Suppressed breeding in the field vole (Microtus agrestis): an adaptation to cyclically fluctuating predation risk

The densities of microtine rodents and their main predators,small mustelids, fluctuate synchronously in 3–5-year cyclesin central and northern Fennoscandia. Predation by small mustelidshas been suggested as one of the driving forces in microtinecyclicity, causing deep synchronous declines of several volespecies. We studied experimentally the effects of small mustelidson mating behavior, foraging, and breeding in nonwintered fieldvoles (Microtus agrestis) originating from a cyclic population.By using mustelid odors, we simulated a crash phase environmentwith high predation risk for breeding pairs of voles. In ourexperiments, 87% of the female field voles suppressed breedingwhen exposed to mustelid odors. Both female and male behaviorchanged, and no mating behaviors were observed under the simulatedpredation risk. Weights of both sexes decreased when exposedto mustelid odor, probably due to decreased foraging; weightsof the control females increased due to pregnancy; and no weightchanges occurred in control males. Decreased breeding and foragingpossibilities under high predation pressure may form the basisfor the ultimate explanation for breeding suppression. Thereare at least two different mechanisms for breeding suppression:either mating does not take place or malnutrition in femalesdoes not' allow breeding to occur. Delayed breeding under highrisk of predation, for whatever reason, could increase the probabilityof individuals, especially that of the females, to survive overthe crash to the next, safer breeding season when their youngwould have better possibilities to survive.     

Summer acclimatization in the short-tailed field vole,Microtus agrestis

We investigated the changes that occurred in basal and noradrenaline-induced metabolic rate, body temperature and body mass in short-tailed field voles,Microtus agrestis, during exposure to naturally increasing photoperiod and ambient temperature. These parameters were first measured in winter-acclimatized voles (n=8) and then in the same voles which had been allowed to seasonally acclimatize to photoperiod and ambient temperature (6 months later). Noradrenaline induced metabolic rate, basal metabolic rate and nonshivering thermogenesis were significantly higher in winter-acclimatized compared to summer-acclimatized voles. There was a significant positive relationship between basal metabolic rate and noradrenaline-induced metabolic rate. Body mass was significantly higher in summer-acclimatized compared to winter-acclimatized voles. There was a significant positive relationship between body mass and noradrenaline-induced metabolic rate in both winter-acclimalized and summer-acclimatized voles; however, there was no relationship between basal metabolic rate and body mass in either seasonal group of voles. Body temperature after measurements of basal metabolic rate was not significantly different in the seasonal cohorts of voles. However, body temperature was significantly higher in winter-acclimatized compared to summer-acclimatized voles after injection of noradrenaline. Previously we have found that a long photoperiod was not a sufficient stimulus to reduce thermogenic capacity in winter-acclimatized voles during cold exposure, since basal metabolic rate increased to compensate for a reduction in regulatory nonshivering thermogenesis. Here we found that a combination of increased ambient temperature and photoperiod did significantly reduce thermogenic capacity in winter-acclimatized voles. This provided evidence that the two aspects of non-shivering thermogenesis, obligatory and regulatory, are stimulated by different exogenous cues. Summer acclimatization in the shorttailed field vole is manifest as a significant decrease in both basal and noradrenaline-induced metabolic rate, combined with a significant increase in body mass.Abbreviations ANCOV A analysis of covariance - BAT brown adipose tissue - BM body mass - BMR basal metabolic rate - NST non-shivering thermogenesis - NA noradrenaline - V the maximum V recorded following mass specific injection of noradrenaline - V the maximum V recorded following mass specific injection of saline - T _a ambient temperature - T _b rectal body temperature - T _1c lower critical temperature - UCP uncoupling protein - V oxygen consumption     

Evidence for selection at cytokine loci in a natural population of field voles (Microtus agrestis)

Individuals in natural populations are frequently exposed to a wide range of pathogens. Given the diverse profile of gene products involved in responses to different types of pathogen, this potentially results in complex pathogen-specific selection pressures acting on a broad spectrum of immune system genes in wild animals. Thus far, studies into the evolution of immune genes in natural populations have focused almost exclusively on the Major Histocompatibility Complex (MHC). However, the MHC represents only a fraction of the immune system and there is a need to broaden research in wild species to include other immune genes. Here, we examine the evidence for natural selection in a range of non-MHC genes in a natural population of field voles (Microtus agrestis). We concentrate primarily on genes encoding cytokines, signalling molecules critical in eliciting and mediating immune responses and identify signatures of natural selection acting on several of these genes. In particular, genetic diversity within Interleukin 1 beta and Interleukin 2 appears to have been maintained through balancing selection. Taken together with previous findings that polymorphism within these genes is associated with variation in resistance to multiple pathogens, this suggests that pathogen-mediated selection may be an important force driving genetic diversity at cytokine loci in voles and other natural populations. These results also suggest that, along with the MHC, preservation of genetic variation within cytokine genes should be a priority for the conservation genetics of threatened wildlife populations.     

Seasonal variation of reproductive success under female philopatry and male-biased dispersal in a common vole population

Variation of reproductive success, an important determinant of the opportunity for sexual selection, is an outcome of competition within one sex for mating with members of the other sex. In promiscuous species, males typically compete for access to females, and their reproductive strategies are strongly related to the spatial distribution of females. I used 10 microsatellite loci and the mtDNA control region to determine seasonal differences in the reproductive success of males and females of the common vole (Microtus arvalis), one of the most numerous mammals in Europe. The sex-related spatial structure and bias in dispersal between genders were also assessed. Standardized variance of the reproductive success of females did not vary seasonally due to the continuity of female philopatry throughout the breeding season and to the constancy of the number of females reproducing successfully in each season. The males are the dispersing sex, undergoing both natal and breeding dispersal. Their standardized variance of reproductive success was significantly higher than that for females in July, when only two males monopolized 80% of the females in the population and when variance of male reproductive success was highest (I_m = 7.70). The seasonally varying and high standardized variance of male reproductive success may be explained by male-male competition for matings, coupled with seasonal changes in the age structure of the population.     

A shift in female social organization independent of relatedness: an experimental study on the field vole (Microtus agrestis)

Home range size, overlap between home ranges, movement patternsand social behavior in two generations of female field voleswere examined by radio tracking unrelated individuals in enclosedareas. In addition, potential effects of increased relatednesswere examined by comparing setups with groups of sisters andunrelated females. Overwintered females showed less overlapbetween ranges and moved shorter and more irregular distancescompared with females of the year. Based on responses to introduced,unfamiliar conspecifics it was concluded that the overdisperseddistribution of overwintered females was maintained primarilyby avoidance behavior and that infanticidal behavior was equallyfrequent in the two generations. Observed differences betweengenerations could not be ascribed to differences in relatedness,and experimental increase of the degree of relatedness had negligibleeffects. The overdispersion and restricted movements shown byoverwintered females are instead suggested to be caused by acombination of low food availability and exposure to intensepredation in spring/early summer, whereas spacing and movementpatterns of females of the year are less influenced by thesefactors. As aggressive interactions are rare and populationdensity is usually low in spring, it is unlikely that breedingdensity and population growth is restrained by the social behaviorof overwintered females.     

Isolation and characterization of polymorphic microsatellite loci in the field vole,Microtus agrestis,and their cross‐utility in the common vole,Microtus arvalis

We developed nine polymorphic microsatellite loci for the field vole, Microtus agrestis. The number of alleles ranged from five to 15 and observed heterozygosities ranged from 0.40 to 1.00. We also tested the microsatellite loci for amplification and polymorphism in the congeneric species Microtus arvalis. Five of the nine loci were successfully analysed in this species. The microsatellite markers will be employed in studies of reproductive success and fine‐scale spatial genetic structure.     

Philopatry, kin clusters, and genetic relatedness in a population of woodrats (Neotoma macrotis)

Studies of highly kin-structured mammal societies have revealedthe importance of natal philopatry in determining the distributionof genetic variation within populations. In comparison, therelationship between philopatry and genetic diversity withinpopulations of moderately kin-structured societies has receivedrelatively little attention. Previous studies of Neotoma macrotishave suggested that females form distinct kin clusters. Eachkin cluster overlaps spatially with the home range(s) of oneor more males that are not related to each other or to the femaleswith which they are spatially associated. To examine interactionsbetween philopatry and genetic structure in this apparentlymoderately kin-structured species, we characterized spatialand genetic relationships among individually marked femalesin a population of N. macrotis from central coastal California.Our field studies revealed that, contrary to expectation, femalesin this population were not strongly philopatric and spatiallyclustered females were not characterized by high levels of geneticrelatedness. Nevertheless, genetic structure was evident withinthe study population; spatial and genetic distances among femaleswere significantly correlated, suggesting that dispersal patternsinfluenced genetic structure even in the absence of marked femalephilopatry. Because females with overlapping spatial distributionswere not typically closely related to one another, opportunitiesfor the evolution of kin-selected social behavior (e.g., cooperativecare of young) appear to be limited in this population.     

Apoptosis distribution in the first molar tooth germ of the field vole (Microtus agrestis)

Apoptosis represents an important process in organ and tissue morphogenesis and remodeling during embryonic development. A role for apoptosis in shape formation of developing teeth has been suggested. The field vole is a useful model for comparative studies in odontogenesis, particularly because of its contrasting molar morphogenesis when compared to the mouse. However, little is known concerning apoptosis in tooth development of this species. Morphological (cellular and nuclear alterations) and biochemical (specific DNA breaks--TUNEL staining) characteristics of apoptotic cells were used to evaluate the temporal and spatial occurrence of apoptosis in epithelial and mesenchymal tissues of the developing first molar tooth germs of the field vole. Apoptotic cells were found in non-proliferating areas (identified previously) throughout bud to bell stages, particularly in the epithelium, however, scattered also in the mesenchyme. A high concentration of TUNEL positive cells was evident in primary enamel knots at late bud stage with increasing density of apoptotic cells until ED 16 when the primary enamel knot in the field vole disappears and mesenchyme becomes protruded in the middle axes of the bell forming two shallow areas with zig-zag located secondary enamel knots. Distribution of TUNEL positive cells corresponded with localisation of secondary enamel knots as shown using histological and 3D analysis. Apoptosis was shown to be involved in the first molar development of the field vole, however, exact mechanisms and roles of this process in tooth morphogenesis require further investigation.     

Polymorphic microsatellite loci and PCR multiplexing in the common vole,Microtus arvalis

We isolated and characterized 14 dinucleotide microsatellite loci in the common vole Microtus arvalis (Palas). Two multiplex panels both comprising seven loci were developed. Application to a set of 21 individuals allowed clear and easy characterization of allele sizes except for two loci which were then withdrawn from further analyses. The number of alleles ranged from four to 19 per locus with the observed heterozygosity ranging from 0.55 to 0.95. These sets of microsatellite loci provide high throughput capacity for population genetic studies at a minimum cost.     

橙腹田鼠中延缓性密度依赖效应和种群波动

检验了延迟的密度依赖对橙腹田鼠 (Microtusochrogaster)一个波动种群的生存和生殖的影响 ,研究持续了 63个月 ,取样间隔为 3 5天。在研究期间 ,该种群的密度经历了 4次波动 ,每次波动的高峰都在 11月至次年 1月 ,种群数量在冬季下降。生存和生殖都有负面的密度依赖效应 ,最大效应具有 2个月的时滞。种群存活率增长对种群密度最大的正面效应具有 2个月的时滞 ,而对与增加生殖则有 3个月的时滞。内部因素和冬季都可能推延对生殖的密度依赖效应 ,但是本文未能检验这些内部因素的影响。季节性影响看来与对生存的延缓性密度依赖效应无关。负面的延缓性密度依赖效应对生存和生殖的净作用可能在于减少、而不是阻止橙腹田鼠种群波动的幅度     

Natal dispersal in relation to population density and sex ratio in the field vole,Microtus agrestis

Summary In a sample of 240 juvenile field voles 8% of the males and 22% of the females reached sexual maturity within their natal home range. Among individuals retrapped as adults, 58% of males and 23% of females had dispersed, i.e. had moved more than one home range diameter. The mean distance moved for males (58.5 m) exceeded that for females (28.6 m). Male movement distances were negatively associated with total density, and with density of adult females, but not with male density. Female movements were not related to population density. There were no relation between sex ratio and distance moved. The distribution of distances moved for both males and females fit a geometrical distribution, suggesting the importance of competitive processes.     

Burying beetles: intraspecific interactions and reproductive success in the field

Abstract. 1. The discovery and utilization of small carcasses by burying beetles (Silphidae, Nicrophorus ) was studied by placing dead mice at random points on large grids at two Iocations in Michigan, U.S.A.
2. The majority of mice are found within 24 h by more beetles than ultimately will utilize the carcass. If a carcass is likely to be usurped by a larger species of beetle or by a vertebrate, then intraspecific competition may be postponed until the carcass is concealed and buried.
3. Both males and females practice parental care. Maturing broods are tended by no adults, a single female, a single male, or a male—female pair. No differences in brood success were observed among these categories.
4. The female lays a larger clutch than ultimately will survive. Brood size is regulated after the egg stage, such that offspring number varies, but individual offspring size does not.
5. A large amount of unexplained variation exists in brood size, in both the laboratory and the field. This variation is probably caused by the environment, and not the reproductive physiology of the beetles. Competition with microbes is a likely candidate.
6. Differences exist not only between Nicrophorus species, but also between localities for a single species, suggesting adaptation to local environments.     

棕色田鼠与沼泽田鼠犁鼻器和副嗅球的组织结构

用组织学方法研究了棕色田鼠(Microtus mandarinus)、沼泽田鼠(M．fastis)副嗅球和犁鼻器的结构及其在两种鼠间的差异，以此探讨两种田鼠的进化机制与适应功能。两种田鼠的犁鼻器位于鼻腔前端鼻中隔基部的两侧，呈管状结构；沿着犁鼻器的长轴犁鼻管呈现不同的形态学特征，犁鼻管直接开口于鼻腔，从前向后沿着长轴旋转，中间管壁(犁鼻粘膜)变成底部，侧面管壁(假覆层上皮)变成犁鼻管顶壁，最终犁鼻管变小成为一个腺体的分支，不同部位具有不同的组织学特征。通过选取中间相似部位对两种田鼠进行比较研究，发现棕色田鼠犁鼻粘膜比沼泽田鼠厚，而其长度却短于沼泽田鼠。棕色田鼠副嗅球颗粒细胞带宽和僧帽细胞带宽均大于沼泽田鼠，而带长却小于沼泽田鼠。相关分析发现，犁鼻器和副嗅球形态有一定的对应关系，这可能和两个结构之间存在着神经投射有关。棕色田鼠幼体的犁鼻粘膜、神经细胞核、假覆层上皮、血管面积均小于成体[动物学报49(2)：248—255，2003]。     

Adult philopatry and dispersal in the field vol Microtus agrestis

Summary Using mark-recapture data, we related the movements of adult field voles to population density, sex ratio and population growth. Dispersal movements (defined as distances larger than 1 home range diameter) were few in both sexes; 4 out of 197 (2.0%) in males and 8 of 316 (2.5%) in females. The distance moved between sequential trapping periods was similar for males and females; the mean being 10.2 m and 9.0 m respectively. Both males and females moved larger distances during the breeding season than during the nonbreeding period. The distance moved between sequential trapping periods showed a strong negative relation to density, i.e. both sexes moved shorter distances at higher densities, but there were no differences between periods of increasing and declining population densities. These results contradict the dispersal predictions of all major hypotheses proposed to explain population fluctuations in small mammals. The dispersal patterns fit a geometric distribution, suggesting that competition is the primary factor determining the dispersal characteristics of this population.