must be involved in the delay of sexual maturation observed for short-day CT mice. The effects of melatonin, a pineal gland hormone, were tested with chronic s.c. implants or daily injections. In CT mice given either melatonin implants or afternoon injections, sexual maturation was delayed. GA mice were insensitive to all melatonin treatments. Further, no differences in circadian organization (phase angle, duration of activity, period under constant dark) between GA and CT animals were apparent. Collectively, these studies indicate that melatonin is involved in the mechanism responsible for delay of sexual maturation in CT mice. Short-day insensitivity of GA Peromyscus leucopus probably results from a deficiency in the melatonin effector pathway and is not due to a disruption of circadian organization.

Animals↗

Social, but not photoperiodic, influences on reproductive function in male Peromyscus aztecus.

Nontropical rodents rely on environmental factors to restrict breeding to a specific time of the year. Among these factors, photoperiod appears to be the primary environmental cue used for predicting optimal breeding conditions. The purpose of the present study was to characterize reproductive function, as well as photoperiodic and social responsiveness in male Peromyscus aztecus, which occupy low-latitude, high-altitude habitats. In experiment 1, adult male P. aztecus were individually housed in either long (16L:8D) or short days (8L:16D) for 10 wk. Short-day mice did not differ from long-day mice on any reproductive or nonreproductive parameter. Comparisons to related Peromyscus species suggested that relative reproductive organ size and function were reduced in both long- and short-day males. Because ad libitum food and water were available, we reasoned that males in both photoperiodic conditions lacked social stimuli. To test this hypothesis, adult male P. aztecus were housed in long days either individually or with a female conspecific in experiment 2. Mice housed with females had significantly larger relative paired testes and epididymal masses, and higher testicular sperm counts and serum testosterone levels compared to those of individually housed mice. Taken together, these results suggest that social factors may play a more prominent role than photoperiod in stimulating reproductive development in laboratory-housed P. aztecus. These results are consistent with the results found for other low-latitude rodent species and suggest that P. aztecus uses a flexible rather than obligatory breeding strategy.

Animals↗

Natural selection on protein polymorphism in the rodent genus Peromyscus: evidence from interlocus contrasts.

The effects of natural selection are generally locus-specific, whereas migration, drift, and inbreeding are expected to have relatively uniform effects across the entire genome. This suggests that multilocus surveys of multiple populations can be used to distinguish selection from demographic effects. The purpose of this study was to test for evidence of selection on protein polymorphism in natural populations of mice in the genus Peromyscus. We analyzed published data from geographic surveys of allozyme variation and used a coalescent-based simulation model to identify specific loci that deviated from neutral expectations. Observed F(ST) values generally exhibited a remarkably close fit to the expected neutral distributions, indicating that the majority of loci are simply tracking stochastic demographic processes. A smaller number of loci exhibited highly significant departures from the expectations of the neutral model and thus appear to be tracking the direct or indirect effects of selection. Most departures from neutrality were characterized by F(ST) values that far exceeded neutral expectations and were therefore attributable to spatially varying selection. Interestingly, the albumin locus was implicated as a candidate gene for local adaptation in four different species of Peromyscus. The results also demonstrate that selection can severely bias marker-based estimates of neutral parameters.

Adaptation, Physiological↗

Nonshivering thermogenesis in skeletal muscle of seasonally acclimatized mice, Peromyscus.

Nonshivering thermogenesis (NST) is a major contributor to total heat production capabilities of Peromyscus and the magnitude of the NST response increases dramatically in winter-acclimatized animals. To directly assess the contribution from skeletal muscle to this NST, a hindlimb perfusion system was developed for Peromyscus. Oxygen consumption was then measured with and without norepinephrine (the mediator of NST) in freshly captured animals in summer and winter. Norepinephrine (NE) was infused at 0.001, 0.01, and 0.1 micrograms . g hindlimb muscle-1 . min-1. Vascular resistance (VR), calculated as arterial pressure divided by flow rate, increased during all NE infusions. At doses of 0.001 and 0.01, VR stabilized after approximately 10 min, but at 0.1 VR continued to rise. Resting oxygen consumption was 0.817 +/- 0.037 and 0.805 +/- 0.049 mumol O2 . g-1 . min-1 in summer (n = 8) and winter (n = 7) animals, respectively. There was no apparent increase in oxygen consumption with any dosage of NE. It appears that the increase in NST in winter animals is not due to an increased NST in skeletal muscle.

Acclimatization↗

Capillary supply of skeletal muscles from acclimatized white-footed mice Peromyscus.

Winter-acclimatized white-footed mice (Peromyscus leucopus) can increase their aerobic heat production under cold stress by 70%. The possibility that changes in microvascular supply might account, in part, for some of this increased thermogenic capacity was examined in one of the primary thermogenic tissues, skeletal muscle. Capillaries were stained histochemically in four hindlimb muscles of freshly captured Peromyscus in summer and winter. Capillary density, mean fiber area, and mean capillaries in contact per muscle fiber were obtained from the soleus, plantaris, gastrocnemius, and semitendinosus. If results from all individual muscles are combined, mean fiber area is significantly smaller (8%) and mean capillary density is significantly greater (40%) in winter muscles. The mean number of capillaries in contact is not different, but the mean ratio of capillaries in contact per mean fiber area (index of potential perfusion) is significantly greater (25%) in winter muscles.

Acclimatization↗

Sex differences in immunocompetence differ between two Peromyscus species.

Males generally exhibit reduced immunocompetence and greater susceptibility to disease than females. The explanations for why males may be more susceptible to disease than females fall into two categories: 1) the proximate mechanisms mediating immunity, such as hormonal mechanisms, and 2) variation in reproductive success between the sexes. The present study examined the extent to which these factors contribute to sex differences in cell-mediated immune function in polygynous Peromyscus maniculatus and monogamous Peromyscus californicus. Prevailing hypotheses suggest that, because variation in male and female reproductive success is greater among polygynous than monogamous species, sex differences in immunocompetence should be greater among polygynous than monogamous species as well. In contrast to these predictions, sex differences in cell-mediated immunity and body mass were only observed among monogamous P. californicus, in which females exhibited higher splenocyte proliferation in response to the T cell mitogen, concanavalin A, and weighed less than male conspecifics. Male P. maniculatus had higher serum testosterone concentrations than male P. californicus, but females of the two species did not differ in circulating estradiol concentrations. Sex steroid concentrations were not correlated with either immunocompetence or body mass; however, large P. californicus males exhibited reduced immune responses. Taken together, these results do not support the hypothesis that sex differences in immunocompetence are more pronounced among polygynous compared with monogamous species. Furthermore, these data suggest that circulating testosterone does not mediate sex differences in immuno-competence or body mass in P. californicus.

Animals↗

Synaptic adjustment in Peromyscus beatae (Rodentia: Cricetidae) heterozygous for interstitial heterochromatin.

Chromosomal pairing and chiasma formation were studied two individuals of Peromyscus beatae heterozygous for the presence of a large block of interstitial heterochromatin. Although the modified chromosome was of medium size, analysis of C-banded diakinetic configurations revealed that it was the homolog of one of the smallest autosomes. Analysis of silver stained synaptonemal complexes indicated that synapsis was either unidirectional from initiation at one set of telomeres or was bidirectional from initiation at both sets of telomeres. Each pattern resulted in characteristic heteromorphic pairing configurations (interstitial asynapsis or terminally positioned unpaired segments) in early pachynema. These configurations underwent synaptic adjustment and, by mid-pachynema, the lateral elements of the polymorphic bivalent either appeared typical of homomorphic bivalents or exhibited regional heteropycnosis in one or both axes. Synaptonemal complex data for Peromyscus and many other mammalian species reflect an apparent need for fully paired, linear bivalents prior to the end of pachynema.

Animals↗

Unusual patterns of susceptibility to degradation of DNA isolated from tissues in Peromyscus californicus.

Isolation of intact, high molecular weight genomic DNA from the livers of 2 subspecies of Peromyscus californicus without excessive degradation was typically unattainable, whereas highly intact DNA from livers of other Peromyscus (field mice) species is invariably obtained using the same isolation methods. Additionally, highly intact DNA was obtained from splenic tissues of adult P. californicus and hepatic tissue of juvenile animals, indicating that the phenomenon is tissue-specific and age-related.

Animals↗

Genetic diversity and distribution of Peromyscus-borne hantaviruses in North America.

The 1993 outbreak of hantavirus pulmonary syndrome (HPS) in the southwestern United States was associated with Sin Nombre virus, a rodent-borne hantavirus; The virus' primary reservoir is the deer mouse (Peromyscus maniculatus). Hantavirus-infected rodents were identified in various regions of North America. An extensive nucleotide sequence database of an 139 bp fragment amplified from virus M genomic segments was generated. Phylogenetic analysis confirmed that SNV-like hantaviruses are widely distributed in Peromyscus species rodents throughout North America. Classic SNV is the major cause of HPS in North America, but other Peromyscine-borne hantaviruses, e.g., New York and Monongahela viruses, are also associated with HPS cases. Although genetically diverse, SNV-like viruses have slowly coevolved with their rodent hosts. We show that the genetic relationships of hantaviruses in the Americas are complex, most likely as a result of the rapid radiation and speciation of New World sigmodontine rodents and occasional virus-host switching events.

Animals↗