Sex and Species Differences in the Vasopressin Innervation of Sexually Naive and Parental Prairie Voles, Microtus ochrogaster and Meadow Voles, Microtus pennsylvanicus

The presence or absence of specific odor-producing tissues has been used to suggest phylogenetic relationships among microtine rodents, but has not been related to patterns of social organization. We examined the sources of sex-specific scents in prairie voles, Microtus ochrogaster, using a preference task. Prairie voles have eight sources of sex-specific scents. Four scents, namely those from the urine, feces, anogenital area, and mouth were more attractive to opposite- than same-sex conspecifics. Three scents were attractive to one sex but not the other. Scent from the back of females was attractive to males and scents from the chest and head–neck–ears of males were attractive to females. Scent from the male posterolateral region was attractive to both females and males. We then compared these eight sources of scent with the known sources of scent from meadow voles, Microtus pennsylvanicus, a species whose social system is unlike that of prairie voles. Prairie voles have more sources of sex-specific scent than meadow voles. This difference supports the hypothesis that the number of sources of sex-specific scent is greater in a social species (prairie voles) than in an asocial species (meadow voles).

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Comparative neurotranscriptomics reveal widespread species differences associated with bonding

BMC Genomics ◽

10.1186/s12864-021-07720-0 ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Joel A. Tripp ◽

Alejandro Berrio ◽

Lisa A. McGraw ◽

Mikhail V. Matz ◽

Jamie K. Davis ◽

...

Keyword(s):

Gene Expression ◽

Brain Region ◽

Molecular Mechanisms ◽

Species Differences ◽

Cell Structure ◽

Bond Formation ◽

Pair Bonding ◽

Prairie Voles ◽

Meadow Voles ◽

Time Points

Abstract Background Pair bonding with a reproductive partner is rare among mammals but is an important feature of human social behavior. Decades of research on monogamous prairie voles (Microtus ochrogaster), along with comparative studies using the related non-bonding meadow vole (M. pennsylvanicus), have revealed many of the neural and molecular mechanisms necessary for pair-bond formation in that species. However, these studies have largely focused on just a few neuromodulatory systems. To test the hypothesis that neural gene expression differences underlie differential capacities to bond, we performed RNA-sequencing on tissue from three brain regions important for bonding and other social behaviors across bond-forming prairie voles and non-bonding meadow voles. We examined gene expression in the amygdala, hypothalamus, and combined ventral pallidum/nucleus accumbens in virgins and at three time points after mating to understand species differences in gene expression at baseline, in response to mating, and during bond formation. Results We first identified species and brain region as the factors most strongly associated with gene expression in our samples. Next, we found gene categories related to cell structure, translation, and metabolism that differed in expression across species in virgins, as well as categories associated with cell structure, synaptic and neuroendocrine signaling, and transcription and translation that varied among the focal regions in our study. Additionally, we identified genes that were differentially expressed across species after mating in each of our regions of interest. These include genes involved in regulating transcription, neuron structure, and synaptic plasticity. Finally, we identified modules of co-regulated genes that were strongly correlated with brain region in both species, and modules that were correlated with post-mating time points in prairie voles but not meadow voles. Conclusions These results reinforce the importance of pre-mating differences that confer the ability to form pair bonds in prairie voles but not promiscuous species such as meadow voles. Gene ontology analysis supports the hypothesis that pair-bond formation involves transcriptional regulation, and changes in neuronal structure. Together, our results expand knowledge of the genes involved in the pair bonding process and open new avenues of research in the molecular mechanisms of bond formation.

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Influence of the social environment on parental behavior and pup development of meadow voles (Microtus pennsylvanicus) and prairie voles (M. Ochrogaster).

Journal of Comparative Psychology ◽

10.1037/0735-7036.106.2.163 ◽

1992 ◽

Vol 106 (2) ◽

pp. 163-171 ◽

Cited By ~ 79

Author(s):

Zuoxin Wang ◽

Melinda A. Novak

Keyword(s):

Social Environment ◽

Parental Behavior ◽

Microtus Pennsylvanicus ◽

Prairie Voles ◽

Meadow Voles ◽

The Social ◽

Pup Development

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Sex and species differences in cell-mediated immune responses in voles

Canadian Journal of Zoology ◽

10.1139/z98-071 ◽

1998 ◽

Vol 76 (7) ◽

pp. 1394-1398 ◽

Cited By ~ 9

Author(s):

Sabra L Klein ◽

Randy J Nelson

Keyword(s):

Immune Responses ◽

Immune Function ◽

Species Differences ◽

Cell Mediated Immunity ◽

Prairie Voles ◽

Con A ◽

Meadow Voles ◽

Monogamous Species ◽

Cell Mitogen ◽

Androgenic Effect

Males generally display reduced immune responses and greater susceptibility to disease than females, possibly reflecting the suppressive effects of androgens on the immune system. It is presumed that this androgenic effect on immune function is more pronounced among polygynous than monogamous species because concentrations of circulating androgens are generally higher among polygynous than monogamous males. The present study examined sex and species differences in cell-mediated immunity of two Microtus species. Cell-mediated immunity was assessed among individually housed polygynous meadow voles (M. pennsylvanicus) and monogamous prairie voles (M. ochrogaster) by examining the proliferative responses of splenocytes to the T-cell mitogen concanavalin A (Con A) and the B-cell mitogen lipopolysaccharide (LPS). Neither sex nor species differences were observed in response to stimulation with Con A. In contrast, meadow voles exhibited higher proliferative responses to LPS than prairie voles. Sex differences in immune function were only observed among prairie voles; males exhibited higher proliferative responses to LPS than females. Male meadow voles had higher circulating testosterone concentrations than male prairie voles and female prairie voles had higher estradiol concentrations than female meadow voles. Males of both Microtus species weighed more than conspecific females. The immunological differences were not related to differences in either body mass or hormone concentrations. Overall, these data do not support the hypothesis that higher androgen concentrations in polygynous males influence sex or species differences in immune function.

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Parental behaviour of prairie voles (Microtus ochrogaster) and meadow voles (M. pennsylvanicus) in relation to sex of offspring

Behaviour ◽

10.1163/1568539x-00003141 ◽

2014 ◽

Vol 151 (4) ◽

pp. 535-553 ◽

Cited By ~ 3

Author(s):

Betty McGuire ◽

William E. Bemis ◽

Francoise Vermeylen

Keyword(s):

Litter Size ◽

Female Offspring ◽

Prairie Vole ◽

Microtus Ochrogaster ◽

Meadow Vole ◽

Prairie Voles ◽

Meadow Voles ◽

Male And Female ◽

Mothers And Fathers ◽

Offspring Sex

Monogamous parents are predicted to invest equally in male and female offspring whereas polygynous parents in good condition are predicted to invest more in male than female offspring. Sex-biased parental investment can occur in three ways: (1) mothers and fathers invest different amounts of care in their offspring (effect of parent sex); (2) parents invest different amounts of care in male and female offspring (effect of offspring sex); and (3) one parent, but not the other, invests different amounts of care in male and female offspring (interaction between parent sex and offspring sex). Studies of parent–offspring interactions in rodents have focused on either effect of parent sex or effect of offspring sex, but not the interaction between parent sex and offspring sex, and most studies have examined only one species. We studied prairie voles (Microtus ochrogaster), a monogamous species, and meadow voles (M. pennsylvanicus), a polygynous (or promiscuous) species, under laboratory conditions designed to simulate field conditions. For each species, we recorded the frequency and duration with which mothers and fathers licked their male and female offspring. We found that meadow vole fathers licked male offspring for longer durations than female offspring. However, prairie vole fathers, prairie vole mothers, and meadow vole mothers did not lick male and female pups for different durations. From the standpoint of the pups, male prairie vole pups, female prairie vole pups, and female meadow vole pups were licked for longer durations by their mothers than by their fathers. In contrast, for male meadow vole pups there was no difference in the duration with which they were licked by mothers and fathers. We also detected effects of litter size: as litter size increased, the frequency and duration of pup licking decreased for mothers and increased for fathers. For duration (but not frequency) of pup licking, these changes were more dramatic in meadow voles than in prairie voles. Our data are generally consistent with predictions that monogamous parents, such as prairie voles, should invest equally in male and female offspring whereas polygynous (or promiscuous) parents, such as meadow voles, should invest more in male offspring when conditions are favourable. Our data also highlight the complexity of parent–offspring interactions in rodents and emphasize the need to examine whether male and female offspring within a species differ in their behaviour or ability to obtain parental care.

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