The role of avpr1a microsatellite length on reproductive success of female Microtus ochrogaster
In: BehaviourSearch for other papers by Meaghan N. Harris in
Current site
Google Scholar
Search for other papers by Rose M. Alvarez in
Current site
Google Scholar
Search for other papers by Brian Keane in
Current site
Google Scholar
Search for other papers by Alexander D. Talib in
Current site
Google Scholar
Search for other papers by Michael J. Eiswerth in
Current site
Google Scholar
Search for other papers by Nancy G. Solomon in
Current site
Google Scholar
Vasopressin and its’ interactions with the vasopressin 1a receptor (V1aR) are important in the formation of social attachments and parental behavior in male mammals but there also is evidence that vasopressin is involved in maternal behavior in female mammals. Laboratory studies have shown that female rats with greater expression of V1aR in particular brain regions display more maternal behavior than those with less V1aR expression. Previous data showed that variation in neural V1aR expression in males of several species of rodents was influenced by the length of microsatellite DNA within the regulatory region of gene (avpr1a) encoding V1aR. In male prairie voles (Microtus ochrogaster), the neural expression of V1aR differs between individuals with longer versus shorter avpr1a microsatellites. Males with longer avpr1a microsatellites had greater V1aR expression in particular brain regions, spent more time with their female social partner, and licked and groomed pups more than males with shorter avpr1a microsatellite lengths. If avpr1a microsatellite length is correlated with V1aR expression in females in a similar fashion to that in male prairie voles, females with longer avpr1a microsatellites should have greater reproductive success since maternal care should be critical for offspring survival. In addition, female prairie voles may benefit by living with males that have longer avpr1a microsatellites due to increased male presence at the nest and paternal care. We tested these predictions with prairie voles from semi-natural populations. Females that had summed avpr1a microsatellite allele lengths greater than the median produced more litters and total offspring than females with summed avpr1a lengths less than the median. Females with summed avpr1a microsatellite allele lengths greater than the median also produced offspring sired by more males. The avpr1a length of male social and genetic partners did not influence female reproductive success. This is the first field study showing a relationship between avpr1a microsatellite allele length and female reproductive success in any species.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
-
Aschemeier L.M., Keane B., Solomon N.G. (2008). Body size has a greater influence on female mate choice than length of microsatellite region of the avpr1a gene in male prairie voles. — J. Young Investig. 18, available online at http://www.jyi.org/research/re.php?id=1447.
-
Bamshad M., Novak M.A., De Vries G.J. (1993). Sex and species differences in the vasopressin innervation of sexually naive and parental prairie voles, Microtus ochrogaster, and meadow voles, Microtus pennsylvanicus. — J. Neuroendocrinol. 5: 247-255.
-
Bamshad M., Novak M.A., De Vries G.J. (1994). Cohabitation alters vasopressin innervation and paternal behavior in prairie voles (Microtus ochrogaster). — Physiol. Behav. 56: 751-758.
-
Barrett C.E., Keebaugh A.C., Ahern T.H., Bass C.E., Terwilliger E.F., Young L.J. (2013). Variation in vasopressin receptor (Avpr1a) expression creates diversity in behaviors related to monogamy in prairie voles. — Horm. Behav. 63: 518-526.
-
Bisceglia R., Jenkins J.M., Wigg K.G., O’Connor T.G., Moran G., Barr C.L. (2012). Arginine vasopressin 1a receptor gene and maternal behavior: evidence of association and moderation. — Genes Brain Behav. 11: 262-268.
-
Blumstein D.T., Ebensperger L.A., Hayes L.D., Vasquez R.A., Ahern T.H., Burger J.H., Dolezal A.G., Dosmann A., Gonzalez-Mariscal G., Harris B.N., Herrera E.A., Lacey E.A., Mateo J., McGraw L.A., Olazabal D., Ramenofsky M., Rubenstein D.R., Sakhai S.A., Saltzman W., Sainz-Borgo C., Soto-Gamboa M., Stewart M.L., Wey T.W., Wingfield J.C., Young L.J. (2010). Toward an integrative understanding of social behavior: new models and new opportunities. — Front. Behav. Neurosci. 4: DOI:10.3389/fnbeh.2010.00034.
-
Bosch O.J., Neumann I.D. (2008). Brain vasopressin is an important regulator of maternal behavior independent of dams’ trait anxiety. — Proc. Natl. Acad. Sci. USA 105: 17139-17144.
-
Bosch O.J., Neumann I.D. (2010). Vasopressin released within the central amygdala promotes maternal aggression. — Eur. J. Neurosci. 31: 883-891.
-
Bosch O.J., Neumann I.D. (2012). Both oxytocin and vasopressin are mediators of maternal care and aggression in rodents: from central release to sites of action. — Horm. Behav. 61: 293-303.
-
Bosch O.J., Pfortsch J., Beiderbeck D.I., Landgraf R., Neumann I.D. (2010). Maternal behavior is associated with vasopressin release in the medial preoptic area and bed nucleus of the stria terminalis in the rat. — J. Neuroendocrinol. 22: 420-429.
-
Caldwell H.K., Lee H.J., Macbeth A.H., Young W.S. III (2008). Vasopressin: behavioral roles of an “original” neuropeptide. — Prog. Neurobiol. 84: 1-24.
-
Calisi R.M., Bentley G.E. (2009). Lab and field experiments: are they the same animal? — Horm. Behav. 56: 1-10.
-
Carter C.S., DeVries A.C., Taymans S.E., Roberts R.L., Williams J.R., Getz L.L. (1997). Peptides, steroids, and pair bonding. — Ann. NY Acad. Sci. 807: 260-272.
-
Carter C.S., Getz L.L. (1993). Monogamy and the prairie vole. — Sci. Am. 268: 100-110.
-
Castelli F.R., Kelley R.A., Keane B., Solomon N.G. (2011). Female prairie voles show social and sexual preferences for males with longer avpr1a microsatellite alleles. — Anim. Behav. 82: 1117-1126.
-
Chesh A.S., Mabry K.E., Keane B., Noe D.A., Solomon N.G. (2012). Are body mass and parasite load related to social partnerships and mating in Microtus ochrogaster? — J. Mammal. 93: 229-238.
-
Cochran G.R., Solomon N.G. (2000). Effects of food supplementation on the social organization of prairie voles (Microtus ochrogaster). — J. Mammal. 81: 746-757.
-
Curley J.P., Jensen C.L., Franks B., Champagne F.A. (2012). Variation in maternal and anxiety-like behavior associated with discrete patterns of oxytocin and vasopressin 1a receptor density in the lateral septum. — Horm. Behav. 61: 454-461.
-
Desy E.A., Batzli G.O. (1989). Effects of food availability and predation on prairie vole demography: a field experiment. — Ecology 70: 411-421.
-
Dewsbury D.A. (1995). Role of male proximity in pregnancy maintenance in prairie voles, Microtus ochrogaster. — Physiol. Behav. 57: 827-829.
-
Engelmann M., Landgraf R. (1994). Microdialysis administration of vasopressin into the septum improves social recognition in Brattleboro rats. — Physiol. Behav. 55: 145-149.
-
Gaines M.S., Vivas A.M., Baker C.L. (1979). An experimental analysis of dispersal in fluctuating vole populations: demographic parameters. — Ecology 60: 814-828.
-
Ganev I.V., Solomon N.G., Lucia K.E., Keane B. (2009). Multiple captures of adult prairie voles correlated with residency status and genetic parentage. — J. Mammal. 90: 696-703.
-
Getz L.L., McGuire B. (1993). A comparison of living singly and in male–female pairs in the prairie vole. — Ethology 94: 265-278.
-
Getz L.L., McGuire B., Hofmann J., Pizzuto T., Frase B. (1994). Natal dispersal and philopatry in the prairie vole (Microtus ochrogaster): settlement, survival, and potential reproductive success. — Ethol. Ecol. Evol. 6: 267-284.
-
Getz L.L., McGuire B., Pizzuto T. (2004). Does mate choice take place in free-living prairie voles Microtus ochrogaster? Evidence from field data. — Acta Zool. Sin. 50: 527-534.
-
Getz L.L., McGuire B., Pizzuto T., Hofmann J.E., Frase B. (1993). Social organization of the prairie vole (Microtus ochrogaster). — J. Mammal. 74: 44-58.
-
Goodson J.L. (2005). The vertebrate social behavior network: evolutionary themes and variations. — Horm. Behav. 48: 11-22.
-
Goodson J.L., Bass A.H. (2001). Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. — Brain Res. Rev. 35: 246-265.
-
Goodson J.L., Kabelik D. (2009). Dynamic limbic networks and social diversity in vertebrates: from neural context to neuromodulatory pattern. — Front. Neuroendocrinol. 30: 429-441.
-
Goyal U., Bryant L., Solomon N.G., Keane B. (2007). Effects of body size on reproduction and survival in the prairie vole (Microtus ochragaster): is bigger better? — J. Young. Investig. 16, available online at http://www.jyi.org/issue/effects-of-body-size-on-reproduction-and-survival-in-the-prairie-vole-microtus-ochrogaster-is-bigger-better/
-
Hammock E.A.D., Young L.J. (2005). Microsatellite instability generates diversity in brain and sociobehavioral traits. — Science 308: 1630-1634.
-
Insel T.R., Hulihan T.J. (1995). A gender-specific mechanism for pair bonding: oxytocin and partner preference formation in monogamous voles. — Behav. Neurosci. 109: 782-789.
-
Kalinowski S.T., Taper M.L., Marshall T.C. (2007). Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. — Mol. Ecol. 16: 1099-1106.
-
Keane B., Bryant L., Goyal U., Williams S., Kortering S.L., Lucia K.E., Richmond A.R., Solomon N.G. (2007). No effect of body condition at weaning on survival and reproduction in prairie voles. — Can. J. Zool. 85: 718-727.
-
Keller B.L. (1985). Reproductive patterns. — In: Biology of New World Microtus, Special Publication No. 8 ( Tamarin R.H., ed.). The American Society of Mammalogists, Lawrence, KS, p. 725-778.
-
Kelley R.A., Castelli F.R., Mabry K.E., Solomon N.G. (2013). Effects of experience and avpr1a microsatellite length on parental care in male prairie voles (Microtus ochrogaster). — Behav. Ecol. Sociobiol. 67: 985-992.
-
Kirkpatrick B., Williams J.R., Slotnick B.M., Carter C.S. (1994). Olfactory bulbectomy decreases social behavior in male prairie voles (M. ochrogaster). — Physiol. Behav. 55: 885-889.
-
Klemme I., Kataja-aho S., Eccard J.A., Ylönen H. (2012). Variable mode of estrus affects female decision for multiple mating. — Behav. Ecol. 23: 361-367.
-
Koshimizu T., Nakamura K., Egashira N., Hiroyama M., Nonoguchi H., Tanoue A. (2012). Vasopressin V1a and V1b receptors: from molecules to physiological systems. — Physiol. Rev. 92: 1813-1864.
-
Lim M.M., Wang Z., Olazabal D.E., Ren X., Terwilliger E.F., Young L.J. (2004). Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. — Nature 429: 754-757.
-
Lonstein J.S., De Vries G.J. (1999). Comparison of the parental behavior of pair-bonded female and male prairie voles (Microtus ochrogaster). — Physiol. Behav. 66: 33-40.
-
Lucia K.E., Keane B., Hayes L.D., Lin Y.K., Schaefer R.L., Solomon N.G. (2008). Philopatry in prairie voles: an evaluation of the habitat saturation hypothesis. — Behav. Ecol. 19: 774-783.
-
Mabry K.E., Streatfeild C.A., Keane B., Solomon N.G. (2011). avpr1a length polymorphism is not associated with either social or genetic monogamy in free-living prairie voles. — Anim. Behav. 81: 11-18.
-
Mahady S.J., Wolff J.O. (2002). A field test of the Bruce effect in the monogamous prairie vole (Microtus ochrogaster). — Behav. Ecol. Sociobiol. 52: 31-37.
-
Marshall T.C., Slate J., Kruuk L.E.B., Pemberton J.M. (1998). Statistical confidence for likelihood-based paternity inference in natural populations. — Mol. Ecol. 7: 639-655.
-
McGuire B., Getz L.L. (1998). The nature and frequency of social interactions among free-living prairie voles (Microtus ochrogaster). — Behav. Ecol. Sociobiol. 43: 271-279.
-
McGuire B., Getz L.L. (2010). Alternative male reproductive tactics in a natural population of prairie voles (Microtus ochrogaster). — Acta Theriol. 55: 261-270.
-
McGuire B., Russel K.D., Mahoney T., Novak M. (1992). The effects of mate removal on pregnancy success in prairie voles (Microtus ochrogaster) and meadow voles (Microtuspennsylvanicus). — Biol. Reprod. 47: 37-42.
-
Nephew B.C., Bridges R.S. (2008). Central actions of arginine vasopressin and a V1a receptor antagonist on maternal aggression, maternal behavior, and grooming in lactating rats. — Pharmacol. Biochem. Behav. 91: 77-83.
-
Numan M., Insel T.R. (2003). The neurobiology of parental behavior. — Springer-Verlag, New York, NY.
-
O’Connell L.A., Hofmann H.A. (2011). Genes, hormones, and circuits: an integrative approach to study the evolution of social behavior. — Front. Neuroendocrinol. 32: 320-335.
-
Ophir A.G., Campbell P., Hanna K., Phelps S.M. (2008). Field tests of cis-regulatory variation at the prairie vole avpr1a locus: association with V1aR abundance but not sexual or social fidelity. — Horm. Behav. 54: 694-702.
-
Owens I.P.F. (2006). Where is behavioural ecology going? — Trends Ecol. Evol. 21: 356-361.
-
Pitkow L.J., Sharer C.A., Ren X., Insel T.R., Terwilliger E.F., Young L.J. (2001). Facilitation of affiliation and pair-bond formation by vasopressin receptor gene transfer into the ventral forebrain of a monogamous vole. — J. Neurosci. 21: 7392-7396.
-
Robinson G.E., Fernald R.D., Clayton D.F. (2008). Genes and social behavior. — Science 322: 896-900.
-
Schanberg S.M., Evoniuk G., Kuhn C.M. (1984). Tactile and nutritional aspects of maternal care: specific regulators of neuroendocrine function and cellular development. — Proc. Soc. Exp. Biol. Med. 175: 135-146.
-
Sikes R.S., Gannon W.L. & the Animal Care and Use Committee of the American Society of Mammalogists (2011). Guidelines of the American Society of Mammalogists for the use of wild mammals in research. — J. Mammal. 92: 235-253.
-
Solomon N.G. (1991). Age of pairing affects reproduction in prairie voles. — Lab. Anim. 25: 232-235.
-
Solomon N.G. (1993). Comparison of parental behavior in male and female prairie voles (Microtusochrogaster). — Can. J. Zool. 71: 434-437.
-
Solomon N.G., Jacquot J.J. (2002). Characteristics of resident and wandering prairie voles (Microtus ochrogaster). — Can. J. Zool. 80: 951-955.
-
Solomon N.G., Richmond A.R., Harding P.A., Fries A., Jacquemin S., Schaefer R.L., Lucia K.E., Keane B. (2009). Polymorphism at the avpr1a locus in male prairie voles correlated with genetic but not social monogamy in field populations. — Mol. Ecol. 18: 4680-4695.
-
Toth A.L., Varala K., Newman T.C., Miguez F.E., Hutchison S.K., Willoughby D.A., Simons J.F., Egholm M., Hunt J.H., Hudson M.E., Robinson G.E. (2007). Wasp gene expression supports an evolutionary link between maternal behavior and eusociality. — Science 318: 441-444.
-
Van Leeuwen F.W., Caffe A.R., De Vries G.J. (1985). Vasopressin cells in the bed nucleus of the stria terminalis of the rat: sex differences and the influence of androgens. — Brain Res. 325: 391-394.
-
Wang Z., Novak M.A. (1992). The influence of the social environment on parental behavior and pup development of meadow voles (Microtus pennsylvanicus) and prairie voles (M. ochrogaster). — J. Comp. Psychol. 106: 163-171.
-
Wang Z., Ferris C.F., De Vries G.J. (1994). Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster). — Proc. Natl. Acad. Sci. USA 91: 400-404.
-
Wang Z.X., Liu Y., Young L.J., Insel T.R. (2000). Hypothalamic vasopressin gene expression increases in both males and females postpartum in a biparental rodent. — J. Neuroendocrinol. 12: 111-120.
-
Young L.J., Nilsen R., Waymire K.G., MacGregor G.R., Insel T.R. (1999). Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. — Nature 400: 766-768.
-
Zingg H.H., Lefebvre D.L. (1988). Oxytocin and vasopressin gene expression during gestation and lactation. — Mol. Brain Res. 4: 1-6.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 602 | 67 | 11 |
| Full Text Views | 148 | 1 | 0 |
| PDF Views & Downloads | 20 | 0 | 0 |
The role of avpr1a microsatellite length on reproductive success of female Microtus ochrogaster
In: BehaviourSearch for other papers by Meaghan N. Harris in
Current site
Google Scholar
PubMed
Search for other papers by Rose M. Alvarez in
Current site
Google Scholar
PubMed
Search for other papers by Brian Keane in
Current site
Google Scholar
PubMed
Search for other papers by Alexander D. Talib in
Current site
Google Scholar
PubMed
Search for other papers by Michael J. Eiswerth in
Current site
Google Scholar
PubMed
Search for other papers by Nancy G. Solomon in
Current site
Google Scholar
PubMed
Vasopressin and its’ interactions with the vasopressin 1a receptor (V1aR) are important in the formation of social attachments and parental behavior in male mammals but there also is evidence that vasopressin is involved in maternal behavior in female mammals. Laboratory studies have shown that female rats with greater expression of V1aR in particular brain regions display more maternal behavior than those with less V1aR expression. Previous data showed that variation in neural V1aR expression in males of several species of rodents was influenced by the length of microsatellite DNA within the regulatory region of gene (avpr1a) encoding V1aR. In male prairie voles (Microtus ochrogaster), the neural expression of V1aR differs between individuals with longer versus shorter avpr1a microsatellites. Males with longer avpr1a microsatellites had greater V1aR expression in particular brain regions, spent more time with their female social partner, and licked and groomed pups more than males with shorter avpr1a microsatellite lengths. If avpr1a microsatellite length is correlated with V1aR expression in females in a similar fashion to that in male prairie voles, females with longer avpr1a microsatellites should have greater reproductive success since maternal care should be critical for offspring survival. In addition, female prairie voles may benefit by living with males that have longer avpr1a microsatellites due to increased male presence at the nest and paternal care. We tested these predictions with prairie voles from semi-natural populations. Females that had summed avpr1a microsatellite allele lengths greater than the median produced more litters and total offspring than females with summed avpr1a lengths less than the median. Females with summed avpr1a microsatellite allele lengths greater than the median also produced offspring sired by more males. The avpr1a length of male social and genetic partners did not influence female reproductive success. This is the first field study showing a relationship between avpr1a microsatellite allele length and female reproductive success in any species.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 602 | 67 | 11 |
| Full Text Views | 148 | 1 | 0 |
| PDF Views & Downloads | 20 | 0 | 0 |
