A mechanism for population self-regulation: Social density suppresses GnRH expression and reduces reproductivity in voles.
androgens
early life programming
epigenetics
field study
methylation
population cycles
reproductive suppression
vole and lemming cycles
Journal
The Journal of animal ecology
ISSN: 1365-2656
Titre abrégé: J Anim Ecol
Pays: England
ID NLM: 0376574
Informations de publication
Date de publication:
04 2021
04 2021
Historique:
received:
04
09
2020
accepted:
11
01
2021
pubmed:
8
2
2021
medline:
20
4
2021
entrez:
7
2
2021
Statut:
ppublish
Résumé
Nearly 100 years ago, Charles Elton described lemming and vole population cycles as ecological models for understanding population regulation in nature. Yet, the mechanisms driving these cycles are still not fully understood. These rodent populations can continue to cycle in the absence of predation and with food supplementation, and represent a major unsolved problem in population ecology. It has been hypothesized that the social environment at high population density can drive selection for a low-reproduction phenotype, resulting in population self-regulation as an intrinsic mechanism driving the cycles. However, a physiological mechanism for this self-regulation has not been demonstrated. We manipulated population density in wild meadow voles Microtus pennsylvanicus using large-scale field enclosures over 3 years and examined reproductive performance and physiology. Within the field enclosures, we assessed the proportion of breeding animals, mass at sexual maturation, and faecal androgen and oestrogen metabolites. We then collected brain tissue from juvenile voles born at high or low density, quantified mRNA expression of gonadotropin-releasing hormone (GnRH) and oestrogen receptor alpha (ERα) and measured DNA methylation at six CpG sites in a region that was highly conserved with the mouse GnRH promoter. At high density, there was a lower proportion of reproductive animals. Juvenile voles born at high densities had reduced expression of GnRH in the hypothalamus, accompanied by marginally lower faecal sex hormone metabolites. Female juvenile voles born at high density also had higher methylation levels at two CpG sites while males did not, aligning with prior observations that females (but not males) from high-density environments retain reduced reproduction long term. Our results support a physiological basis for population self-regulation in vole cycles, as altering population density alone induced reproductive downregulation at the hypothalamic level. Our results demonstrate that altering the early-life social environment can fundamentally impact reproductive function in the brain. This, in turn, can drive population demography changes in wild animals.
Identifiants
pubmed: 33550586
doi: 10.1111/1365-2656.13430
doi:
Substances chimiques
Gonadotropin-Releasing Hormone
33515-09-2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
784-795Informations de copyright
© 2021 British Ecological Society.
Références
Alvarado, S. G., Lenkov, K., Williams, B., & Fernald, R. D. (2015). Social crowding during development causes changes in GnRH1 DNA methylation. PLoS ONE, 10, e0142043. https://doi.org/10.1371/journal.pone.0142043
Bates, D., Maechler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 1-48.
Berger, S. L. (2007). The complex language of chromatin regulation during transcription. Nature, 447, 407-412. https://doi.org/10.1038/nature05915
Bian, J. H., Du, S. Y., Wu, Y., Cao, Y. F., Nie, X. H., He, H., & You, Z. B. (2015). Maternal effects and population regulation: Maternal density-induced reproduction suppression impairs offspring capacity in response to immediate environment in root voles Microtus oeconomus. Journal of Animal Ecology, 84, 326-336.
Boonstra, R. (1977). Effect of conspecifics on survival during population declines in Microtus townsendii. Journal of Animal Ecology, 46, 835-851. https://doi.org/10.2307/3644
Boonstra, R. (1985). Demography of Microtus pennsylvanicus in southern Ontario: Enumeration versus Jolly-Seber estimation compared. Canadian Journal of Zoology, 63, 1174-1180.
Boonstra, R. (1989). Life history variation in maturation in fluctuating meadow vole populations (Microtus pennsylvanicus). Oikos, 54, 265-274. https://doi.org/10.2307/3565284
Boonstra, R., & Boag, P. T. (1987). A test of the Chitty hypothesis: Inheritance of life history traits in meadow voles Microtus pennsylvanicus. Evolution, 41, 929-947.
Boonstra, R., & Hochachka, W. (1997). Maternal effects and additive genetic inheritance in the collared lemming (Dicrostonyx groenlandicus). Evolutionary Ecology, 11, 169-182. https://doi.org/10.1023/A:1018447815825
Boonstra, R., Krebs, C. J., & Stenseth, N. C. (1998). Population cycles in small mammals: The problem of explaining the low phase. Ecology, 79, 1479-1488.
Boonstra, R., & Rodd, F. H. (1983). Regulation of breeding density in Microtus pennsylvanicus. Journal of Animal Ecology, 52, 757-780. https://doi.org/10.2307/4452
Bossdorf, O., Richards, C. L., & Pigliucci, M. (2008). Epigenetics for ecologists. Ecology Letters, 11, 106-115.
Champagne, F. A., Weaver, I. C., Diorio, J., Dymov, S., Szyf, M., & Meaney, M. J. (2006). Maternal care associated with methylation of the estrogen receptor-α1b promoter and estrogen receptor-α expression in the medial preoptic area of female offspring. Endocrinology, 147, 2909-2915. https://doi.org/10.1210/en.2005-1119
Chitty, D. (1960). Population processes in the vole and their relevance to general theory. Canadian Journal of Zoology, 38, 99-113. https://doi.org/10.1139/z60-011
Chitty, D. (1967). The natural selection of self-regulatory behaviour in animal populations. Proceedings of the Ecological Society of Australia, 2, 51-78.
Cole, F., & Batzli, G. (1978). Influence of supplemental feeding on a vole population. Journal of Mammalogy, 59, 809-819. https://doi.org/10.2307/1380145
Cushing, B. S., Razzoli, M., Murphy, A. Z., Epperson, P. M., Le, W. W., & Hoffman, G. E. (2004). Intraspecific variation in estrogen receptor alpha and the expression of male sociosexual behavior in two populations of prairie voles. Brain Research, 1016, 247-254. https://doi.org/10.1016/j.brainres.2004.05.010
Dantzer, B., McAdam, A. G., Palme, R., Humphries, M. M., Boutin, S., & Boonstra, R. (2011). Maternal androgens and behaviour in free-ranging North American red squirrels. Animal Behaviour, 81, 469-479. https://doi.org/10.1016/j.anbehav.2010.11.021
DiVall, S. A., Radovick, S., & Wolfe, A. (2007). Egr-1 binds the GnRH promoter to mediate the increase in gene expression by insulin. Molecular and Cellular Endocrinology, 270, 64-72. https://doi.org/10.1016/j.mce.2007.02.007
Edwards, P. (2020). Data from: Social density suppresses GnRH expression in voles. figshare, https://doi.org/10.6084/m9.figshare.13256918.v1
Edwards, P. D., Dean, E. K., Palme, R., & Boonstra, R. (2019). Assessing space use in meadow voles: The relationship to reproduction and the stress axis. Journal of Mammalogy, 100, 4-12. https://doi.org/10.1093/jmammal/gyy161
Elton, C. S. (1924). Periodic fluctuations in the numbers of animals: Their causes and effects. British Journal of Experimental Biology, 2, 119-163.
Feng, T., An, S., Kinden, R., Zhang, X., Jia, R., & Tai, F. (2019). Alteration in oxytocin levels induced by early social environment affects maternal behavior and estrogen receptor alpha in mandarin voles (Microtus mandarinus). Behavioural Brain Research, 365, 36-47. https://doi.org/10.1016/j.bbr.2019.02.038
Getz, L. L., Cole, F. R., Verner, L., Hofmann, J. E., & Avalos, D. (1979). Comparisons of population demography of Microtus ochrogaster and M. pennsylvanicus. Acta Theriologica, 24, 319-349. https://doi.org/10.4098/AT.arch.79-31
Horie, K., Inoue, K., Suzuki, S., Adachi, S., Yada, S., Hirayama, T., Hidema, S., Young, L. J., & Nishimori, K. (2019). Oxytocin receptor knockout prairie voles generated by CRISPR/Cas9 editing show reduced preference for social novelty and exaggerated repetitive behaviors. Hormones and Behavior, 111, 60-69. https://doi.org/10.1016/j.yhbeh.2018.10.011
Horton, B. M., Hudson, W. H., Ortlund, E. A., Shirk, S., Thomas, J. W., Young, E. R., & Maney, D. L. (2014). Estrogen receptor α polymorphism in a species with alternative behavioral phenotypes. Proceedings of the National Academy of Sciences of the United States of America, 111, 1443-1448.
Johnsen, K., Devineau, O., & Andreassen, H. P. (2019). Phase-and season-dependent changes in social behaviour in cyclic vole populations. BMC Ecology, 19, 5. https://doi.org/10.1186/s12898-019-0222-3
Keebaugh, A. C., & Young, L. J. (2011). Increasing oxytocin receptor expression in the nucleus accumbens of pre-pubertal female prairie voles enhances alloparental responsiveness and partner preference formation as adults. Hormones and Behavior, 60, 498-504. https://doi.org/10.1016/j.yhbeh.2011.07.018
Keller, S. M., Doherty, T. S., & Roth, T. L. (2018). Pharmacological manipulation of DNA methylation in adult female rats normalizes behavioral consequences of early-life maltreatment. Frontiers in Behavioral Neuroscience, 12, 126. https://doi.org/10.3389/fnbeh.2018.00126
Kent, W. J., Sugnet, C. W., Furey, T. S., Roskin, K. M., Pringle, T. H., Zahler, A. M., & Haussler, D. (2002). The human genome browser at UCSC. Genome Research, 12, 996-1006.Retrieved from http://genome.ucsc.edu/
Krebs, C. J. (1966). Demographic changes in fluctuating populations of Microtus californicus. Ecological Monographs, 36, 239-273. https://doi.org/10.2307/1942418
Krebs, C. J. (2002). Two complementary paradigms for analysing population dynamics. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 357, 1211-1219. https://doi.org/10.1098/rstb.2002.1122
Krebs, C. J. (2009). Population dynamics of large and small mammals: Graeme Caughley's grand vision. Wildlife Research, 36, 1-7. https://doi.org/10.1071/WR08004
Krebs, C. J. (2013). Population fluctuations in rodents. The University of Chicago Press.
Krebs, C. J. (2020). Whither mammalian ecology? Journal of Mammalogy, 101(5), 1224-1230. https://doi.org/10.1093/jmammal/gyaa072
Krebs, C. J., Gaines, M. S., Keller, B. L., Myers, J. H., & Tamarin, R. H. (1973). Population cycles in small rodents: Demographic and genetic events are closely coupled in fluctuating populations of field mice. Science, 179, 35-41. https://doi.org/10.1126/science.179.4068.35
Krebs, C. J., Keller, B. L., & Tamarin, R. H. (1969). Microtus population biology: Demographic changes in fluctuating populations of M. ochrogaster and M. pennsylvanicus in southern Indiana. Ecology, 50, 587-607. https://doi.org/10.2307/1936248
Kriegsfeld, L. J., & Nelson, R. J. (1999). Photoperiod affects the gonadotropin-releasing hormone neuronal system of male prairie voles (Microtus ochrogaster). Neuroendocrinology, 69, 238-244.
Kurian, J. R., & Terasawa, E. (2013). Epigenetic control of gonadotropin releasing hormone neurons. Frontiers in Endocrinology, 4, 61. https://doi.org/10.3389/fendo.2013.00061
Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., Byrnes, E. J., Chen, L., Chen, L. I., Chen, T.-M., Chi Chin, M., Chong, J., Crook, B. E., Czaplinska, A., Dang, C. N., Datta, S., … Jones, A. R. (2007). Genome-wide atlas of gene expression in the adult mouse brain. Nature, 445, 168-176. https://doi.org/10.1038/nature05453
Li, L. C., & Dahiya, R. (2002). MethPrimer: Designing primers for methylation PCRs. Bioinformatics, 18, 1427-1431. https://doi.org/10.1093/bioinformatics/18.11.1427
Madison, D. M. (1980). Space use and social structure in meadow voles, Microtus pennsylvanicus. Behavioral Ecology and Sociobiology, 7, 65-71. https://doi.org/10.1007/BF00302520
Mallon, E. B., Amarasinghe, H. E., & Ott, S. R. (2016). Acute and chronic gregarisation are associated with distinct DNA methylation fingerprints in desert locusts. Scientific Reports, 6, 35608. https://doi.org/10.1038/srep35608
Marcstrom, V., Kenward, R. E., & Engren, E. (1988). The impact of predation on boreal tetraonids during vole cycles: An experimental study. Journal of Animal Ecology, 57, 859-872. https://doi.org/10.2307/5097
Maron, J. L., Pearson, D. E., & Fletcher Jr., R. J. (2010). Counterintuitive effects of largescale predator removal on a midlatitude rodent community. Ecology, 91, 3719-3728. https://doi.org/10.1890/10-0160.1
Maruska, K. P., & Fernald, R. D. (2011). Social regulation of gene expression in the hypothalamic-pituitary-gonadal axis. Physiology, 26, 412-423. https://doi.org/10.1152/physiol.00032.2011
Massey, A., & Vandenbergh, J. G. (1980). Puberty delay by a urinary cue from female house mice in feral populations. Science, 209, 821-822. https://doi.org/10.1126/science.7190728
Mihok, S. (1979). Behavioral structure and demography of subarctic Clethrionomys glareolus and Peromyscus maniculatus. Canadian Journal of Zoology, 57, 1520-1535.
Mihok, S., & Boonstra, R. (1992). Breeding performance in captivity of meadow voles (Microtus pennsylvanicus) from decline-and increase-phase populations. Canadian Journal of Zoology, 70, 1561-1566.
Norrdahl, K., & Korpimäki, E. (2002). Changes in population structure and reproduction during a 3-yr population cycle of voles. Oikos, 96, 331-345. https://doi.org/10.1034/j.1600-0706.2002.960215.x
Novikov, E. A., Panov, V. V., & Moshkin, M. P. (2012). Density-dependent regulation in populations of northern red-backed voles (Myodes rutilus) in optimal and suboptimal habitats of southwest Siberia. Biology Bulletin Reviews, 2, 431-438. https://doi.org/10.1134/S2079086412050052
Okhovat, M., Maguire, S. M., & Phelps, S. M. (2017). Methylation of avpr1a in the cortex of wild prairie voles: Effects of CpG position and polymorphism. Royal Society Open Science, 4, 160646.
Oli, M. K. (2019). Population cycles in voles and lemmings: State of the science and future directions. Mammal Review, 49, 226-239. https://doi.org/10.1111/mam.12156
Ostfeld, R. S., Canham, C. D., & Pugh, S. R. (1993). Intrinsic density-dependent regulation of vole populations. Nature, 366, 259-261. https://doi.org/10.1038/366259a0
Ostfeld, R. S., Pugh, S. R., Seamon, J. O., & Tamarin, R. H. (1988). Space use and breeding success in a population of meadow voles. Journal of Animal Ecology, 57, 385-394.
Palme, R., & Möstl, E. (1994). Biotin-streptavidin enzyme immunoassay for the determination of oestrogens and androgens in boar feces. In S. Görög (Ed.), Advances in steroid analysis '93 (pp. 111-117). Akadémiai Kiadó.
Palme, R., Touma, C., Arias, N., Dominchin, F., & Lepschy, M. (2013). Steroid extraction: Get the best out of faecal samples. Wiener Tierarztliche Monatsschrift - Veterinary Medicine Austria, 100, 238-246.
Perkins, J. R., Dawes, J. M., McMahon, S. B., Bennett, D. L., Orengo, C., & Kohl, M. (2012). ReadqPCR and NormqPCR: R packages for the reading, quality checking and normalisation of RT-qPCR quantification cycle (Cq) data. BMC Genomics, 13, 296. https://doi.org/10.1186/1471-2164-13-296
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & R Core Team. (2020). nlme: Linear and nonlinear mixed effects models. R package version 3.1-148. Retrieved from https://CRAN.R-project.org/package=nlme
Pocock, M. J., Frantz, A. C., Cowan, D. P., White, P. C., & Searle, J. B. (2004). Tapering bias inherent in minimum number alive (MNA) population indices. Journal of Mammalogy, 85, 959-962. https://doi.org/10.1644/BPR-023
R Core Team. (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing. Retrieved from www.R-project.org
Rolland, R. M., Hunt, K. E., Kraus, S. D., & Wasser, S. K. (2005). Assessing reproductive status of right whales (Eubalaena glacialis) using fecal hormone metabolites. General and Comparative Endocrinology, 142, 308-317. https://doi.org/10.1016/j.ygcen.2005.02.002
Schmittgen, T. D., & Livak, K. J. (2008). Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3, 1101-1108. https://doi.org/10.1038/nprot.2008.73
Schwarzenberger, F., Rietschel, W., Vahala, J., Holeckova, D., Thomas, P., Maltzan, J., Baumgartner, K., & Schaftenaar, W. (2000). Fecal progesterone, estrogen, and androgen metabolites for noninvasive monitoring of reproductive function in the female Indian rhinoceros, Rhinoceros unicornis. General and Comparative Endocrinology, 119, 300-307. https://doi.org/10.1006/gcen.2000.7523
Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J., Thompson, J. D., & Higgins, D. G. (2011). Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology, 7, 539. https://doi.org/10.1038/msb.2011.75
Sinclair, A. R. E. (1989). Population regulation in animals. In J. M. Cherrett (Ed.), Ecological concepts (pp. 197-241). Blackwell Scientific Publications.
Stetzik, L., Ganshevsky, D., Lende, M. N., Roache, L. E., Musatov, S., & Cushing, B. S. (2018). Inhibiting ERα expression in the medial amygdala increases prosocial behavior in male meadow voles (Microtus pennsylvanicus). Behavioural Brain Research, 351, 42-48. https://doi.org/10.1016/j.bbr.2018.05.035
Sundell, J., Ylönen, H., & Haapakoski, M. (2019). Do phase-dependent life history traits in cyclic voles persist in a common environment? Oecologia, 190, 399-410. https://doi.org/10.1007/s00442-019-04410-3
Van Cann, J., Koskela, E., Mappes, T., Sims, A., & Watts, P. C. (2019). Intergenerational fitness effects of the early life environment in a wild rodent. Journal of Animal Ecology, 88, 1355-1365. https://doi.org/10.1111/1365-2656.13039
Verhoeven, K. J., Vonholdt, B. M., & Sork, V. L. (2016). Epigenetics in ecology and evolution: What we know and what we need to know. Molecular Ecology, 25, 1631-1638.
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., & Meaney, M. J. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7, 847-854. https://doi.org/10.1038/nn1276
Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. Springer-Verlag.
Wolff, J. O. (1997). Population regulation in mammals: An evolutionary perspective. Journal of Animal Ecology, 66, 1-13. https://doi.org/10.2307/5959
Ye, J., Coulouris, G., Zaretskaya, I., Cutcutache, I., Rozen, S., & Madden, T. L. (2012). Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics, 13, 134, https://doi.org/10.1186/1471-2105-13-134