Skip to main content

Advertisement

Log in

Trojan Genes or Transparent Genomes? Sexual Selection and Potential Impacts of Genetically Modified Animals in Natural Ecosystems

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Introgression of genetically engineered modifications (GMs) into natural populations represents a new realm for mutation theory. GMs, like mutations, have direct and pleiotropic impacts that can disrupt evolved adaptive suites. If GM males are more competitive or attractive mates, the “Trojan Gene Hypothesis” predicts potentially drastic impacts. We examined sexual selection in transgenic growth hormone (Tg) mice that are strong Trojan candidates given their exceptional size and extensive pleiotropic deficits. We hypothesized that the sophisticated olfactory abilities of females would recognize dysregulation of Tg males (the Transparent Genome Hypothesis). Females expressed interest in Tg males and their volatile scent, but when allowed nasal contact with urine (critical to mate choice) they preferred normal males. Tg male urine had reduced major urinary proteins (important in social signaling) and contained albumin and transferrin indicative of pathology. Novel Tg males failed to elicit pregnancy block in recently inseminated females (the “Bruce Effect”) whereas normal males were highly effective. Normal males expressed high aggression but Tg males were placid, non-aggressive and were largely ignored by normal males. Female mice also strongly preferred normal males over p53± knockout males in response to volatiles, contact with urine and male presence. This study suggests that conspecific discrimination of fitness may be more powerful than generally appreciated. This has great implications for introductions of GM animals and sexual selection generally.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Able, D. J. (1996). The contagion indicator hypothesis for parasite-mediated sexual selection. Proccedings National Academy of Sciences of the United States of America, 93, 2229–2233.

    CAS  Google Scholar 

  • Abrahams, M. V., & Sutterlin, A. (1999). The foraging and antipredator behaviour of growth enhanced transgenic Atlantic salmon. Animal Behavior, 58, 933–942.

    Google Scholar 

  • Agmo, A., Choleris, E., Kavaliers, M., Pfaff, D. W., & Ogawa, S. (2008). Social and sexual incentive properties of estrogen receptor α, estrogen receptor β, or oxytocin knockout mice. Genes Brain and Behavior, 7, 70–77.

    CAS  Google Scholar 

  • Agrawal, A. F., & Whitlock, M. C. (2010). Environmental duress and epistasis: How does stress affect the strength of selection on new mutations?. Trends in Ecology & Evolution, 25, 450–458.

    Google Scholar 

  • Agrawal, A. F., & Whitlock, M. C. (2012). Mutation load: The fitness of individuals in populations where deleterious alleles are abundant. Annual Review of Ecology Evolution Systematics, 43, 115–135.

    Google Scholar 

  • Ahluwalia, A., Clodfelter, K. H., & Waxman, D. J. (2004). Sexual dimorphism of rat liver gene expression: Regulatory role of growth hormone revealed by deoxyribonucleic acid microarray analysis. Molecular Endocrinology, 18, 747–760.

    CAS  PubMed  Google Scholar 

  • Aikio, S., Valosaari, K. R., & Kaitala, V. (2008). Mating preference in the invasion of growth enhanced fish. Oikos, 117, 406–414.

    Google Scholar 

  • Aksenov, V., Khanna, P., Long, J., Liu, J., Szechtman, H., Matravadia, S., et al. (2012). A complex dietary supplement improves spatial learning, increases brain size and improves mitochondrial activity in aging mice. AGE, 35, 25–33. doi:10.1007/s11357-011-9325-2.

    Google Scholar 

  • Aksenov, V., Long, J., Lokuge, S., Foster, J., Liu, J., & Rollo, C. D. (2010). A dietary intervention ameliorates age-related declines in locomotion, neurotransmitters and mitochondrial activity. Experimental Biology and Medicine, 235, 66–76.

    CAS  PubMed  Google Scholar 

  • Almroth, B. C., Johnsson, J. J., Devlin, R., & Sturve, J. (2012). Oxidative stress in growth hormone transgenic coho salmon with compressed lifespan—A model for addressing aging. Free Radical Research. doi:10.3109/10715762.2012.698009.

  • Alonso-Alvarez, C., Bertrand, S., Faivre, B., & Sorci, G. (2007). Increased susceptibility to oxidative damage as a cost of accelerated somatic growth in zebra finches. Functional Ecology, 21, 873–879.

    Google Scholar 

  • Alves, G. J., Ribeiro, A., & Palermo-Neto, J. (2012). The neuroimmune changes induced by cohabitation with an Ehrlich tumor-bearing cage mate rely on olfactory information. Brain, Behavior, and Immunity, 26, 32–39.

    CAS  PubMed  Google Scholar 

  • Alves, G. J., Vismari, L., Lazzarini, R., Merruse, J. L. B., & Palermo-Neto, J. (2010). Odor cues from tumor-bearing mice induces neuroimmune changes. Behavioral Brain Research, 214, 357–367.

    CAS  Google Scholar 

  • Andre, F., Chaput, N., Schartz, N. E. C., Flament, C., Aubert, N., Bernard, J., et al. (2004). Exosomes as potent cell-free peptide-based vaccine. I. Dendritic cell-derived exosomes transfer functional MHC Class I/peptide complexes to dendritic cells. Journal of Immunology, 172, 2126–2136.

    CAS  Google Scholar 

  • Armstrong, S. D., Robertson, D. H., Cheetham, S. A., Hurst, J. L., & Beynon, R. J. (2005). Structural and functional differences in isoforms of mouse major urinary proteins: A male-specific protein that preferentially binds a male pheromone. Biochemistry Journal, 391, 343–350.

    CAS  Google Scholar 

  • Balseiro, S. C., & Correia, H. R. (2006). Is olfactory detection of human cancer by dogs based on major histocompatibility complex dependent odour components? A possible cure and a precocious diagnosis of cancer. Medical Hypotheses, 66, 270–272.

    CAS  PubMed  Google Scholar 

  • Baranowska, I., & Plonka, J. (2008). Determination of biogenic amines and vitamins in urine samples with HPLC. Journal of Liquid Chromatography and Related Technology, 31, 2974–2987.

    CAS  Google Scholar 

  • Bartke, A. (2011). Pleiotropic effects of growth hormone signaling in aging. Trends in Endocrinology and Metabolism, 22, 437–442.

    CAS  PubMed  Google Scholar 

  • Bartke, A., Cecim, M., Tang, K., Steger, R. W., Chandrashekar, V., & Turyn, D. (1994). Neuroendocrine and reproductive consequences of overexpression of growth hormone in transgenic mice. Proceedings of the Society for Experimental Biology and Medicine, 206, 345–359.

    CAS  PubMed  Google Scholar 

  • Bartke, A., Chandrashekar, V., Turyn, D., Steger, R. W., Debeljuk, L., Winters, T. A., et al. (1999). Effects of growth hormone overexpression and growth hormone resistance on neuroendocrine and reproductive functions in transgenic and knock-out mice. Proceedings of the Society for Experimental Biology and Medicine, 222, 113–123.

    CAS  PubMed  Google Scholar 

  • Beauchamp, G. K., & Yamazaki, K. (2003). Chemical signaling in mice. Biochemical Society Transactions, 31, 147–151.

    CAS  PubMed  Google Scholar 

  • Becker, S. D., & Hurst, J. L. (2008). Pregnancy block from a female perspective. In J. L. Hurst, R. J. Beynon, S. C. Roberts, & T. D. Wyatt (Eds.), Chemical signals in vertebrates 11 (pp. 141–150). New York: Springer.

    Google Scholar 

  • Becker, S. D., & Hurst, J. L. (2009). Female behaviour plays a critical role in controlling murine pregnancy block. Proceedings of the Royal Society of London B, 276, 1723–1729.

    Google Scholar 

  • Beiderbeck, D. I., Reber, S. O., Havasi, A., Bredewold, R., Veenema, A. H., & Neumann, I. D. (2012). High and abnormal forms of aggression in rats with extremes in trait anxiety—Involvement of the dopamine system in the nucleus accumbens. Psychoneuroendocrinology, 37, 1969–1980.

    CAS  PubMed  Google Scholar 

  • Berry, M. D. (2004). Mammalian central nervous system trace amines. Pharmacologic amphetamines, physiologic neuromodulators. Journal of Neurochemistry, 90, 257–271.

    CAS  PubMed  Google Scholar 

  • Bessey, C., Devlin, R. H., Liley, N. R., & Biagi, C. A. (2004). Reproductive performance of growth-enhanced transgenic coho salmon. Transactions of the American Fisheries Society, 133, 1205–1220.

    Google Scholar 

  • Beynon, R. J., & Hurst, J. L. (2003). Multiple roles of major urinary proteins in the house mouse, Mus domesticus. Biochemical Society Transactions, 31, 142–146.

    CAS  PubMed  Google Scholar 

  • Bielsky, I. F., Hu, S. B., Szegda, K. L., Westphal, H., & Young, L. J. (2004). Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology, 29, 483–493.

    CAS  PubMed  Google Scholar 

  • Billeter, J. C., Jagadeesh, S., Stepek, N., Azanchi, R., & Levine, J. D. (2012). Drosophila melanogaster females change mating behaviour and offspring production based on social context. Proceedings of the Royal Society of London B, 279, 2417–2425.

    Google Scholar 

  • Binns, K. E., & Brennan, P. A. (2005). Changes in electrophysiological activity in the accessory olfactory bulb and medial amygdala associated with mate recognition in mice. European Journal of Neuroscience, 21, 2529–2537.

    CAS  PubMed  Google Scholar 

  • Boehm, T., & Zufall, F. (2006). MHC peptides and the sensory evaluation of genotype. Trends in Neuroscience, 29, 100–107.

    CAS  Google Scholar 

  • Bonadonna, F., & Mardon, J. (2013). Besides colours and songs, odour is the new black of avian communication. In M. L. East & M. Dehnhard (Eds.), Chemical signals in vertebrates 12 (pp. 325–339). New York: Springer.

    Google Scholar 

  • Bredy, T. W., & Barad, M. (2009). Social modulation of associative fear learning by pheromone communication. Learning and Memory, 16, 12–18.

    PubMed Central  PubMed  Google Scholar 

  • Brennan, P. A. (2009). Outstanding issues surrounding vomeronasal mechanisms of pregnancy block and individual recognition in mice. Behavioural Brain Research, 200, 287–294.

    CAS  PubMed  Google Scholar 

  • Brennan, P. A., & Binns, K. E. (2005). Vomeronasal mechanisms of mate recognition in mice. Chemical Senses, 30, i148–i149.

    PubMed  Google Scholar 

  • Brennan, P. A., & Peele, P. (2003). Towards an understanding of the pregnancy-blocking urinary chemosignals of mice. Biochemical Society Transactions, 31, 152–155.

    CAS  PubMed  Google Scholar 

  • Brennan, P. A., Schellinck, H. M., & Keverne, E. B. (1999). Patterns of expression of the immediate-early gene egr-1 in the accessory olfactory bulb of female mice exposed to pheromonal constituents of male urine. Neuroscience, 90, 1463–1470.

    CAS  PubMed  Google Scholar 

  • Brennan, P. A., & Zufall, F. (2006). Pheromonal communication in vertebrates. Nature, 444, 308–315.

    CAS  PubMed  Google Scholar 

  • Broad, K. D., & Keverne, E. B. (2008). More to pheromones than meets the nose. Nature Neuroscience, 11, 128–129.

    CAS  PubMed  Google Scholar 

  • Brown-Borg, H. M. (2006). Longevity in mice: Is stress resistance a common factor? AGE, 28, 145–162.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brown-Borg, H. M., Rakoczy, S. G., Sharma, S., & Bartke, A. (2009). Long-living growth hormone receptor knockout mice: Potential mechanisms of altered stress resistance. Experimental Gerontology, 44, 10–19.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bruce, H. M. (1960). A block to pregnancy in the mouse caused by proximity of strange males. Journal of Reproduction and Fertility, 1, 96–103.

    CAS  PubMed  Google Scholar 

  • Bruce, H. M. (1965). Effect of castration on the reproductive pheromones of male mice. Journal of Reproduction and Fertility, 10, 141–143.

    CAS  PubMed  Google Scholar 

  • Caspers, B. A., & Krause, E. T. (2013). Intraspecific olfactory communication in zebra finches (Taeniopygia guttata): Potential information apart from visual and acoustic cues. In M. L. East & M. Dehnhard (Eds.), Chemical signals in vertebrates 12 (pp. 341–351). New York: Springer.

    Google Scholar 

  • Catoni, C., Peters, A., & Schaefer, H. M. (2008). Life history trade-offs are influenced by the diversity, availability and interactions of dietary antioxidants. Animal Behavior, 76, 1107–1119.

    Google Scholar 

  • Cavaggioni, A., Mucignat, C., & Tirindelli, R. (1999). Pheromone signalling in the mouse: Role of urinary proteins and vomeronasal organ. Archives Italian Biology, 137, 193–200.

    CAS  Google Scholar 

  • Celerier, A., Bon, C., Malapert, A., Palmas, P., & Bonadonna, F. (2011). Chemical kin label in seabirds. Biological Letters, 7, 807–810.

    CAS  Google Scholar 

  • Chamero, P., Katsoulidou, V., Hendrix, P., Bufe, B., Roberts, R., Matsunami, H., et al. (2011). G protein Gao is essential for vomeronasal function and aggressive behavior in mice. Proceedings of the National Academy of Sciences of the United States of America, 108, 12898–12903.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chamero, P., Leinders-Zufall, T., & Zufall, F. (2012). From genes to social communication: Molecular sensing by the vomeronasal organ. Trends in Neuroscience, 35, 597–606.

    CAS  Google Scholar 

  • Chamero, P., Marton, T. F., Logan, D. W., Flanagan, K., Cruz, J. R., Saghatelian, A., et al. (2007). Identification of protein pheromones that promote aggressive behaviour. Nature, 450, 899–902.

    CAS  PubMed  Google Scholar 

  • Chaput, N., Schartz, N. E. C., Andre, F., Taieb, J., Novault, S., Bonnaventure, P., et al. (2004). Exosomes as potent cell-free peptide-based vaccine. II. Exosomes in CpG adjuvants efficiently prime naive Tc1 lymphocytes leading to tumor rejection. Journal of Immunology, 172, 2137–2146.

    CAS  Google Scholar 

  • Chaudhry, A. M., Marsh-Rollo, S. E., Aksenov, V., Rollo, C. D., & Szechtman, H. (2008). Modifier selection by transgenes: The case of growth hormone transgenesis and hyperactive circling mice. Evolutionary Biology, 35, 267–286.

    Google Scholar 

  • Cheetham, S. A., Smith, A. L., Armstrong, S. D., Beynon, R. J., & Hurst, J. L. (2009). Limited variation in the major urinary proteins of laboratory mice. Physiology & Behavior, 96, 253–261.

    CAS  Google Scholar 

  • Cheetham, S., Thom, M., Jury, F., Ollier, W., Beynon, R., & Hurst, J. (2007). The genetic basis of individual-recognition signals in the mouse. Current Biology, 17, 1771–1777.

    CAS  PubMed  Google Scholar 

  • Cho, K. W., Zhou, Y., Sheng, L., & Rui, L. (2011). Lipocalin-13 regulates glucose metabolism by both insulin-dependent and insulin-independent mechanisms. Molecular and Cellular Biology, 31, 450–457.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Choleris, E., Clipperton-Allen, A. E., Phan, A., & Kavaliers, M. (2009). Neuroendocrinology of social information processing in rats and mice. Frontiers in Neuroendocrinology, 30, 442–459.

    CAS  PubMed  Google Scholar 

  • Choleris, E., Clipperton-Allen, A. E., Phan, A., Valsecchi, P., & Kavaliers, M. (2012). Estrogenic involvement in social learning, social recognition and pathogen avoidance. Frontiers in Neuroendocrinology, 33, 140–159. doi:10.1016/j.yfrne.2012.02.001.

    CAS  PubMed  Google Scholar 

  • Choleris, E., Gustafsson, J. A., Korach, K. S., Muglia, L. J., Pfaff, D. W., & Ogawa, S. (2003). An estrogen dependent 4-gene micronet regulating social recognition: A study with oxytocin and estrogen receptor -α and –β knockout mice. Proceedings of the National Academy of Sciences of the United States of America, 100, 6192–6197.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Clancy, A. N., Coquelin, A., Macrides, F., Gorski, R. A., & Noble, E. P. (1984). Sexual behaviour and aggression in male mice: Involvement of the vomeronasal system. Journal of Neuroscience, 4, 2222–2229.

    CAS  PubMed  Google Scholar 

  • Clipperton, A. E., Spinato, J. M., Chernets, C., Pfaff, D. F., & Choleris, E. (2008). Differential effects of estrogen receptor alpha and beta specific agonists on social learning of food preferences in female mice. Neuropsychopharmacology, 33, 2362–2375.

    CAS  PubMed  Google Scholar 

  • Cook, J. T., McNiven, M. A., Richardson, G. F., & Sutterlin, A. M. (2000). Growth rate, body composition and feed digestibilityrconversion of growth-enhanced transgenic Atlantic salmon (Salmo salar). Aquaculture, 188, 15–32.

    Google Scholar 

  • Coopersmith, C. B., & Lenington, S. (1998). Female preferences based on male quality in house mice: Interaction between male dominance rank and t-complex genotype. Ethology, 90, 1–16.

    Google Scholar 

  • Crews, D. (2008). Epigenetics and its implications for behavioral neuroendocrinology. Frontiers in Neuroendocrinology, 29, 344–357.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dahlback, B., & Nielsen, L. B. (2006). Apolipoprotein M—A novel player in high-density lipoprotein metabolism and atherosclerosis. Current Opinion in Lipidology, 17, 291–295.

    PubMed  Google Scholar 

  • Dalle-Donne, I., Giustarini, D., Colombo, R., Rossi, R., & Milzani, A. (2003). Protein carbonylation in human diseases. Trends in Molecular Medicine, 9, 169–176.

    CAS  PubMed  Google Scholar 

  • Dean, M. D., Ardlie, K. G., & Nachman, M. W. (2006). The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Molecular Ecology, 15, 4141–4151.

    CAS  PubMed Central  PubMed  Google Scholar 

  • deCatanzaro, D., Muir, C., O’Brien, J., & Williams, S. (1995). Strange-male-induced pregnancy disruption in mice: Reduction of vulnerability by 17 beta-estradiol antibodies. Physiolgy and Behavior, 58, 401–404.

    CAS  Google Scholar 

  • Decramer, S., Gonzalez de Peredo, A., Breuil, B., Mischak, H., Monsarrat, B., Bascands, J. L., et al. (2008). Urine in clinical proteomics. Molecular and Cellular Proteomics, 7, 1850–1862.

    CAS  PubMed  Google Scholar 

  • Devlin, R. H., Johnsson, J. I., Smailus, D. E., Biagi, C. A., Jonsson, E., & Bjornsson, B. T. (1999). Increased ability to compete for food by growth hormone-transgenic coho salmon Oncorhynchus kisutch (Walbaum). Aquatic Research, 30, 479–482.

    Google Scholar 

  • Devlin, R. H., Sundstrom, L. F., & Muir, W. M. (2006). Interface of biotechnology and ecology for environmental risk assessments of transgenic fish. Trends in Biotechnology, 24, 89–97.

    CAS  PubMed  Google Scholar 

  • Dowling, D. K., & Simmons, L. W. (2009). Reactive oxygen species as universal constraints in life-history evolution. Proceedings of the Royal Society of London B, 276, 1737–1745.

    CAS  Google Scholar 

  • Drickamer, L. C. (1989). Pregnancy block in wild stock house mice, Mus domesticus -olfactory preferences of females during gestation. Animal Behavior, 37, 690–692.

    Google Scholar 

  • Duan, M., Zhang, T., Hu, W., Li, Z., Sundström, L. F., Zhu, T., et al. (2011). Behavioral alterations in GH transgenic common carp may explain enhanced competitive feeding ability. Aquaculture, 317, 175–181.

    CAS  Google Scholar 

  • Ehman, K. D., & Scott, M. E. (2001). Urinary odour preferences of MHC congenic female mice, Mus domesticus: Implications for kin recognition and detection of parasitized males. Animal Behavior, 62, 781–789.

    Google Scholar 

  • Evans, J. P. (2010). Quantitative genetic evidence that males trade attractiveness for ejaculate quality in guppies. Proceedings of the Royal Society of London B Sci., 277, 3195–3201. doi:10.1098/rspb.2010.0826.

    Google Scholar 

  • Farrell, A. P., Bennett, W., & Devlin, R. H. (1997). Growth-enhanced transgenic salmon can be inferior swimmers. Canadian Journal of Zoology, 75, 335–337.

    Google Scholar 

  • Fitzpatrick, J. L., Akbarashandiz, H., Sakhrani, D., Biagi, C. A., Pitcher, T. E., & Devlin, R. H. (2011). Cultured growth hormone transgenic salmon are reproductively out-competed by wild-reared salmon in semi-natural mating arenas. Aquaculture, 312, 185–191.

    CAS  Google Scholar 

  • Fraga, C. G., Shigenaga, M. K., Park, J. W., Degan, P., & Ames, B. N. (1990). Oxidative damage to DNA during aging: 8-hydroxy-2′-deoxyguanosine in rat organ DNA and urine. Proceedings of the National Academy of Sciences of the United States of America, 87, 4533–4537.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gabor, C. S., Phan, A., Clipperton-Allen, A. E., Kavaliers, M., & Choleris, E. (2012). Interplay of oxytocin, vasopressin, and sex hormones in the regulation of social recognition. Behavioral Neuroscience, 126, 97–109.

    CAS  PubMed  Google Scholar 

  • Gates, A. C., Bernal-Mizrachi, C., Chinault, S. L., Feng, C., Schneider, J. G., Coleman, T., et al. (2007). Respiratory uncoupling in skeletal muscle delays death and diminishes age-related disease. Cell Metabolism, 6, 497–505.

    CAS  PubMed  Google Scholar 

  • Giller, K., Huebbe, P., Doering, F., Pallauf, K., & Rimbach, G. (2013). Major urinary protein 5, a scent communication protein, is regulated by dietary restriction and subsequent re-feeding in mice. Proceedings of the Royal society of London B, 280, doi:10.1098/rspb.2013.0101.

  • Grillon, C., Krimsky, M., Charney, D. R., Vytal, K., Ernst, M., & Cornwell, B. (2012). Oxytocin increases anxiety to unpredictable threat. Molecular Psychiatry, 18, 958–960. doi:10.1038/mp.2012.156.

    PubMed Central  PubMed  Google Scholar 

  • Guzzo, A. C., Berger, R. G., & deCatanzaro, D. (2010). Excretion and binding of tritium-labelled oestradiol in mice (Mus musculus): Implications for the Bruce effect. Reproduction, 139, 255–263.

    CAS  PubMed  Google Scholar 

  • Guzzo, A. C., Jheon, J., Imtiaz, F., & deCatanzaro, D. (2012). Oestradiol transmission from males to females in the context of the Bruce and Vandenbergh effects in mice (Mus musculus). Reproduction, 143, 539–548.

    CAS  PubMed  Google Scholar 

  • Hajdu, I., Obal, F., Jr., Fang, J., Krueger, J. M., & Rollo, C. D. (2002). Sleep of transgenic mice producing excess rat growth hormone. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 282, R70–R76.

    CAS  PubMed  Google Scholar 

  • Hamilton, W. D., & Zuk, M. (1982). Heritable true fitness and bright birds? A role for parasites? Science, 218, 384–387.

    CAS  PubMed  Google Scholar 

  • Harvey, L. M., Harvey, S. J., Hom, M., Perna, A., & Salib, J. (2006). The use of bloodhounds in determining the impact of genetics and the environment on the expression of human odortype. Journal of Forensic Science, 51, 1109–1114.

    Google Scholar 

  • He, J., Ma, L., Kim, S., Nakai, J., & Yu, C. R. (2008). Encoding gender and individual information in the mouse vomeronasal organ. Science, 320, 535–538.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Henderson, L. J., Heidinger, B. J., Evans, N. P., & Arnold, K. E. (2013). Ultraviolet crown coloration in female blue tits predicts reproductive success and baseline corticosterone. Behavioral Ecology,. doi:10.1093/beheco/art066.

    Google Scholar 

  • Holden, C. (2004). Random samples. Science, 303, 166.

    Google Scholar 

  • Holmes, A., Murphy, D. L., & Crawley, J. N. (2002). Reduced aggression in mice lacking the serotonin transporter. Psychopharmacology (Berl), 161, 160–167.

    CAS  Google Scholar 

  • Horvath, G., Jarverud, G. K., Jarverud, S., & Horvath, I. (2008). Human ovarian carcinomas detected by specific odor. Integrative Cancer Therapy, 7, 76–80.

    Google Scholar 

  • Howard, R. D., DeWoody, J. A., & Muir, W. M. (2004). Transgenic male mating advantage provides opportunity for Trojan gene effect in a fish. Proceedings of the National Academy of Sciences of the United States of America, 101, 2934–2938.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hui, X., Zhu, W., Wang, Y., Lam, K. S. L., Zhang, J., Wu, D., et al. (2009). Major urinary protein-1 increases energy expenditure and improves glucose intolerance through enhancing mitochondrial function in skeletal muscle of diabetic mice. Journal of Biological Chemistry, 284, 14050–14057.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hull-Thompson, J., Muffat, J., Sanchez, D., Walker, D. W., Benzer, S., Ganfornina, M. D., et al. (2009). Control of metabolic homeostasis by stress signaling is mediated by the lipocalin NLaz. PLoS Genetics, 5(4), e1000460. doi:10.1371/journal.pgen.1000460.

    PubMed Central  PubMed  Google Scholar 

  • Humphries, R. E., Robertson, D. H., Beynon, R. J., & Hurst, J. L. (1999). Unravelling the chemical basis of competitive scent marking in house mice. Animal Behavior, 58, 1177–1190.

    Google Scholar 

  • Hurst, J. L. (2009). Female recognition and assessment of males through scent. Behavioral Brain Research, 200, 295–303.

    CAS  Google Scholar 

  • Hurst, J. L., & Beynon, R. J. (2004). Scent wars: The chemobiology of competitive signalling in mice. BioEssays, 26, 1288–1298.

    CAS  PubMed  Google Scholar 

  • Hurst, J. L., & Beynon, R. J. (2013). Rodent urinary proteins: Genetic identity signals and pheromones. In M. L. East & M. Dehnhard (Eds.), Chemical signals in vertebrates (pp. 117–133). New York: Springer.

    Google Scholar 

  • Hurst, J. L., Payne, C. E., Nevison, C. M., Marie, A. D., Humphries, R. E., Robertson, D. H. L., et al. (2001). Individual recognition in mice mediated by major urinary proteins. Nature, 414, 631–634.

    CAS  PubMed  Google Scholar 

  • Ilieva, D. B., Jørgensen, S. M., Rodec, M., Krasnov, A., Harneshaug, I., & Jørgensen, J. B. (2010). CpG-induced secretion of MHCIIb and exosomes from salmon (Salmo salar) APCs. Developmental and Comparative Immunology, 34, 29–41.

    Google Scholar 

  • Isogai, Y., Si, S., Pont-Lezica, L., Tan, T., Kapoor, V., Murthy, V. N., et al. (2011). Molecular organization of vomeronasal chemoreception. Nature Letters, 478, 241–245.

    CAS  Google Scholar 

  • Jemiolo, B., Alberts, J., Sochinski-Wiggins, S., Harvey, S., & Novotny, M. (1985). Behavioural and endocrine responses of female mice to synthetic analogues of volatile compounds in male urine. Animal Behavior, 33, 1114–1118.

    Google Scholar 

  • Jemiolo, B., Xie, T. M., & Novotny, M. (1991). Socio-sexual olfactory preference in female mice: Attractiveness of synthetic chemosignals. Physiology and Behaviour, 50, 1119–1122.

    CAS  Google Scholar 

  • Jobin, R. M. J. (1988). Effect of growth hormone on rainbow trout: An ecological asssessment of the potential impact of genetic engineering on organismal design. M.Sc. thesis, Department of Biology, McMaster, University, Supervisor, C.D. Rollo.

  • Jonsson, E., Johnsson, J. I., & Bjornsson, B. T. (1998). Growth hormone increases aggressive behavior in juvenile rainbow trout. Hormones and Behavior, 33, 9–15.

    CAS  PubMed  Google Scholar 

  • Kajiura, L. J., & Rollo, C. D. (1994). A mass budget for transgenic “Supermice” engineered with extra rat growth hormone genes: Evidence for energetic limitation. Canadian Journal of Zoology, 72, 1010–1017.

    Google Scholar 

  • Kajiura, L. J., & Rollo, C. D. (1996). The ontogeny of resource allocation in giant transgenic rat growth hormone mice. Canadian Journal of Zoology, 74, 492–507.

    Google Scholar 

  • Kavaliers, M., Agmo, A., Choleris, E., Gustafsson, J. A., Korach, K. S., Muglia, L. J., et al. (2004). Oxytocin and estrogen receptor α and β knockout mice provide discriminably different odor cues in behavioral assays. Genes Brain and Behavior, 3, 189–195.

    CAS  Google Scholar 

  • Kavaliers, M., & Choleris, E. (2011). Sociality, pathogen avoidance, and the neuropeptides oxytocin and arginine vasopressin. Psychological Science, 22, 1367–1374.

    PubMed  Google Scholar 

  • Kavaliers, M., Choleris, E., & Pfaff, D. W. (2005a). Recognition and avoidance of the odors of parasitized conspecifics and predators: Differential genomic correlates. Neuroscience and Biobehavioral Reviews, 29, 1347–1359.

    PubMed  Google Scholar 

  • Kavaliers, M., Choleris, E., & Pfaff, D. W. (2005b). Genes, odours and the recognition of parasitized individuals by rodents. Trends in Parasitology, 21, 423–429.

    CAS  PubMed  Google Scholar 

  • Keller, M., Baum, M. J., Brock, O., Brennan, P. A., & Bakker, J. (2009). The main and the accessory olfactory systems interact in the control of mate recognition and sexual behavior. Behavioral Brain Research, 200, 268–276.

    Google Scholar 

  • Keller, S., Rupp, C., Stoeck, A., Runz, S., Fogel, M., Lugert, S., et al. (2007). CD24 is a marker of exosomes secreted into urine and amniotic fluid. Kidney International, 72, 1095–1102.

    CAS  PubMed  Google Scholar 

  • Kelliher, K. R. (2007). The combined role of the main olfactory and vomeronasal systems in social communication in mammals. Hormones and Behavior, 52, 561–570.

    PubMed Central  PubMed  Google Scholar 

  • Kelliher, K. R., & Wersinger, S. R. (2009). Olfactory regulation of the sexual behavior and reproductive physiology of the laboratory mouse: Effects and neural mechanisms. Institute of Laboratory Animal Research Journal, 50, 28–42.

    CAS  Google Scholar 

  • Kim, S. Y., Noguera, J. C., Morales, J., & Velando, A. (2011). Quantitative genetic evidence for trade-off between growth and resistance to oxidative stress in a wild bird. Evolutionary Ecology, 25, 461–472.

    Google Scholar 

  • Kimchi, T., Xu, J., & Dulac, C. (2007). A functional circuit underlying male sexual behaviour in the female mouse brain. Nature, 448, 1009–1014.

    CAS  PubMed  Google Scholar 

  • Kingsolver, J. G., & Pfennig, D. W. (2004). Individual-level selection as a cause of Cope’s rule of phyletic size increase. Evolution, 58, 1608–1612.

    PubMed  Google Scholar 

  • Knepper, M. A., & Pisitkun, T. (2007). Exosomes in urine: Who would have thought…? Kidney International, 72, 1043–1045.

    CAS  PubMed  Google Scholar 

  • Kondrashov, A. S. (1988). Deleterious mutations and the evolution of sexual reproduction. Nature, 336, 435–440.

    CAS  PubMed  Google Scholar 

  • Konrad, M., Vyleta, M. L., Theis, F. J., Stock, M., Tragust, S., Klatt, M., et al. (2012). Social transfer of pathogenic fungus promotes active immunisation in ant colonies. PLoS Biology, 10(4), e1001300. doi:10.1371/journal.pbio.1001300.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kuo, T. H., Fedina, T. Y., Hansen, I., Dreisewerd, K., Dierick, H. A., Yew, J. Y., et al. (2012). Insulin signaling mediates sexual attractiveness in Drosophila. PLoS Genetics, 8(4), e1002684. doi:10.1371/journal.pgen.1002684.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kwak, J., Josue, J., Faranda, A., Opiekun, M. C., Preti, G., Osada, K., et al. (2011). Butylated hydroxytoluene is a ligand of urinary proteins derived from female mice. Chemical Senses, 36, 443–452.

    CAS  PubMed  Google Scholar 

  • Kwak, J., Opiekun, M. C., Matsumura, K., Preti, G., Yamazaki, K., & Beauchamp, G. K. (2009). Major histocompatibility complex-regulated odor types: Peptide-free urinary volatile signals. Physiology & Behavior, 96, 184–188.

    CAS  Google Scholar 

  • Labov, J. B. (1981). Pregnancy blocking in rodents: Adaptive advantages for females. American Naturalist, 118, 361–371.

    Google Scholar 

  • Lachmansingh, E. I., & Rollo, C. D. (1994). Evidence for a tradeoff between growth and behavioural activity in giant “supermice” genetically engineered with extra growth hormone genes. Canadian Journal of Zoology, 72, 2158–2168.

    Google Scholar 

  • Lanyon, C. V., Rushton, S. P., O’Donnell, A. G., Goodfellow, M., Ward, A. C., Petrie, M., et al. (2007). Murine scent mark microbial communities are genetically determined. Federation of European Microbiological Societies Microbiology Ecology, 59, 576–583.

    CAS  Google Scholar 

  • Leinders-Zufall, T., Brennan, P., Widmayer, P., Chandramani, P., Maul-Pavicic, A., Jager, M., et al. (2004). MHC class I peptides as chemosensory signals in the vomeronasal organ. Science, 306, 1033–1037.

    CAS  PubMed  Google Scholar 

  • Leinders-Zufall, T., Ishii, T., Mombaerts, P., Zufall, F., & Boehm, T. (2009). Structural requirements for the activation of vomeronasal sensory neurons by MHC peptides. Nature Neuroscience, 12, 1551–1558.

    CAS  PubMed  Google Scholar 

  • Lemon, J. A., Rollo, C. D., & Boreham, D. R. (2008a). Elevated DNA damage in a mouse model of oxidative stress: Impacts of ionizing radiation and a protective dietary supplement. Mutagenesis, 23, 473–482.

    CAS  PubMed  Google Scholar 

  • Lemon, J. A., Rollo, C. D., McFarlane, N. M., & Boreham, D. R. (2008b). Radiation-induced apoptosis in mouse lymphocytes is modified by a complex dietary supplement: The effect of genotype and gender. Mutagenesis, 23, 465–472.

    CAS  PubMed  Google Scholar 

  • Li, D., Fu, C., HU, W., Zhong, S., Wang, Y., & Zhu, Z. (2007). Rapid growth cost in “all-fish” growth hormone gene transgenic carp: Reduced critical swimming speed. Chinese Science Bulletin, 52, 1501–1506.

    CAS  Google Scholar 

  • Liberles, S. D., & Buck, L. B. (2006). A second class of chemosensory receptors in the olfactory epithelium. Nature, 442, 645–650.

    CAS  PubMed  Google Scholar 

  • Lin, D., Boyle, M. P., Dollar, P., Lee, H., Lein, E. S., Perona, P., et al. (2011). Functional identification of an aggression locus in the mouse hypothalamus. Nature, 470, 221–226.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lindeman, L., Meyer, C. A., Jeanneau, K., Bradaia, A., Ozmen, L., Bluethmann, H., et al. (2008). Trace amine-associated receptor 1 modulates dopaminergic activity. Journal of Pharmacological and Experimental Therapeutics, 324, 948–956.

    Google Scholar 

  • Liu, B., Chen, Y., & St. Clair, D. K. (2008). ROS and p53: A versatile partnership. Free Radical Biology & Medicine, 44, 1529–1535.

    CAS  Google Scholar 

  • Liu, D., & Xu, Y. (2011). p53, oxidative stress, and aging. Antioxidants & Redox Signaling, 15, 1669–1678.

    CAS  Google Scholar 

  • Lorenzen, K., Beveridge, M. C. M., & Mangel, M. (2012). Cultured fish: Integrative biology and management of domestication and interactions with wild fish. Biological Reviews, 87, 639–660.

    PubMed  Google Scholar 

  • Lowry, O. H., Rosenbrough, N. J., Farr, A. L., & Randall, R. J. (1951). Protein measurement with the Folin phenoll reagent. Journal of Biological Chemistry, 193, 265–275.

    CAS  PubMed  Google Scholar 

  • Maillet, A., & Pervaiz, S. (2012). Redox regulation of p53, redox effectors regulated by p53: A subtle balance. Antioxidants & Redox Signaling, 16, 1285–1294.

    CAS  Google Scholar 

  • Mandiyan, V. S., Coats, J. K., & Shah, N. M. (2005). Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nature Neuroscience, 8, 1660–1662.

    CAS  PubMed  Google Scholar 

  • Marashi, V., & Rulicke, T. (2012). The Bruce effect in norway rats. Biology of Reproduction, 86, 1–5.

    PubMed  Google Scholar 

  • Marchlewska-Koj, A. (1977). Pregnancy block elicited by urinary proteins of male mice. Biology of Reproduction, 17, 729–732.

    CAS  PubMed  Google Scholar 

  • Marchlewska-Koj, A. (1981). Pregnancy block elicited by male urinary peptides in mice. Journal of Reproduction and Fertility, 61, 221–224.

    CAS  PubMed  Google Scholar 

  • Marchlewska-Koj, A., Cavaggioni, A., Mucignat-Caretta, C., & Olejniczak, P. (2000). Stimulation of estrus in female mice by male urinary proteins. Journal of Chemical Ecology, 26, 2355–2366.

    CAS  Google Scholar 

  • Marchlewska-Koj, A., Jemiolo, B., Woniacka, J., & Kozowski, K. (1980). Male-pheromone effect on the efficiency of pregnancy in female mice. Journal of Reproduction and Fertility, 58, 363–367.

    CAS  PubMed  Google Scholar 

  • Marquez, C., Poirier, G. L., Cordero, M. I., Larsen, M. H., Groner, A., Marquis, J., et al. (2013). Peripuberty stress leads to abnormal aggression, altered amygdala and orbitofrontal reactivity and increased prefrontal MAOA gene expression. Translational Psychiatry, 3(e216), 2013. doi:10.1038/tp.2012.144.

    Google Scholar 

  • Masternak, M. M., & Bartke, A. (2012). Growth hormone, inflammation and aging. Pathobiology of Aging and Age-related Disease, 2, 17293. doi:10.3402/pba.v2i0.17293.

    CAS  Google Scholar 

  • Matte, A. C. (1981). Growth hormone and isolation-induced aggression in wild male mice. Pharmacology, Biochemistry and Behavior, 14, 85–87.

    CAS  PubMed  Google Scholar 

  • McCarthy, M. M. (2008). Estradiol and the developing brain. Physiological Reviews, 88, 91–134.

    CAS  PubMed Central  PubMed  Google Scholar 

  • McCulloch, M., Jezierski, T., Broffman, M., Hubbard, A., Turner, K., & Janecki, T. (2006). Diagnostic accuracy of canine scent detection in early- and late-stage lung and breast cancers. Integrative Cancer Therapies, 5, 30–39.

    PubMed  Google Scholar 

  • Metcalfe, N. B., & Alonso-Alvarez, C. (2010). Oxidative stress as a life-history constraint: The role of reactive oxygen species in shaping phenotypes from conception to death. Functional Ecology, 24, 984–996.

    Google Scholar 

  • Metcalfe, N. B., Valdimarsson, S. K., & Morgan, I. J. (2003). The relative roles of domestication, rearing environment, prior residence and body size in deciding territorial contests between hatchery and wild juvenile salmon. Journal of Applied Ecology, 40, 535–544.

    Google Scholar 

  • Monaghan, P., Metcalfe, N. B., & Torres, R. (2009). Oxidative stress as a mediator of life history trade-offs: Mechanisms, measurements and interpretation. Ecological Letters, 12, 75–92.

    Google Scholar 

  • Montoya, E. R., Terburg, D., Bos, P. A., & van Honk, J. (2012). Testosterone, cortisol, and serotonin as key regulators of social aggression: A review and theoretical perspective. Motivation and Emotion, 36, 65–73.

    PubMed Central  PubMed  Google Scholar 

  • More, L. (2006). Mouse major urinary proteins trigger ovulation via the vomeronasal organ. Chemical Senses, 31, 393–401.

    CAS  PubMed  Google Scholar 

  • Moreau, D. T. R., Conway, C., & Fleming, I. A. (2011a). Reproductive performance of alternative male phenotypes of growth hormone transgenic Atlantic salmon (Salmo salar). Evolutionary Applications, 4, 736–748.

    CAS  PubMed Central  Google Scholar 

  • Moreau, D. T. R., Fleming, I. A., Fletcher, G. L., & Brown, J. A. (2011b). Growth hormone transgenesis does not influence territorial dominance or growth and survival of first-feeding Atlantic salmon Salmo salar in food-limited stream microcosms. Journal of Fish Biology, 78, 726–740.

    CAS  PubMed  Google Scholar 

  • Mori, T., Hiraka, I., Kurata, Y., Kawachi, H., Mano, N., Devlin, R. H., et al. (2007). Changes in hepatic gene expression related to innate immunity, growth and iron metabolism in GH-transgenic amago salmon (Oncorhynchus masou) by cDNA subtraction and microarray analysis, and serum lysozyme activity. General and Comparative Endocrinology, 151, 42–54.

    CAS  PubMed  Google Scholar 

  • Moshkin, M. P., Gerlinskaya, L. A., & Evsikov, V. I. (2000). The role of the immune system in behavioral strategies of reproduction. Journal of Reproduction and Development, 46, 341–365.

    CAS  Google Scholar 

  • Mucignat-Caretta, C., Caretta, A., & Cavaggioni, A. (1995). Acceleration of puberty onset in female mice by male urinary proteins. Journal of Physiology, 486, 517–522.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Muir, W. M., & Howard, R. D. (1999). Possible ecological risks of transgenic organism release when transgenes affect mating success: Sexual selection and the Trojan gene hypothesis. Proceedings of the National Academy of Sciences of the United States of America, 96, 13853–13856.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mullen, S. P., Mendelson, T. C., Schal, C., & Shaw, K. L. (2007). Rapid evolution of cuticular hydrocarbons in a species radiation of acoustically diverse Hawaiian crickets (Grylidae: Trigonidiinae: Laupala). Evolution, 61, 223–231.

    CAS  PubMed  Google Scholar 

  • Mulligan, K. A., Fuerer, C., Ching, W., Fish, M., Willert, K., & Nusse, R. (2012). Secreted wingless-interacting molecule (Swim) promotes long-range signaling by maintaining wingless solubility. Proceedings of the National Academy of Sciences of the United States of America, 109, 370–377.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nei, M. (2007). The new mutation theory of phenotypic evolution. Proceedings of the National Academy of Sciences of the United States of America, 104, 12235–12242.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Neregard, L., Sundt-Hansen, L., Bjornsson, B. T., & Johnsson, J. I. (2008). Growth hormone affects behaviour of wild brown trout Salmo trutta in territorial owner–intruder conflicts. Journal of Fish Biology, 73, 2341–2351.

    CAS  Google Scholar 

  • Nishimura, K., Utsumi, K., Yuhara, M., Fujitani, Y., & Iritani, A. (1989). Identification of puberty-accelerating pheromones in male mouse urine. Journal of Experimental Zoology, 251, 300–305.

    CAS  PubMed  Google Scholar 

  • Nodari, F., Hsu, F. F., Fu, X., Holekamp, T. F., Kao, L. F., Turk, J., et al. (2008). Sulfated steroids as natural ligands of mouse pheromone-sensing neurons. Journal of Neuroscience, 28, 6407–6418.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Noguera, J. C., Kim, S. Y., & Velando, A. (2012). Pre-fledgling oxidative damage predicts recruitment in a long-lived bird. Biologyl Letters, 8, 61–63.

    CAS  Google Scholar 

  • Norstedt, G., & Palmiter, R. (1984). Secretory rhythm of growth hormone regulates sexual differentiation of mouse liver. Cell, 36, 805–812.

    CAS  PubMed  Google Scholar 

  • Novotny, M., Harvey, S., & Jemiolo, B. (1990). Chemistry of male dominance in the house mouse, Mus domesticus. Experientia, 46, 109–113.

    CAS  PubMed  Google Scholar 

  • Novotny, M. V., Soini, H. A., Koyama, S., Wiesler, D., Bruce, K. E., & Penn, D. J. (2007). Chemical identification of MHC-influenced volatile compounds in mouse urine. I: Quantitative proportions of major chemosignals. Journal of Chemical Ecology, 33, 417–434.

    CAS  PubMed  Google Scholar 

  • Palmiter, R. D., Brinster, R. L., Hammer, R. E., Trumbauer, M. E., Rosenfeld, M. G., Birnberg, M. C., et al. (1982). Dramatic growth of mice that develop from eggs microinjected with metallothionien-growth hormone fusion genes. Nature, 300, 611–615.

    CAS  PubMed  Google Scholar 

  • Paslakis, G., Blum, W. F., & Deuschle, M. (2012). Intranasal insulin-like growth factor I (IGF-I) as a plausible future treatment of depression. Medical Hypotheses, 79, 222–225.

    CAS  PubMed  Google Scholar 

  • Peele, P., Salazar, I., Mimmack, M., Keverne, E. B., & Brennan, P. A. (2003). Low molecular weight constituents of male mouse urine mediate the pregnancy block effect and convey information about the identity of the mating male. European Journal of Neuroscience, 18, 622–628.

    CAS  PubMed  Google Scholar 

  • Penn, D. J., & Potts, W. K. (1999). The evolution of mating preferences and major histocompatability complex genes. American Naturalist, 153, 145–164.

    Google Scholar 

  • Penn, D., Schneider, G., White, K., Slev, P., & Potts, W. (1998). Influenza infection neutralizes the attractiveness of male odour to female mice (Mus musculus). Ethology, 104, 685–694.

    Google Scholar 

  • Pisitkun, T., Shen, R. F., & Knepper, M. A. (2004). Identification and proteomic profiling of exosomes in human urine. Proceedings of the National Academy of Sciences of the United States of America, 101, 13368–13373.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Prado, N., Marazuela, E. G., Segura, E., Fernandez-Garcia, H., Villalba, M., Thery, C., et al. (2008). Exosomes from bronchoalveolar fluid of tolerized mice prevent allergic reaction. Journal of Immunology, 181, 1519–1525.

    CAS  Google Scholar 

  • Qazi, K. R., Gehrmann, U., Domange Jordo, E., Karlsson, M. C. I., & Gabrielsson, S. (2009). Antigen-loaded exosomes alone induce Th1-type memory through a B cell-dependent mechanism. Blood, 113, 2673–2683.

    CAS  PubMed  Google Scholar 

  • Ramm, S. A., Cheetham, S. A., & Hurst, J. L. (2008). Encoding choosiness: Female attraction requires prior physical contact with individual male scents in mice. Proceedings of the Royal Society of London R, 275, 1727–1735.

    Google Scholar 

  • Redford, K. H., Adams, W., & Mace, G. M. (2013). Synthetic biology and conservation of nature: Wicked problems and wicked solutions. PLoS Biology, 11(4), e1001530. doi:10.1371/journal.pbio.1001530.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Reichhardt, T. (2000). Will souped up salmon sink or swim? Nature, 406, 10–12.

    CAS  PubMed  Google Scholar 

  • Remage-Healey, L., Dong, S., Maidment, N. T., & Schlinger, B. A. (2011). Presynaptic control of rapid estrogen fluctuations in the songbird auditory forebrain. Journal of Neuroscience, 31, 10034–10038.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Renault, J., Gheusi, G., & Aubert, A. (2008). Changes in social exploration of a lipopolysaccharides-treated conspecific in mice: Role of environmental cues. Brain, Behavior, and Immunity, 22, 1201–1207.

    CAS  PubMed  Google Scholar 

  • Rich, T. J., & Hurst, J. L. (1998). Scent marks as reliable signals of the competitive ability of mates. Animal Behavior, 56, 727–735.

    Google Scholar 

  • Rich, T. J., & Hurst, J. L. (1999). The competing countermarks hypothesis: Reliable assessment of competitive ability by potential mates. Animal Behavior, 58, 1027–1037.

    Google Scholar 

  • Roberts, S. A., Simpson, D. M., Armstrong, S. D., Davidson, A. J., Robertson, D. H., McLean, L., et al. (2010). Darcin: A male pheromone that stimulates female memory and sexual attraction to an individual male’s odour. Biomed Central Biology, 8, 75. doi:10.1186/1741-7007-8-75.

    Google Scholar 

  • Rodier, F., Campisi, J., & Bhaumik, D. (2007). Two faces of p53: Aging and tumor suppression. Nucleic Acids Research, 35, 7475–7484.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rolland, C., de MacDonald, D. W., Fraipont, M., & Berdoy, M. (2003). Free female choice in house mice: Leaving best for last. Behaviour, 140, 1371–1388.

    Google Scholar 

  • Rollo, C. D. (1994). Phenotypes: Their epigenetics, ecology and evolution. London: Chapman and Hall.

    Google Scholar 

  • Rollo, C. D. (2002). Growth negatively impacts the life span of mammals. Evolution and Development, 4, 55–61. doi:10.1046/j.1525-142x.2002.01053.x.

    PubMed  Google Scholar 

  • Rollo, C. D. (2007a). Multidisciplinary aspects of regulatory systems relevant to multiple stressors: Aging, xenobiotics and radiation. In C. Mothersill, I. Mosse, & C. Seymour (Eds.), Multiple stressors: A challenge for the future (pp. 185–224). New York: Springer (NATO Science).

    Google Scholar 

  • Rollo, C. D. (2007b). Overview of research on giant transgenic mice with emphasis on the brain and aging. In T. Samaras (Ed.), Human body size and the laws of scaling (pp. 235–260). New York: Nova Biomedical Publishers.

    Google Scholar 

  • Rollo, C. D. (2010). Aging and the mammalian regulatory triumvirate. Aging and Disease, 1, 105–138.

    PubMed Central  PubMed  Google Scholar 

  • Rollo, C. D. (2012). Circadian Redox Regulation. In K. Pantopoulos & H. M. Shipper (Eds.), Principles of free radical biomedicine (pp. 575–627). New York: Nova Scientific Publishers.

    Google Scholar 

  • Rollo, C. D., Carlson, J., & Sawada, M. (1996). Accelerated aging of giant transgenic mice is associated with elevated free radical processes. Canadian Journal of Zoology, 74, 606–620.

    CAS  Google Scholar 

  • Rollo, C. D., Foss, J., Lachmansingh, E., & Singh, R. (1997a). Behavioural rhythmicity in transgenic growth hormone mice: Trade-offs, energetics and sleep-wake cycles. Canadian Journal of Zoology, 75, 1020–1034.

    Google Scholar 

  • Rollo, C. D., Lai, M., Whitehead, K., Perreault, M. L., Lemon, J. A., & Chaudhry, A. (2004). Thermoregulation of transgenic growth hormone mice. Canadian Journal of Zoology, 82, 934–949.

    CAS  Google Scholar 

  • Rollo, C. D., Rintoul, J., & Kajiura, L. J. (1997b). Lifetime reproduction of giant transgenic mice: The energy stress paradigm. Canadian Journal of Zoology, 75, 1336–1345.

    Google Scholar 

  • Rosser, A. E., & Keverne, E. B. (1985). The importance of central noradrenergic neurons in the formation of an olfactory memory in the prevention of pregnancy block. Neuroscience, 15, 1141–1147.

    CAS  PubMed  Google Scholar 

  • Rosser, A. E., Remfry, C. J., & Keverne, E. B. (1989). Restricted exposure of mice to primer pheromones coincident with prolactin surges blocks pregnancy by changing hypothalamic dopamine release. Journal of Reproduction and Fertility, 87, 553–559.

    CAS  PubMed  Google Scholar 

  • Sagazio, A., Shohreh, R., & Salvatori, R. (2011). Effects of GH deficiency and GH replacement on inter-male aggressiveness in mice. Growth Hormone and Insulin-like Growth Factor Research, 21, 76–80.

    CAS  Google Scholar 

  • Sanchez-Andrade, G., & Kendrick, K. M. (2011). Roles of α- and β-estrogen receptors in mouse social recognition memory: Effects of gender and the estrous cycle. Hormones and Behavior, 59, 114–122.

    CAS  PubMed  Google Scholar 

  • Sano, K., Tsuda, M. C., Musatov, S., Sakamoto, T., & Ogawa, S. (2013). Differential effects of site-specific knockdown of estrogen receptor α in the medial amygdala, medial pre-optic area, and ventromedial nucleus of the hypothalamus on sexual and aggressive behavior of male mice. European Journal of Neuroscience, 37, 1308–1319. doi:10.1111/ejn.12131.

    PubMed  Google Scholar 

  • Serguera, C., Triaca, V., Kelly-Barrett, J., Banchaabouchi, M. A., & Minichiello, L. (2008). Increased dopamine after mating impairs olfaction and prevents odor interference with pregnancy. Nature Neuroscience, 11, 949–956.

    CAS  PubMed  Google Scholar 

  • Sharp, N. P., & Agrawal, A. F. (2008). Mating density and the strength of sexual selection against deleterious alleles in Drosophila melanogaster. Evolution, 62, 857–867.

    PubMed  Google Scholar 

  • Sherborne, A. L., Thom, M. D., Paterson, S., Jury, F., Ollier, W. E. R., Stockley, P., et al. (2007). The genetic basis of inbreeding avoidance in house mice. Current Biology, 17, 2061–2066.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sheriff, M. J., Krebs, C. J., & Boonstra, R. (2010). The ghosts of predators past: Population cycles and the role of maternal programming under fluctuating predation risk. Ecology, 91, 2983–2994.

    PubMed  Google Scholar 

  • Singer, A. G., Beauchamp, G. K., & Yamazaki, K. (1997). Volatile signals of the major histocompatibility complex in male mouse urine. Proceedings of the National Academy of Sciences of the United States of America, 94, 2210–2214.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sironi, L., Tremoli, E., Miller, I., Guerrini, U., Calvio, A. M., Eberini, I., et al. (2001). Acute-phase proteins before cerebral ischemia in stroke-prone rats: Identification by proteomics. Stroke, 32, 753–760.

    CAS  PubMed  Google Scholar 

  • Smith, R. W., Wang, J., Bucking, C. P., Mothersill, C. E., & Seymour, C. B. (2007). Evidence for a protective response by the gill proteome of rainbow trout exposed to X-ray induced bystander signals. Proteomics, 7, 4171–4180.

    CAS  PubMed  Google Scholar 

  • Soderpalm, B., Ericsson, M., Bohlooly, Y. M., Engel, J. A., & Tornell, J. (1999). Bovine growth hormone transgenic mice display alterations in locomotor activity and brain monoamine neurochemistry. Endocrinology, 140, 5619–5625.

    CAS  PubMed  Google Scholar 

  • Sorensen, P. W., & Stacey, M. E. (1999). Evolution and specialization of fish hormonal pheromones. In R. E. Johnston, D. Müller-Schwarze, & P. W. Sorensen (Eds.), Chemical signals in vertebrates (pp. 15–48). New York: Kluwer Academic, Plenum Publishing.

    Google Scholar 

  • Spehr, M., Kelliher, K. R., Li, X. H., Boehm, T., Leinders-Zufall, T., & Zufall, F. (2006). Essential role of the main olfactory system in social recognition of major histocompatability complex peptide ligands. J. Neuroscience, 26, 1970–1991.

    Google Scholar 

  • Staskal, D. F., Hakk, H., Bauer, D., Diliberto, J. J., & Birnbaum, L. S. (2006). Toxicokinetics of polybrominated diphenyl ether congeners 47, 99, 100, and 153 in mice. Toxicological Science, 94, 28–37.

    CAS  Google Scholar 

  • Stowers, L., Cameron, P., & Keller, J. A. (2012). Ominous odors: Olfactory control of instinctive fear and aggression in mice. Current Opinion in Neurobiology, 23, 339–345. doi:10.1016/j.conb.2013.01.007.

    Google Scholar 

  • Sturm, T., Leinders-Zufall, T., Macek, B., Walzer, M., Jung, S., Pommer, B., et al. (2013). Mouse urinary peptides provide a molecular basis for genotype discrimination by nasal sensory neurons. Nature Communications, 4, 1616. doi:10.1038/ncomms2610|www.nature.com/naturecommunications.

  • Sundstrom, L. F., Lohmus, M., Johnsson, J. I., & Devlin, R. H. (2004). Growth hormone transgenic salmon pay for growth potential with increased predation mortality. Proceedings of the Royal Society of London B, 271, S350–S352.

    Google Scholar 

  • Surinov, B. P. (2007). Mice with radiation or toxic damage or malignant tumors produce aversive chemosignals repelling intact animals. Doklady Biological Science, 414, 199–201.

    CAS  Google Scholar 

  • Surinov, B. P., Isaeva, V. G., & Dukhova, B. B. (2005). Postradiation immunosuppressive and attractive urinary secretions: The “Baystander Effect” or alleleopathy in groups of animals. Doklady Biological Science, 400, 28–30.

    Google Scholar 

  • Surinov, B. P., Isaeva, V. G., & Karpova, N. A. (2008). Immunostimulating chemosignaling in animals with secondary immunodeficiency. Doklady Biological Science, 418, 41–43.

    CAS  Google Scholar 

  • Surinov, B. P., Isayeva, V. G., & Sharetsky, A. N. (2012). Direct and reverse bystander effect between irradiated and unirradiated organisms: The modulating role of chemosignalling in ecology. In C. E. Mothersill, V. Korogodina, & C. B. Seymour (Eds.), Radiobiology and environmental security (pp. 99–108). New York: Springer (NATO Science for Peace and Security Series C).

    Google Scholar 

  • Surinov, B. P., Sharetsky, A. N., Shpagin, D. V., Isayeva, V. G., & Dukhova, N. N. (2007). Post-radiated and post-stressed volatile secretions: Secondary immune and behavioral reactions in groups of animals. In C. Mothersill, I. Mosse, & C. Seymour (Eds.), Multiple stressors: A challenge for the future (pp. 127–138). New York: Springer.

    Google Scholar 

  • Takayanagi, Y., Yoshida, M., Bielsky, I. F., Ross, H. E., Kawamata, M., Onaka, T., et al. (2005). Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proceedings of the National Academy of Sciences of the United States of America, 102, 16096–16101.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Thom, M. D., Stockley, P., Jury, F., Ollier, W. E. R., Beynon, R. J., & Hurst, J. L. (2008). The direct assessment of genetic heterozygosity through scent in the mouse. Current Biology, 18, 619–623.

    CAS  PubMed  Google Scholar 

  • Thompson, R. N., McMillon, R., Napier, A., & Wekesa, K. S. (2007). Pregnancy block by MHC class peptides is mediated via the production of inositol 1,4,5-trisphosphate in the vomeronasal organ. Journal of Experimental Biology, 210, 406–412.

    Google Scholar 

  • Thornhill, R., & Gangestad, S. W. (2006). Facial sexual dimorphism, developmental stability, and susceptibility to disease in men and women. Evolution and Human Behavior, 27, 131–144.

    Google Scholar 

  • Traniello, J. F. A., Rosengaus, R. B., & Savoie, K. (2002). The development of immunity in a social insect: Evidence for the group facilitation of disease resistance. Proceedings of the National Academy of Sciences of the United States of America, 99, 6838–6842.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tsuchiya, S., Kido, N., Nagasawa, M., Mogi, K., & Kikusui, T. (2011). Different distribution patterns of activated neurons in the accessory olfactory bulb between mate partner and unfamiliar male mice in Bruce effect. Neuroscience Research, 71(Suppl), e356. doi:10.1016/j.neures.2011.07.1562.

    Google Scholar 

  • Tyner, S. D., Venkatachalam, S., Choi, J., Jones, S., Ghebraniousk, N., Igelmann, H., et al. (2002). p53 mutant mice that display early ageing-associated phenotypes. Nature, 415, 45–53.

    CAS  PubMed  Google Scholar 

  • Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M., Lee, J. J., & Lotvall, J. O. (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature Cell Bioliology, 9, 654–659.

    CAS  Google Scholar 

  • van der Vos, K. E., & Coffer, P. J. (2011). The extending network of FOXO transcriptional target genes. Antioxidants & Redox Signaling, 14, 579–592.

    Google Scholar 

  • Varela, I., Cadinanos, J., Pendas, A. M., Gutierrez-Fernandez, A., Folgueras, A. R., Sanchez, L. M., et al. (2007). Accelerated ageing in mice deficient in Zmpste24 protease is linked to p53 signalling activation. Nature, 435, 564–568.

    Google Scholar 

  • von Schantz, T., Bensch, S., Grahn, M., Hasselquist, D., & Wittzell, H. (1999). Good genes, oxidative stress and condition–dependent sexual signals. Proceedings of the Royal society of London B, 266, 1–12.

    Google Scholar 

  • Wacker, D. W., & Ludwig, M. (2012). Vasopressin, oxytocin, and social odor recognition. Hormones and Behavior, 61, 259–265.

    CAS  PubMed  Google Scholar 

  • Wang, H., Duclot, F., Liu, Y., Wang, Z., & Kabbaj, M. (2013). Histone deacetylase inhibitors facilitate partner preference formation in female prairie voles. Nature Neuroscience, 16(919–924), 2013. doi:10.1038/nn.3420.

    Google Scholar 

  • Wang, X., He, H., Leng, W., & Tang, X. (2006). Evaluation of brain-targeting for the nasal delivery of estradiol by the microdialysis method. International Journal of Pharmaceutics, 317, 40–46.

    CAS  PubMed  Google Scholar 

  • Ward, J. L., & Blum, M. J. (2012). Exposure to an environmental estrogen breaks down sexual isolation between native and invasive species. Evolutionary Applications, 5, 901–912. doi:10.1111/j.1752-4571.2012.00283.x.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Waxman, D. J., & O’Connor, C. (2006). Growth hormone regulation of sex-specific liver gene expression. Molecular Endocrinology, 20, 2613–2629.

    CAS  PubMed  Google Scholar 

  • Wersinger, S. R., Caldwell, H. K., Christiansen, M., & Young, W. S. I. I. I. (2007). Disruption of the vasopressin 1b receptor gene impairs the attack component of aggressive behavior in mice. Genes Brain and Behavior, 6, 653–660.

    CAS  Google Scholar 

  • Wersinger, S. R., Temple, J. L., Caldwell, H. K., & Young, W. S. I. I. I. (2008). Inactivation of the oxytocin and the vasopressin (Avp) 1b receptor genes, but not the Avp 1a receptor gene, differentially impairs the Bruce Effect in laboratory mice (Mus musculus). Endocrinology, 149, 116–121.

    CAS  PubMed Central  PubMed  Google Scholar 

  • West-Eberhard, M. J. (2003). Developmental plasticity and evolution (p. 794). New York: Oxford University Press.

    Google Scholar 

  • Whitlock, M. C., & Agrawal, A. F. (2009). Purging the genome with sexual selection: Reducing mutation load through selection on males. Evolution, 63, 569–582.

    CAS  PubMed  Google Scholar 

  • Willis, C. M., Church, S. M., Guest, C. M., Cook, W. A., McCarthy, N., Bransberry, A. J., et al. (2004). Olfactory detection of human bladder cancer by dogs: Proof of principle study. British Medical Journal, 329, 712–714.

    PubMed Central  PubMed  Google Scholar 

  • Willis, C., & Poulin, R. (2000). Preference of female rats for the odours of non-parasitised males: The smell of good genes? Folia Parasitology, 47, 6–10.

    CAS  Google Scholar 

  • Willse, A., Belcher, A. M., Preti, G., Wahl, J. H., Thresher, M., Yang, P., et al. (2005). Identification of major histocompatibility complex-regulated body odorants by statistical analysis of a comparative gas chromatography/mass spectrometry experiment. Analytical Chemistry, 77, 2348–2361.

    CAS  PubMed  Google Scholar 

  • Willse, A., Kwak, J., Yamazaki, K., Preti, G., Wahl, J. H., & Beauchamp, G. K. (2006). Individual odortypes: Interaction of MHC and background genes. Immunogenetics, 58, 967–982.

    CAS  PubMed  Google Scholar 

  • Winter, R. M. (1996). What’s in a face? Nature Genetics, 12, 124–129.

    CAS  PubMed  Google Scholar 

  • Yamazaki, K., Beauchamp, G., Wysocki, C., Bard, J., Thomas, L., & Boyse, E. (1983). Recognition of H-2 types in relation to the blocking of pregnancy in mice. Science, 221, 186–188.

    CAS  PubMed  Google Scholar 

  • Yamazaki, K., Boyse, E. A., Bard, J., Curran, M., Kim, D., Ross, S. R., et al. (2002). Presence of mouse mammary tumor virus specifically alters the body odor of mice. Proceedings of the National Academy of Sciences of the United States of America, 99, 5612–5615.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yamazaki, K., Boyse, E. A., Mike, V., Thaler, H. T., Mathieson, B. J., Abbott, J., et al. (1976). Control of mating preferences in mice by genes in the major histocompatibility complex. Journal of Experimental Medicine, 144, 1324–1335.

    CAS  PubMed  Google Scholar 

  • Yang, X., Meng, S., Jiang, H., Zhu, C., & Wu, W. (2011). Exosomes derived from immature bone marrow dendritic cells induce tolerogenicity of intestinal transplantation in rats. Journal of Surgical Research, 171, 826–832.

    CAS  PubMed  Google Scholar 

  • Zabel, C., Chamrad, D. C., Priller, J., Woodman, B., Meyer, H. E., Bates, G. P., et al. (2002). Alterations in the mouse and human proteome caused by Huntington’s disease. Molecular and Cellular Proteomics, 1, 366–375.

    CAS  PubMed  Google Scholar 

  • Zala, S. M., Potts, W. K., & Penn, D. J. (2004). Scent-marking displays provide honest signals of health and infection. Behavioral Ecology, 15, 338–344.

    Google Scholar 

  • Zar, J. H. (1974). Biostatistical analysis. Englewood Cliffs New Jersey: Prentice Hall.

    Google Scholar 

  • Zhou, Y., Jiang, L., & Rui, L. (2009). Identification of MUP1 as a regulator for glucose and lipid metabolism in mice. Journal of Biological Chemistry, 284, 11152–11159.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zomer, S., Dixon, S. J., Xu, Y., Jensen, S. P., Wang, H., Lanyon, C. V., et al. (2009). Consensus multivariate methods in gas chromatography mass spectrometry and denaturing gradient gel electrophoresis: MHC-congenic and other strains of mice can be classified according to the profiles of volatiles and microflora in their scent-marks. Analyst, 134, 114–123.

    CAS  PubMed  Google Scholar 

  • Zuk, M. (1996). Disease, endocrine-immune interactions, and sexual selection. Ecology, 77, 1037–1042.

    Google Scholar 

Download references

Acknowledgments

This research was supported by a grant from the Natural Sciences and Engineering Research Council of Canada to CDR. We thank Dr. Ayesha Khan for consultation and help with many aspects of the project as well as an anonomous reviewer and our editor Dr. Benedikt Hallgrimsson for facilitating publication.

Ethical standards

All experiments and protocols adhered to Canadian law and Canada Council for Animal Care and McMaster University guidelines.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. David Rollo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rollo, C.D., Kumar, A., Smith, R. et al. Trojan Genes or Transparent Genomes? Sexual Selection and Potential Impacts of Genetically Modified Animals in Natural Ecosystems. Evol Biol 41, 276–298 (2014). https://doi.org/10.1007/s11692-013-9268-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-013-9268-x

Keywords

Navigation