[en] Parental care is essential for the survival of mammals, yet the mechanisms underlying its evolution remain largely unknown. Here we show that two sister species of mice, Peromyscus polionotus and Peromyscus maniculatus, have large and heritable differences in parental behaviour. Using quantitative genetics, we identify 12 genomic regions that affect parental care, 8 of which have sex-specific effects, suggesting that parental care can evolve independently in males and females. Furthermore, some regions affect parental care broadly, whereas others affect specific behaviours, such as nest building. Of the genes linked to differences in nest-building behaviour, vasopressin is differentially expressed in the hypothalamus of the two species, with increased levels associated with less nest building. Using pharmacology in Peromyscus and chemogenetics in Mus, we show that vasopressin inhibits nest building but not other parental behaviours. Together, our results indicate that variation in an ancient neuropeptide contributes to interspecific differences in parental care.
Disciplines :
Genetics & genetic processes
Author, co-author :
Bendesky, Andres; Howard Hughes Medical Institute, Harvard University, Cambridge, ; Department of Organismic and Evolutionary Biology, Harvard University, ; Department of Molecular and Cellular Biology, Harvard University,
Kwon, Young-Mi; Howard Hughes Medical Institute, Harvard University, Cambridge, ; Department of Organismic and Evolutionary Biology, Harvard University,
Lassance, Jean-Marc ; Université de Liège - ULiège > Département de gestion vétérinaire des Ressources Animales (DRA) > Génomique animale ; Howard Hughes Medical Institute, Harvard University, Cambridge, ; Department of Organismic and Evolutionary Biology, Harvard University, ; Department of Molecular and Cellular Biology, Harvard University,
Lewarch, Caitlin L; Howard Hughes Medical Institute, Harvard University, Cambridge, ; Department of Molecular and Cellular Biology, Harvard University,
Yao, Shenqin; Howard Hughes Medical Institute, Harvard University, Cambridge, ; Department of Molecular and Cellular Biology, Harvard University,
Peterson, Brant K; Howard Hughes Medical Institute, Harvard University, Cambridge, ; Department of Organismic and Evolutionary Biology, Harvard University,
He, Meng Xiao; Graduate Program in Biophysics, Harvard University, Cambridge,
Dulac, Catherine; Howard Hughes Medical Institute, Harvard University, Cambridge, ; Department of Molecular and Cellular Biology, Harvard University, ; Center for Brain Science, Harvard University, Cambridge, Massachusetts
Hoekstra, Hopi E; Howard Hughes Medical Institute, Harvard University, Cambridge, ; Department of Organismic and Evolutionary Biology, Harvard University, ; Department of Molecular and Cellular Biology, Harvard University, ; Graduate Program in Biophysics, Harvard University, Cambridge, ; Center for Brain Science, Harvard University, Cambridge, Massachusetts ; Museum of Comparative Zoology, Harvard University, Cambridge,
Language :
English
Title :
The genetic basis of parental care evolution in monogamous mice.
Lukas, D., & Clutton-Brock, T. H. The evolution of social monogamy in mammals. Science 341, 526-530 (2013
Lim, M. M., et al. Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature 429, 754-757 (2004
Okhovat, M., Berrio, A., Wallace, G., Ophir, A. G., & Phelps, S. M. Sexual fidelity trade-offs promote regulatory variation in the prairie vole brain. Science 350, 1371-1374 (2015
Wang, Z., Ferris, C. F., & De Vries, G. J. Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster). Proc. Natl Acad. Sci. USA 91, 400-404 (1994
Bosch, O. J., & Neumann, I. D. 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 (2012
Dulac, C., O'Connell, L. A., & Wu, Z. Neural control of maternal and paternal behaviors. Science 345, 765-770 (2014
Scott, N., Prigge, M., Yizhar, O., & Kimchi, T. A sexually dimorphic hypothalamic circuit controls maternal care and oxytocin secretion. Nature 525, 519-522 (2015
Turner, L. M., et al. Monogamy evolves through multiple mechanisms: evidence from V1aR in deer mice. Mol. Biol. Evol. 27, 1269-1278 (2010
Birdsall, D. A., & Nash, D. Occurrence of successful multiple insemination of females in natural populations of deer mice (Peromyscus maniculatus). Evolution 27, 106-110 (1973
Dewsbury, D. A. Aggression, copulation, and differential reproduction of deer mice (Peromyscus maniculatus) in a semi-natural enclosure. Behaviour 91, 1-23 (1984
Dewsbury, D. A., & Lovecky, D. V. Copulatory behavior of old-field mice (Peromyscus polionotus) from different natural populations. Behav. Genet. 4, 347-355 (1974
Foltz, D. W. Genetic evidence for long-Term monogamy in a small rodent, Peromyscus polionotus. Am. Nat. 117, 665-675 (1981
Dewsbury, D. A. An exercise in the prediction of monogamy in the field from laboratory data on 42 species of muroid rodents. Biologist 63, 138-162 (1981
Peterson, B. K., Weber, J. N., Kay, E. H., Fisher, H. S., & Hoekstra, H. E. Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS ONE 7, e37135 (2012
Andolfatto, P., et al. Multiplexed shotgun genotyping for rapid and efficient genetic mapping. Genome Res. 21, 610-617 (2011
Royle, N. J., Smiseth, P. T & Kölliker, M. The Evolution of Parental Care (Oxford Univ. Press, 2012
Choi, Y., Sims, G. E., Murphy, S., Miller, J. R., & Chan, A. P. Predicting the functional effect of amino acid substitutions and indels. PLoS ONE 7, e46688 (2012
Lagoutte, E., et al. Oxidation of hydrogen sulfide remains a priority in mammalian cells and causes reverse electron transfer in colonocytes. Biochim. Biophys. Acta Bioenerg. 1797, 1500-1511 (2010
Seth, R. B., Sun, L., Ea, C.-K., & Chen, Z. J. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-? B and IRF 3. Cell 122, 669-682 (2005
Renella, R., et al. Codanin-1 mutations in congenital dyserythropoietic anemia type 1 affect HP1α localization in erythroblasts. Blood 117, 6928-6938 (2011
Lindfors, P. H., Lindahl, M., Rossi, J., Saarma, M., & Airaksinen, M. S. Ablation of persephin receptor glial cell line-derived neurotrophic factor family receptor α4 impairs thyroid calcitonin production in young mice. Endocrinology 147, 2237-2244 (2006
Numan, M. Medial preoptic area and maternal behavior in the female rat. J. Comp. Physiol. Psychol. 87, 746-759 (1974
Insel, T. R., & Harbaugh, C. R. Lesions of the hypothalamic paraventricular nucleus disrupt the initiation of maternal behavior. Physiol. Behav. 45, 1033-1041 (1989
Insel, T. R. The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron 65, 768-779 (2010
Kramer, K. M., Yamamoto, Y., Hoffman, G. E., & Cushing, B. S. Estrogen receptor α and vasopressin in the paraventricular nucleus of the hypothalamus in Peromyscus. Brain Res. 1032, 154-161 (2005
Neumann, I. D., & Landgraf, R. Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors. Trends Neurosci. 35, 649-659 (2012
Bult, A., van der Zee, E. A., Compaan, J. C., & Lynch, C. B. Differences in the number of arginine-vasopressin-immunoreactive neurons exist in the suprachiasmatic nuclei of house mice selected for differences in nest-building behavior. Brain Res. 578, 335-338 (1992
Bendesky, A., & Bargmann, C. I. Genetic contributions to behavioural diversity at the gene-environment interface. Nat. Rev. Genet. 12, 809-820 (2011
De Vries, G. J. Sex differences in adult and developing brains: compensation, compensation, compensation. Endocrinology 145, 1063-1068 (2004
Tinbergen, N. The hierarchical organization of nervous mechanisms underlying instinctive behaviour. Symp. Soc. Exp. Biol. 4, 305-312 (1950
Kennedy, A., et al. Internal states and behavioral decision-making: toward an integration of emotion and cognition. Cold Spring Harb. Symp. Quant. Biol. 79, 199-210 (2014
Devidze, N., Lee, A. W., Zhou, J., & Pfaff, D. W. CNS arousal mechanisms bearing on sex and other biologically regulated behaviors. Physiol. Behav. 88, 283-293 (2006
Wu, Z., Autry, A. E., Bergan, J. F., Watabe-Uchida, M., & Dulac, C. G. Galanin neurons in the medial preoptic area govern parental behaviour. Nature 509, 325-330 (2014
Insel, T. R., Gelhard, R., & Shapiro, L. E. The comparative distribution of forebrain receptors for neurohypophyseal peptides in monogamous and polygamous mice. Neuroscience 43, 623-630 (1991
Donaldson, Z. R., & Young, L. J. Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322, 900-904 (2008
Dawson, W. D. Fertility and size inheritance in a Peromyscus species cross. Evolution 19, 44-55 (1965
Li, H., & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009
Lunter, G., & Goodson, M. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res. 21, 936-939 (2011
Van der Auwera, G. A., et al. From FastQ data to high confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr. Protoc. Bioinformatics 11, 11.10.1-11.10.33 (2013
Painter, T. S. A comparative study of the chromosomes of mammals. Am. Nat. 59, 385-409 (1925
Greenbaum, I. F., et al. Cytogenetic nomenclature of deer mice, Peromyscus (Rodentia): revision and review of the standardized karyotype. Report of the Committee for the Standardization of Chromosomes of Peromyscus. Cytogenet. Cell Genet. 66, 181-195 (1994
Fraley, C., & Raftery, A. mclust version 4 for R: normal mixture modeling for model-based clustering, classification, and density estimation (Department of Statistics, University of Washington, 2012
Broman, K. W. R/qtlcharts: interactive graphics for quantitative trait locus mapping. Genetics 199, 359-361 (2015
Kenney-Hunt, J., et al. A genetic map of Peromyscus with chromosomal assignment of linkage groups (a Peromyscus genetic map). Mamm. Genome 25, 160-179 (2014
Li, H., et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009
Cande, J., Andolfatto, P., Prudhomme, B., Stern, D. L., & Gompel, N. Evolution of multiple additive loci caused divergence between Drosophila yakuba and D. santomea in wing rowing during male courtship. PLoS ONE 7, e43888 (2012
Lynch, M & Walsh, B. Genetics and Analysis of Quantitative Traits 469-476 (Sinauer, 1998
Broman, K. W., Wu, H., Sen, S., & Churchill, G. A. R/qtl: QTL mapping in experimental crosses. Bioinformatics 19, 889-890 (2003
Zapala, M. A., et al. Adult mouse brain gene expression patterns bear an embryologic imprint. Proc. Natl Acad. Sci. USA 102, 10357-10362 (2005
Dobin, A., et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21 (2013
Rozowsky, J., et al. AlleleSeq: analysis of allele-specific expression and binding in a network framework. Mol. Syst. Biol. 7, 522 (2011
Li, B., & Dewey, C. N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323 (2011
Ritchie, M. E., et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015
Law, C. W., Chen, Y., Shi, W., & Smyth, G. K. voom: precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol. 15, R29 (2014
Robinson, M. D., & Oshlack, A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11, R25 (2010
Benjamini, Y., & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289-300 (1995
Cingolani, P., et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. Fly 6, 80-92 (2012
Clark, R. G., Jones, P. M., & Robinson, I. C. A. F. Clearance of vasopressin from cerebrospinal fluid to blood in chronically cannulated Brattleboro rats. Neuroendocrinology 37, 242-247 (1983
Diamant, M., & De Wied, D. Differential effects of centrally injected AVP on heart rate, core temperature, and behavior in rats. Am. J. Physiol. 264, R51-R61 (1993
Pedersen, C. A., Ascher, J. A., Monroe, Y. L., & Prange, A. J., Jr. Oxytocin induces maternal behavior in virgin female rats. Science 216, 648-650 (1982
Fahrbach, S. E., Morrell, J. I., & Pfaff, D. W. Oxytocin induction of short-latency maternal behavior in nulliparous, estrogen-primed female rats. Horm. Behav. 18, 267-286 (1984
Winslow, J. T., Hastings, N., Carter, C. S., Harbaugh, C. R., & Insel, T. R. A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365, 545-548 (1993
Kessler, M. S., Bosch, O. J., Bunck, M., Landgraf, R., & Neumann, I. D. Maternal care differs in mice bred for high vs. low trait anxiety: impact of brain vasopressin and cross-fostering. Soc. Neurosci. 6, 156-168 (2011
Bosch, O. J., & Neumann, I. D. Brain vasopressin is an important regulator of maternal behavior independent of dams? trait anxiety. Proc. Natl Acad. Sci. USA 105, 17139-17144 (2008
Kuroda, K. O., Tachikawa, K., Yoshida, S., Tsuneoka, Y., & Numan, M. Neuromolecular basis of parental behavior in laboratory mice and rats: with special emphasis on technical issues of using mouse genetics. Prog. Neuropsychopharmacol. Biol. Psychiatry 35, 1205-1231 (2011
Xu, X., et al. Modular genetic control of sexually dimorphic behaviors. Cell 148, 596-607 (2012
