Sex differences and effects of neonatal aromatase inhibition on masculine and feminine copulatory potentials in prairie voles

Copulatory behaviors in most rodents are highly sexually dimorphic, even when circulating hormones are equated between the sexes. Prairie voles (Microtus ochrogaster) are monomorphic in their display of some social behaviors, including partner preferences and parenting, but differences between the sexes in their masculine and feminine copulatory behavior potentials have not been studied in detail. Furthermore, the role of neonatal aromatization of testosterone to estradiol on the development of prairie vole sexual behavior potentials or their brain is unknown. To address these issues, prairie vole pups were injected daily for the first week after birth with 0.5 mg of the aromatase inhibitor 1,4,6-androstatriene-3,17-dione (ATD) or oil. Masculine and feminine copulatory behaviors in response to testosterone or estradiol were later examined in both sexes. Males and females showed high mounting and thrusting in response to testosterone, but only males reliably showed ejaculatory behavior. Conversely, males never showed feminine copulatory behaviors in response to estradiol. Sex differences in these behaviors were not affected by neonatal ATD, but ATD-treated females received fewer mounts and thrusts than controls, possibly indicating reduced attractiveness to males. In other groups of subjects, neonatal ATD demasculinized males' tyrosine hydroxylase expression in the anteroventral periventricular preoptic area, and estrogen receptor alpha expression in the medial preoptic area. Thus, although sexual behavior in both sexes of prairie voles is highly masculinized, aromatase during neonatal life is necessary only for females' femininity. Furthermore, copulatory behavior potentials and at least some aspects of brain development in male prairie voles are dissociable by their requirement for neonatal aromatase.     

Limits to food intake and fiber utilization in the prairie vole,Microtus ochrogaster: effects of food quality and energy need

We fed prairie voles (Microtus ochrogaster) rat chow diluted with variable amounts of -cellulose to determine 1) how much fiber the voles could tolerate in their diet; 2) changes in food intake and digestibility of dry matter and of fiber; 3) the extent to which voles utilized fiber as an energy source; and 4) whether any of these variables differed between groups of animals maintained at 5 or 22°C. Fiber content of the diets ranged from 20 to 84%. Animals held at 5°C maintained body mass through a diet containing 69% fiber, while animals held at 22°C maintained body mass through the 84% fiber diet. Dry matter intake increased with fiber level from 9.3 to 15.0 g·day^-1 for animals at 5°C and from 5.6 to 14.0 g·day^-1 for animals at 22°C; intake on the highest fiber diet eaten by either group was not different. Dry matter digestibility decreased significantly as the fiber in the diets increased, but was not affected by temperature treatments. Digestible dry matter intake for each group remained constant regardless of diet quality, but on each diet digestible dry matter intake for animals at 5°C was significantly higher than that of the animals held at 22°C. Digestibility of the fiber portion of the experimental diets remained constant as food quality decreased, so the percent of daily energy need met by fiber utilization increased with higher food intake. On the lowest quality diet each group tolerated, fiber digestion provided approximately 42 and 68% of the energy needs of voles at 5 and 22°C, respectively.Abbreviations BM body mass - BMR basal metabolic rate - DE digestible energy - DM dry matter - DMD dry matter digestibility - DDMI digestible dry matter intake - MR metabolic rate - NDF neutral detergent fiber (=cell walls) - NDS neutral detergent solubles (=cell solubles) - SEM standard error of mean - T _a ambient temperature     

avpr1a length polymorphism is not associated with either social or genetic monogamy in free-living prairie voles

Recent discoveries of single-gene influences on social behaviour have generated a great deal of interest in the proximate mechanisms underlying the expression of complex behaviours. Length polymorphism in a microsatellite in the regulatory region of the gene encoding the vasopressin 1a receptor (avpr1a) has been associated with both inter- and intra-specific variation in socially monogamous behaviour in voles (genus Microtus) under laboratory conditions. Here, we evaluate the relationship between avpr1a length polymorphism and social associations, genetic monogamy, and reproductive success in free-living prairie vole (M. ochrogaster) populations. We found no evidence of a relationship between avpr1a microsatellite length and any of our correlates of either social or genetic monogamy in the field. Our results, especially when taken in conjunction with those of recent experimental studies in semi-natural enclosures, suggest that avpr1a polymorphism is unlikely to have been a major influence in the evolution or maintenance of social monogamy in prairie voles under natural conditions.     

Sex and age-specific differences in ultraviolet reflectance of scent marks of bank voles (Clethrionomys glareolus)

Scent markings of voles are visible via their ultraviolet reflection. Kestrels, and possibly other diurnal raptors, may use this property when hunting. We performed a laboratory study on bank voles to determine whether UV-reflectance of scent marks differs in relation to sex, age and social status. When reflectance spectra of scent marks were measured with a spectroradiometer, we found UV reflectance to be strongest in mature males. There were no differences between mature females and immature juveniles, nor between sexes in juveniles or mature and immature individuals in females. Moreover, we did not find any difference in UV reflectance between dominant and subordinate mature males. The results of this study support earlier findings that UV sensitive predators may use UV reflectance of scent marks as a prey cue. Consequently, studies on differing vulnerability of voles to avian predators should take into account not only their space use and behaviour but also the UV reflectance of their scent marks. Accepted: 21 August 1999     

Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences

Voles of the genus Microtus represent one of the most speciose mammalian genera in the Holarctic. We established a molecular phylogeny for Microtus to resolve contentious issues of systematic relationships and evolutionary history in this genus. A total of 81 specimens representing ten Microtus species endemic to Europe as well as eight Eurasian, six Asian and one Holarctic species were sequenced for the entire cytochrome b gene (1140 bp). A further 25 sequences were retrieved from GenBank, providing data on an additional 23, mainly Nearctic, Microtus species. Phylogenetic analysis of these 48 species generated four well-supported monophyletic lineages. The genus Chionomys, snow voles, formed a distinct and well-supported lineage separate from the genus Microtus. The subgenus Microtus formed the strongest supported lineage with two sublineages displaying a close relationship between the arvalis species group (common voles) and the socialis species group (social voles). Monophyly of the Palearctic pitymyid voles, subgenus Terricola, was supported, and this subgenus was also subdivided into two monophyletic species groups. Together, these groupings clarify long-standing taxonomic uncertainties in Microtus. In addition, the "Asian" and the Nearctic lineages reported previously were identified although the latter group was not supported. However, relationships among the main Microtus branches were not resolved, suggesting a rapid and potentially simultaneous radiation of a widespread ancestor early in the history of the genus. This and subsequent radiations discernible in the cytochrome b phylogeny, show the considerable potential of Microtus for analysis of historical and ecological determinants of speciation in small mammals. It is evident that speciation is an ongoing process in the genus and that the molecular data provides a vital insight into current species limits as well as cladogenic events of the past.     

Determinants of reproductive success in voles: space use in relation to food and litter size manipulation

Spacing behaviour of female mammals is suggested to depend on the distribution and abundance of food. In addition, food limitation has been found to constrain the reproductive success of females. However, whether females maximize their reproductive success by adjusting space use in relation to current food availability and reproductive effort (e.g. litter size) has not been experimentally studied. We examined these questions by manipulating simultaneously food resources (control vs. food supplementation) and litter sizes (control vs. plus two pups) of territorial female bank voles (Clethrionomys glareolus) in large outdoor enclosures. Females with supplementary food had smaller home ranges (foraging area) and home range overlaps than control females, whereas litter size manipulation had no effect on space use. In contrast, the size of territory (exclusive area) was not affected by food supplementation or litter size manipulation. As we have previously shown elsewhere, extra food increases the reproductive success of bank vole females in terms of size and proportion of weaned offspring. According to the present data, greater overlap of female home ranges had a negative effect on reproductive success of females, particularly on survival of offspring. We conclude that higher food availability increases the reproductive success of bank vole females, and this effect may be mediated through lower vulnerability of offspring to direct killing and/or detrimental effects from other females in the population. Moreover, it seems that when density of conspecifics is controlled for, home range sizes of females, but not territoriality, is related to food resources in Clethrionomys voles.     

The cost of habitat selection in prairie voles: an empirical assessment using isodar analysis

The ideal free distribution assumes that habitat selection is without cost and predicts that fitness should be equal in different habitats. If habitat selection has a cost, then individuals should only move to another habitat when potential fitness in the new habitat exceeds that in the source habitat by an amount greater than the cost of habitat selection. We used isodar techniques to assess the cost of habitat selection. In an experimental landscape, we monitored density, movement, and reproductive success of adult female prairie voles, Microtus ochrogaster, in adjacent paired habitats with low and high cover. We tested the following hypotheses: (1) adult female prairie voles exhibited density-dependent habitat selection; (2) the cost of habitat selection was density-independent. Habitat quality based on population density and fitness of adult females was higher in high cover habitats. Net movement was from low cover to high cover habitats. The results indicated that adult female prairie voles exhibited density-dependent habitat selection. Furthermore, there was a significant cost of habitat selection, and the cost was density-independent.     

CRF receptors in the nucleus accumbens modulate partner preference in prairie voles

Recent evidence suggests a role for corticotropin-releasing factor (CRF) in the regulation of pair bonding in prairie voles. We have previously shown that monogamous and non-monogamous vole species have dramatically different distributions of CRF receptor type 1 (CRF(1)) and CRF receptor type 2 (CRF(2)) in the brain and that CRF(1) and CRF(2) receptor densities in the nucleus accumbens (NAcc) are correlated with social organization. Monogamous prairie and pine voles have significantly lower levels of CRF receptor type 1 (CRF(1)), and significantly higher levels of type 2 (CRF(2)) binding, in NAcc than non-monogamous meadow and montane voles. Here, we report that microinjections of CRF directly into the NAcc accelerate partner preference formation in male prairie voles. Control injections of CSF into NAcc, and CRF into caudate-putamen, did not facilitate partner preference. Likewise, CRF injections into NAcc of non-monogamous meadow voles also did not facilitate partner preference. In prairie voles, this CRF facilitation effect was blocked by co-injection of either CRF(1) or CRF(2) receptor antagonists into NAcc. Immunocytochemical staining for CRF and Urocortin-1 (Ucn-1), two endogenous ligands for CRF(1) and CRF(2) receptors in the brain, revealed that CRF, but not Ucn-1, immunoreactive fibers were present in NAcc. This supports the hypothesis that local CRF release into NAcc could activate CRF(1) or CRF(2) receptors in the region. Taken together, our results reveal a novel role for accumbal CRF systems in social behavior.     

Male and female meadow voles Microtus pennsylvanicus respond differently to scent marks from the top- middle-,and bottom-scent donors of an over-mark

Previous studies have shown that individuals responded preferentially to the mark of the top-scent donor relative to that of the bottom-scent donor of an over-m...     

Rates of vegetation change associated with prairie dog (Cynomys ludovicianus) grazing in North American mixed-grass prairie

A prairie dog (Cynomys ludovicianus) colony with a known history of habitation was studied to quantify the effects of herbivory on plant species composition, dominance, stature and diversity in a North American mixedgrass prairie. Gradient analysis was used to quantify the relationship between plant community structure, prairie dog density, burrow density and habitation history and to document community-level responses of plants subjected to heavy grazing pressure. The results quantify the type, rate and extent of change which plant populations and communities may undergo in response to the differential grazing of plants variously tolerant of defoliation.Detrended correspondence analysis indicated that 69% of the between-sample floristic variance on the site was attributable to prairie dog habitation. Perennial grasses were rapidly displaced from the site within 3 yr of colonization and were replaced by annual forbs. The net result was an increase in species richness and diversity on the prairie dog colony. Within the colony, however, the number of species was more a function of stand size than colonization history.Significant decreases in canopy stature after 2 yr of habitation resulted from replacement of mid-height grass species by shortgrass species and forbs. In addition, there was a shift from tall growth forms of off-colony species to dwarf growth forms of the same species on the colony. Decreases in litter and increases in bare soil cover were substantial during the first 2 yr of habitation but changed little thereafter.Abbreviations WCC Wind Cave Canyon - DCA Detrended Correspondence Analysis     

Heterogeneity in the concerted evolution process of a tandem satellite array in meadow mice (Microtus)

The evolutionary history of a 160-bp tandem satellite array, originally described from Microtus chrotorrhinus and called MSAT-160, was examined in related species of arvicolid rodents by sequence analyses, quantitative dot blotting, and Southern blotting. Results indicate that MSAT-160 is present in 12 of the 20 species and subspecies of Microtus assayed, but not in species belonging to any of the eight other genera examined. DNA from each species containing MSAT-160 was digested with 12 restriction endonucleases and restriction patterns were obtained reflecting the variable extent of homogenization of any given variant in different species. For example, with MboI digestion, M. chrotorrhinus produced a type A ladder pattern where most monomers contain the restriction site, M. ochrogaster generated a type B pattern where most monomers lack the site, and M. agrestis yielded a pattern intermediate between the A and B types. Further, dot blotting revealed copy-number differences between species. These findings indicate that changes in the periodic structure and amount of satellite DNA have occured since these species last shared a common ancestor. In addition, various species-pacific patterns were documented, illustrating that mechanism other than genomewide homogenization, such as stochastic mutation, out-of-register crossing over, deletion, and random amplification also play a role in structuring tandem arrays. Stochastic mutation and homogenization rates in satellite DNA, levels of species diversity, and magnitudes of chromosomal divergence differ significantly in Microtus, Mus, and Ctenomys, the three rodent lineages examined.     

Discrimination by male ring-tailed Lemurs (Lemur catta) between the scent marks of male and those of female conspecifics

Olfaction plays an important role in the social communication of all prosimians. (The experiment reported in this paper forms part of an intensive chemobehavioral study of olfaction in Lemur catta (ring-tailed lemur) being carried out in this laboratory.) Five male Lemur cattawere tested on their behavioral responses to paired scent stimuli. Responses measured were (1) total investigation time, (2) arm-marking, (3) ABO/BO rubbing, and (4) flehmen. Males showed a strong discrimination between the scent stimuli,giving higher levels of response to female scent on measures 1, 3, and 4. This response suggests an olfactory-related preference by males for female scent under controlled conditions. This preference may be a consequence of the females’ dominance over males and the brevity of estrus in L. catta,both of which would favor such choice behavior.     

Genetic control of enzyme polymorphisms in the California vole,Microtus californicus

Inheritance of 15 polymorphic isozymes was investigated in captive Microtus californicus. Eleven of the isozymes show patterns consistent with a Mendelian model of inheritance: glycerol-3-phosphate dehydrogenase (GPD), lactate dehydrogenases A and B (LDH-A and LDH-B), malic enzyme 2 (ME-2), isocitrate dehydrogenase 1 (ICD-1), phosphogluconate dehydrogenase (PGD), glutamate-oxaloacetate transaminase 1 (GOT-1) phosphoglucomutase 2 (PGM-2), leucine aminopeptidase (LAP), glucosephosphate isomerase (GPI), and esterase 2 (ES-2, from kidney). four of the isozymes show patterns that cannot be interpreted by a simple genetic model: esterases 1 and 4 (ES-1, ES-4, from hemolysate), esterase 3 (ES-3, from plasma), and protein 1 (PT-1). The following pairs of loci are assorting independently: LAP and PGD, LAP and PGM-2, GOT-1 and PGD, GOT-1 and GPD, LAP and GPD, GPD and PGD, GPI and PGD. Data from one test cross mating indicate that GPD and PGM-2 are loosely linked with recombination about 30%. Additional data are needed to confirm this relationship.This study was conducted while the first author was the recipient of an NIH Traineeship. The Departments of Genetics and Zoology provided financial support for the maintenance of the animal colony. This work was supported in part by an NIH-Biomed grant (3-S05-RR-07006-08S1) to W. Z. Lidicker.     

Host-parasitoid extinction and colonization in a fragmented prairie landscape

Few field studies of natural populations have examined the factors influencing local extinctions and colonization of empty habitat patches for a prey species and its predator. In this study, I carried out a census of planthopper (Prokelisia crocea; Hemiptera: Delphacidae) and egg parasitoid (Anagrus columbi; Hymenoptera: Mymaridae) incidence and densities in 147 host-plant patches (Spartina pectinata; Poaceae) over seven planthopper generations in a tall-grass prairie landscape. For both species, the likelihood of going extinct in a patch was related to a number of patch-specific variables: density, temporal variability in density, proportion of hosts parasitized (planthopper only), host-plant density, patch size, patch isolation, and composition of the surrounding matrix. Colonization likelihood was related only to the physical attributes of the patch. There was high patch turnover in this prairie landscape. On average, planthoppers went extinct in 23% of the patches and A. columbi went extinct in 51% of the patches in each generation. For the planthopper, extinction likelihood increased with a decrease in patch size and the proportion of the matrix composed of mudflat. Parasitism of eggs had no effect on the extinction likelihood of local P. crocea populations, suggesting that A. columbi may not play a major role in the patch dynamics of its host. The likelihood of extinction for A. columbi was dependent on factors that spanned three trophic levels. An increase in plant density, decrease in host density and decrease in parasitoid density all increased the likelihood of A. columbi extinction within a patch. The dependency on multiple trophic levels may explain the higher extinction risk for the parasitoid than its host. A. columbi extinction was also affected by the matrix habitat surrounding the patch—the effect was the opposite of that for P. crocea. Finally, vacant patches were colonized at rates of 53% and 34% per generation for the planthopper and parasitoid, respectively. For both species, colonization probabilities decreased with an increase in patch isolation. High host densities in a patch also favored high rates of colonization by A. columbi. I discuss how anthropogenic changes to the prairie landscape can affect the metapopulation dynamics and persistence time of this host-parasitoid interaction.     

Allee effects and conspecific cueing jointly lead to conspecific attraction

Conspecific attraction is the preferential settlement into habitat patches with conspecifics. To be a good proximate strategy, fitness gains from settling with conspecifics must outweigh the costs of higher conspecific densities, such as intraspecific competition. Two types of benefits have been proposed to explain conspecific attraction: Allee effects (i.e., positive density dependence) and conspecific cueing (using conspecifics as an indicator of habitat quality). I present empirical evidence for conspecific attraction in the settlement of the porcelain crab, Petrolisthes cinctipes Randall (Anomura: Porcellanidae). Previous work demonstrated that P. cinctipes experiences strong intraspecific competition and that both Allee effects and conspecific cueing are present in P. cinctipes life-history. I developed an empirically-based fitness model of the costs and benefits of settling with conspecifics. Based on this model, I simulated optimal settlement to habitat patches that varied in conspecific density and habitat quality, where the correlation between density and habitat quality determined the level of conspecific cueing. I tested whether Allee effects alone, conspecific cueing alone, or Allee effects and conspecific cueing together could provide an ultimate explanation for the proximate settlement behavior of P. cinctipes. The settlement simulation was consistent with empirical settlement only when Allee effects and conspecific cueing were both included. Three life-history features are critical to this conclusion: (1) fitness is maximized at intermediate density, (2) fitness depends on the decisions of previous settlers, and (3) conspecific density provides good information about habitat quality. The quality of information garnered from conspecifics determines whether conspecific attraction is a good proximate strategy for settlement. I present a graphical illustration demonstrating how Allee effects and conspecific cueing work together to influence fitness, providing a conceptual framework for other systems.Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.