Prolactin Receptor Gene Diversity in Azara's Owl Monkeys (Aotus azarai) and Humans (Homo sapiens) Suggests a Non-Neutral Evolutionary History among Primates

International Journal of Primatology

Volumn 35, Issue 1, 2014, Pages 129-155

  Babb, Paul L ^a,b   McIntosh, Annick M ^c   Fernandez Duque, Eduardo ^a,d   Schurr, Theodore G ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c YALE UNIVERSITY   (United States)

^d Centro de Ecologia Aplicada del Littoral   (Argentina)

Author keywords

Behavioral genetics; Night monkey; Paternal care; Platyrrhini; PRLR

Indexed keywords

EID: 84893610216     PISSN: 01640291     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10764-013-9721-9     Document Type: Article

References (107)

1. 1000 Genomes Project Consortium. (2010). A map of human genome variation from population-scale sequencing. Nature, 467(7319), 1061-1073.
2. 1000 Genomes Project Consortium. (2012). An integrated map of genetic variation from 1092 human genomes. Nature, 491(7422), 56-65.
3. Almond, R. E., Brown, G. R., & Keverne, E. B. (2006). Suppression of prolactin does not reduce infant care by parentally experienced male common marmosets (Callithrix jacchus). Hormones and Behavior, 49(5), 673-680.
4. Altekar, G., Dwarkadas, S., Huelsenbeck, J. P., & Ronquist, F. (2004). Parallel metropolis coupled Markov Chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics, 20(3), 407-415.
5. Babb, P. L., Fernandez-Duque, E., & Schurr, T. G. (2010). AVPR1A sequence variation in monogamous owl monkeys (Aotus azarai) and its implications for the evolution of platyrrhine social behavior. Journal of Molecular Evolution, 71(4), 279-297.
6. Babb, P. L., Fernandez-Duque, E., Baiduc, C. A., Gagneux, P., Evans, S., & Schurr, T. G. (2011). mtDNA diversity in Azara's owl monkeys (Aotus azarai azarai) of the Argentinean Chaco. American Journal of Physical Anthropology, 146(2), 209-224.
7. Bandelt, H. J., & Parson, W. (2008). Consistent treatment of length variants in the human mtDNA control region, a reappraisal. International Journal of Legal Medicine, 122(1), 11-21.
8. Bandelt, H. J., Forster, P., & Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16(1), 37-48.
9. Beard, K. C., & Wang, J. (2004). The eosimiid primates (Anthropoidea) of the Heti Formation, Yuanqu Basin, Shanxi and Henan Provinces, People's Republic of China. Journal of Human Evolution, 46(4), 401-432.
10. Ben-Jonathan, N., LaPensee, C. R., & LaPensee, E. W. (2008). What can we learn from rodents about prolactin in humans? Endocrine Reviews, 29(1), 1-41.
11. Bentley, D. R., Balasubramanian, S., Swerdlow, H. P., Smith, G. P., Milton, J., Brown, C. G., et al. (2008). Accurate whole human genome sequencing using reversible terminator chemistry. Nature, 456(7218), 53-59.
12. Bole-Feysot, C., Goffin, V., Edery, M., Binart, N., & Kelly, P. A. (1998). Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocrine Reviews, 19(3), 225-268.
13. Briggs, A. W., Stenzel, U., Johnson, P. L., Green, R. E., Kelso, J., Prüfer, K., et al. (2007). Patterns of damage in genomic DNA sequences from a Neandertal. Proceedings of the National Academy of Sciences of the United States of America, 104(37), 14616-14621.
14. Brooks, P. L., Vella, E. T., & Wynne-Edwards, K. E. (2005). Dopamine agonist treatment before and after the birth reduces prolactin concentration but does not impair paternal responsiveness in Djungarian hamsters Phodopus campbelli. Hormones and Behavior, 47(3), 358-366.
15. Burley, N. T., & Johnson, K. (2002). The evolution of avian parental care. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 357(1419), 241-250.
16. Chen, F. C., & Li, W. H. (2001). Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. American Journal of Human Genetics, 68(2), 444-456.
17. Clutton-Brock, T. H. (1991). The evolution of parental care. Princeton: Princeton University Press.
18. Dalrymple, A., Edery, M., & Jabbour, H. N. (2000). Sequence and functional characterisation of the marmoset monkey (Callithrix jacchus) prolactin receptor: comparative homology with the human long-form prolactin receptor. Molecular and Cellular Endocrinology, 167(1-2), 89-97.
19. Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.
20. Dixson, A. F., & George, L. (1982). Prolactin and parental behaviour in a male New World primate. Nature, 299, 551-553.
21. Don, R. H., Cox, P. T., Wainwright, B. J., Baker, K., & Mattick, J. S. (1991). Touchdown PCR to circumvent spurious priming during gene amplification. Nucleic Acids Research, 19(14), 4008.
22. Drummond, A. J., & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
23. Drummond, A. J., Ho, S. Y. W., Phillips, M. J., & Rambaut, A. (2006). Relaxed phylogenetics and dating with confidence. PLoS Biology, 4(5), e88.
24. Drummond, A. J., Ashton, B., Cheung, M., Heled, J., Kearse, M., Moir, R., Stones-Havas, S., Thierer, T., Wilson, A. (2010). Geneious v5. 0. Available at: http://www. geneious. com.
25. Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite ver 3. 5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564-567.
26. Felsenstein, J. (2005). PHYLIP (Phylogeny Inference Package) version 3. 6. Distributed by the author. Seattle: Department of Genome Sciences, University of Washington.
27. Fernandez-Duque, E. (2012). Owl monkeys Aotus spp in the wild and in captivity. International Zoo Yearbook, 46(1), 89-94.
28. Fernandez-Duque, E., & Huck, M. (2013). Till death (or an intruder) do us part: intrasexual- competition in a monogamous primate. PLoS One, 8(1), e53724.
29. Fernandez-Duque, E., Rotundo, M., & Sloan, C. (2001). Density and population structure of owl monkeys (Aotus azarai) in the Argentinean Chaco. American Journal of Primatology, 53(3), 99-108.
30. Fernandez-Duque, E., Juárez, C. P., & Di Fiore, A. (2008). Adult male replacement and subsequent infant care by male and siblings in socially monogamous owl monkeys (Aotus azarai). Primates, 49, 81-84.
31. Fernandez-Duque, E., Valeggia, C., & Mendoza, S. P. (2009). The biology of paternal care in human and nonhuman primates. Annual Review of Anthropology, 38, 115-130.
32. Flicek, P., Amode, M. R., Barrell, D., Beal, K., Brent, S., Chen, Y., et al. (2011). Ensembl 2011. Nucleic Acids Research, 39, D800-D806.
33. Goffin, V., Binart, N., Touraine, P., & Kelly, P. A. (2002). Prolactin: the new biology of an old hormone. Annual Review of Physiology, 64, 47-67.
34. Gordon, I., Zagoory-Sharon, O., Leckman, J. F., & Feldman, R. (2010). Prolactin, oxytocin, and the development of paternal behavior across the first six months of fatherhood. Hormones and Behavior, 58(3), 513-518.
35. Green, R. E., Krause, J., Ptak, S. E., Briggs, A. W., Ronan, M. T., Simons, J. F., et al. (2006). Analysis of one million base pairs of Neanderthal DNA. Nature, 444(7117), 330-336.
36. Green, R. E., Krause, J., Briggs, A. W., Maricic, T., Stenzel, U., Kircher, M., et al. (2010). A draft sequence of the Neandertal Genome. Science, 328(5979), 710-722.
37. Gubernick, D. J., & Nelson, R. J. (1989). Prolactin and paternal behavior in the biparental California mouse, Peromyscus californicus. Hormones and Behavior, 23(2), 203-210.
38. Gubernick, D. J., & Teferi, T. (2000). Adaptive significance of male parental care in a monogamous mammal. Proceedings of the Royal Society B: Biological Sciences, 267(1439), 147-150.
39. Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate method to estimate large phylogenies by maximum-likelihood. Systems Biology, 52(5), 696-704.
40. Hartwig, W. C., & Meldrum, D. J. (2002). Miocene platyrrhines of the northern Neotropics. In W. C. Hartwig (Ed.), The primate fossil record (pp. 175-188). Cambridge: Cambridge University Press.
41. He, X., & Zhang, J. (2006). Toward a molecular understanding of pleiotropy. Genetics, 173(4), 1885-1891.
42. Henikoff, S., & Henikoff, J. G. (1992). Amino acid substitution matrices from protein blocks. Proceedings of the National Academy of Sciences of the United States of America, 89(22), 10915-10919.
43. Hodgson, J. A., Sterner, K. N., Matthews, L. J., Burrell, A. S., Jani, R. A., Raaum, R. L., et al. (2009). Successive radiations, not stasis, in the South American primate fauna. Proceedings of the National Academy of Sciences of the United States of America, 106(14), 5534-5539.
44. Horseman, N. D., Zhao, W., Montecino-Rodriguez, E., Tanaka, M., Nakashima, K., Engle, S. J., et al. (1997). Defective mammopoiesis, but normal hematopoiesis, in mice with a targeted disruption of the prolactin gene. EMBO Journal, 16(23), 6926-6935.
45. Hu, Z. Z., Zhuang, L., Meng, J., Tsai-Morris, C. H., & Dufau, M. L. (2002). Complex 5′ genomic structure of the human prolactin receptor: multiple alternative exons 1 and promoter utilization. Endocrinology, 143(6), 2139-2142.
46. Huck, M., & Fernandez-Duque, E. (2012). Children of divorce: effects of adult replacements on previous offspring in Argentinean owl monkeys. Behavioral Ecology and Sociobiology, 66(3), 505-517.
47. Huelsenbeck, J. P., & Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17(8), 754-755.
48. Iafrate, A. J., Feuk, L., Rivera, M. N., Listewnik, M. L., Donahoe, P. K., Qi, Y., et al. (2004). Detection of large-scale variation in the human genome. Nature Genetics, 36(9), 949-951.
49. Karolchik, D., Kuhn, R. M., Baertsch, R., Barber, G. P., Clawson, H., Diekhans, M., et al. (2008). The UCSC genome browser database: 2008 update. Nucleic Acids Research, 36, 773-779.
50. Keinan, A., & Clark, A. (2012). Recent explosive human population growth has resulted in an excess of rare genetic variants. Science, 336(6082), 740-743.
51. Kent, W. J., Sugnet, C. W., Furey, T. S., Roskin, K. M., Pringle, T. H., Zahler, A. M., et al. (2002). The human genome browser at UCSC. Genome Research, 12(6), 996-1006.
52. Khong, H. K., Kuah, M. K., Jaya-Ram, A., & Shu-Chien, A. C. (2009). Prolactin receptor mRNA is upregulated in discus fish (Symphysodon aequifasciata) skin during parental phase. Comparative Biochemistry and Physiology - Part B, 153(1), 18-28.
53. Kimura, M. (1981). Estimation of evolutionary distances between homologous nucleotide sequences. Proceedings of the National Academy of Sciences of the United States of America, 78(1), 454-458.
54. Korbie, D. J., & Mattick, J. S. (2008). Touchdown PCR for increased specificity and sensitivity in PCR amplification. Nature Protocols, 3(9), 1452-1456.
55. Lebrun, J. J., Ali, S., Goffin, V., Ullrich, A., & Kelly, P. A. (1995a). A single tyrosine residue of the prolactin receptor is responsible for activation of gene transcription. Proceedings of the National Academy of Sciences of the United States of America, 92, 4031-4035.
56. Lebrun, J. J., Ali, S., Ullrich, A., & Kelly, P. A. (1995b). Proline-rich sequence mediated Jak2 association to the prolactin receptor is required but not sufficient for signal transduction. Journal of Biological Chemistry, 270, 10664-10670.
57. Lucas, B. K., Ormandy, C. J., Binart, N., Bridges, R. S., & Kelly, P. A. (1998). Null mutation of the prolactin receptor gene produces a defect in maternal behavior. Endocrinology, 139(10), 4102-4107.
58. Ma, E., Lau, J., Grattan, D. R., Lovejoy, D. A., & Wynne-Edwards, K. E. (2005). Male and female prolactin receptor mRNA expression in the brain of a biparental and a uniparental hamster, Phodopus, before and after the birth of a litter. Journal of Neuroendocrinology, 17(2), 81-90.
59. Maynard-Smith, J. (1977). Parental investment: a prospective analysis. Animal Behaviour, 25(1), 1-9.
60. Miller, E. R., & Simons, E. L. (1997). Dentition of Proteopithecus sylviae, an archaic anthropoid from the Fayum, Egypt. Proceedings of the National Academy of Sciences of the United States of America, 94(25), 13760-13764.
61. Mills, R. E., Luttig, C. T., Larkins, C. E., Beauchamp, A., Tsul, C., Pittard, W. S., et al. (2006). An initial map of insertion and deletion (INDEL) variation in the human genome. Genome Research, 16(9), 1182-1890.
62. Mota, M. T., & de Sousa, M. B. (2000). Prolactin levels of fathers and helpers related to alloparental care in common marmosets, Callithrix jacchus. Folia Primatologica, 71, 22-26.
63. Mota, M. T., Franci, C. R., & de Sousa, M. B. C. (2006). Hormonal changes related to paternal and alloparental care in common marmosets (Callithrix jacchus). Hormones and Behavior, 49(3), 293-302.
64. Neuman, M., & Insel, R. (2003). The neurobiology of parental behaviour. New York: Springer Science+Business Media.
65. Noonan, J. P. (2010). Neanderthal genomics and the evolution of modern humans. Genome Research, 20(5), 547-553.
66. Noonan, J. P., Coop, G., Kudaravalli, S., Smith, D., Krause, J., Alessi, J., et al. (2006). Sequencing and analysis of Neanderthal genomic DNA. Science, 314(5802), 1113-1118.
67. Ormandy, C. J., Camus, A., Barra, J., Damotte, D., Lucas, B., Buteau, H., et al. (1997). Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes and Development, 11(2), 167-178.
68. Paradis, E. (2010). pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics, 26, 419-420.
69. Perelman, P., Johnson, W. E., Roos, C., Seuánez, H. N., Horvath, J. E., Moreira, M. A. M., et al. (2011). A molecular phylogeny of living primates. PLoS Genetics, 7(3), e1001342.
70. Perrot-Applanat, M., Gualillo, O., Pezet, A., Vincent, V., Edery, M., & Kelly, P. A. (1997). Dominant negative and cooperative effects of mutant forms of prolactin receptor. Molecular Endocrinology, 11(8), 1020-1032.
71. Pezet, A., Buteau, H., Kelly, P. A., & Edery, M. (1997a). The last proline of Box 1 is essential for association with JAK2 and functional activation of the prolactin receptor. Molecular and Cellular Endocrinology, 129(2), 199-208.
72. Pezet, A., Ferrag, F., Kelly, P. A., & Edery, M. (1997b). Tyrosine docking sites of the rat prolactin receptor required for association and activation of stat5. Journal of Biological Chemistry, 272(40), 25043-25050.
73. Qazi, A. M., Tsai-Morris, C. H., & Dufau, M. L. (2006). Ligand-independent homo- and heterodimerization of human prolactin receptor variants: inhibitory action of the short forms by heterodimerization. Molecular Endocrinology, 20(8), 1912-1923.
74. R Core Team. (2012). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: http://www. R-project. org/.
75. Rambaut, A., & Drummond, A. J. (2007). Tracer v1. 5. Available at: http://beast. bio. ed. ac. uk/Tracer.
76. Reburn, C. J., & Wynne-Edwards, K. E. (1999). Hormonal changes in males of a naturally biparental and a uniparental mammal. Hormones and Behavior, 35(2), 163-176.
77. Rojas-Garcia, P. P., Germain, A., Torres-Farfan, C. L., Richter, H. G., Campino, C., Seron-Ferre, M. J. (2003). Expression of prolactin (PRL) receptor in ovary of capuchin monkey. Initial studies. Submitted to EMBL/GenBank/DDBJ databases, accession number: AY227708.
78. Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19(12), 1572-1574.
79. Rotundo, M., Fernandez-Duque, E., & Dixson, A. (2005). Infant development and parental care in free-ranging Aotus azarai azarai in Argentina. International Journal of Primatology, 26(6), 1459-1473.
80. Rozakis-Adcock, M., & Kelly, P. A. (1991). Mutational analysis of the ligand-binding domain of the prolactin receptor. Journal of Biological Chemistry, 266(25), 16472-16477.
81. Rozakis-Adcock, M., & Kelly, P. A. (1992). Identification of ligand-binding determinants of the prolactin receptor. Journal of Biological Chemistry, 267(11), 7428-7433.
82. Rozen, S., & Skaletsky, H. J. (2000). Primer3 on the WWW for general users and for biologist programmers. In S. Krawetz & S. Misener (Eds.), Methods in molecular biology (pp. 365-386). Totowa: Humana Press.
83. Schradin, C. (2008). Differences in prolactin levels between three alternative male reproductive tactics in striped mice (Rhabdomys pumilio). Proceedings of the Royal Society B: Biological Sciences, 275(1638), 1047-1052.
84. Schradin, C., & Anzenberger, G. (1999). Prolactin, the hormone of paternity. News in Physiological Sciences, 14, 223-231.
85. Schradin, C., & Pillay, N. (2004). Prolactin levels in paternal striped mouse (Rhabdomys pumilio) fathers. Physiology and Behavior, 81(1), 43-50.
86. Schradin, C., Reeder, D. M., Mendoza, S. P., & Anzenberger, G. (2003). Prolactin and paternal care: comparison of three species of monogamous new world monkeys (Callicebus cupreus, Callithrix jacchus, and Callimico goeldii). Journal of Comparative Psychology, 117(2), 166-175.
87. Serre, D., Langaney, A., Chech, M., Teschler-Nicola, M., Paunovic, M., Mennecier, P., et al. (2004). No evidence of Neandertal mtDNA contribution to early modern humans. PLoS Biology, 2(3), e57.
88. Setoguchi, T., & Rosenberger, A. L. (1987). A fossil owl monkey from La Venta, Colombia. Nature, 326(6114), 692-694.
89. Simons, E. L., Rasmussen, D. T., & Gebo, D. L. (1987). A new species of Propliopithecus from the Fayum, Egypt. American Journal of Physical Anthropology, 73(2), 139-147.
90. Smuts, B. B., & Gubernick, D. J. (1992). Male-infant relationships in nonhuman primates: Paternal investment or mating effort? In B. S. Hewlett (Ed.), Father-child relations: Cultural and biosocial contexts (pp. 1-30). New York: Aldine de Gruyter.
91. Somers, W., Ultsch, M., De Vos, A. M., & Kossiakoff, A. A. (1994). The x-ray structure of a growth-hormone prolactin receptor complex. Nature, 372(6505), 478-481.
92. Storey, A. E., Walsh, C. J., Quinton, R. L., & Wynne-Edwards, K. E. (2000). Hormonal correlates of paternal responsiveness in new and expectant fathers. Evolution and Human Behavior, 21(2), 79-95.
93. Swofford, D. L. (2002). PAUP*: Phylogenetic analysis using parsimony (and other methods), version 4. 0b10 beta. Sunderland: Sinauer Associates.
94. Tajima, F. (1989a). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123(3), 585-595.
95. Tajima, F. (1989b). The effect of change in population size on DNA polymorphism. Genetics, 123(3), 597-601.
96. Takai, M., Anaya, F., Shigehara, N., & Steoguchi, T. (2000). New fossil materials of the earliest New World monkey, Branisella boliviana, and the problem of platyrrhine origins. American Journal of Physical Anthropology, 111(2), 263-281.
97. Tejedor, M. F., Tauber, A. A., Rosenberger, A. L., Swisher, C. C., 3rd, & Palacios, M. E. (2006). New primate genus from the Miocene of Argentina. Proceedings of the National Academy of Sciences of the United States of America, 103(14), 5437-5441.
98. The Chimpanzee Sequencing and Analysis Consortium (2005). Initial sequence of the chimpanzee genome and comparison with the human genome. Nature, 437, 69-87.
99. Wang, J., Wang, W., Li, R., Li, Y., Tian, G., Goodman, L., et al. (2008). The diploid genome sequence of an Asian individual. Nature, 456(7218), 60-65.
100. Wheeler, D. A., Srinivasan, M., Egholm, M., Shen, Y., Chen, L., McGuire, A., et al. (2008). The complete genome of an individual by massively parallel DNA sequencing. Nature, 452(7189), 872-876.
101. Wolovich, C. K., Perea-Rodriguez, J. P., & Fernandez-Duque, E. (2008). Food transfers to young and mates in wild owl monkeys (Aotus azarai). American Journal of Primatology, 70(3), 211-221.
102. Wright, P. C. (1990). Patterns of paternal care in primates. International Journal of Primatology, 11(2), 89-102.
103. Wright, P. C. (1994). The behavior and ecology of the owl monkey. In J. F. Baer, R. E. Weller, & I. Kakoma (Eds.), Aotus: The owl monkey (pp. 97-113). San Diego: Academic Press.
104. Wynne-Edwards, K. E., & Reburn, C. J. (2000). Behavioral endocrinology of mammalian fatherhood. Trends in Ecology & Evolution, 15(11), 464-468.
105. Yang, Z. (2007). PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24(8), 1586-1591.
106. Ziegler, T. E., Wegner, F. H., & Snowdon, C. T. (1996). Hormonal responses to parental and nonparental conditions in male cotton-top tamarins, Saguinus oedipus, a New World primate. Hormones and Behavior, 30(3), 287-297.
107. Ziegler, T. E., Washabaugh, K. F., & Snowdon, C. T. (2004). Responsiveness of expectant male cotton-top tamarins, Saguinus oedipus, to mate's pregnancy. Hormones and Behavior, 45(2), 84-92.