Brain, Behavior and Evolution
LaDage L.D.a· Yu T.b· Zani P.A.caDivision of Mathematics & Natural Sciences, Penn State Altoona, Altoona, PA, USA
bDepartment of Biochemistry & Molecular Biology, The Pennsylvania State University, University Park, PA, USA
cDepartment of Biology, University of Wisconsin – Stevens Point, Stevens Point, WI, USA
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Article / Publication Details
Received: November 17, 2021
Accepted: April 28, 2022
Published online: May 10, 2022
Number of Print Pages: 11
Number of Figures: 4
Number of Tables: 0
ISSN: 0006-8977 (Print)
eISSN: 1421-9743 (Online)
For additional information: https://www.karger.com/BBE
AbstractSeveral areas of the vertebrate brain are involved in facilitating and inhibiting the production of sexual behaviors and displays. In the laboratory, a higher rate of sexual displays is correlated with a larger ventral posterior amygdala (VPA), an area of the brain involved in the expression of sexual display behaviors, as well as larger VPA neuronal somas. However, it remains unclear if individuals in the field reflect similar patterns, as there are likely many more selective pressures in the field that may also modulate the VPA architecture. In this study, we examined variation in VPA volume and neuron soma volume in wild-caught common side-blotched lizards (Uta stansburiana) from two different populations. In a population from Nevada, males experience high predation pressure and have decreased sexual display rates during the breeding season, whereas a population in Oregon has lower levels of predation and higher rates of male sexual displays. We found that wild-caught males from the population with lower display rates also exhibited decreased VPA volume and VPA neuron cell soma volume, which may suggest that decreased display rate, possibly due to increased predation rate, covaries with VPA attributes.
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References Alexander BM, Rose JD, Stellflug JN, Fitzgerald JA, Moss GE. Low-sexually performing rams but not male-oriented rams can be discriminated by cell size in the amygdala and preoptic area: a morphometric study. Behav Brain Res. 2001;119:15–21. Amdekar MS, Thaker M. Risk of social colours in an agamid lizard: implications for the evolution of dynamic signals. Biol Lett. 2019;15:20190207. Baas D, Aleman A, Kahn RS. Lateralization of amygdala activation: a systemic review of functional neuroimaging studies. Brain Res Rev. 2004;45:96–103. Baird TA, York JR. Does courtship behavior predict parentage in collared lizards? Influence of male social status and habitat structure. Evol Ecol. 2021;35(5–6):795–808. Bajer K, Molnar O, Torok J, Herczeg G. Temperature, but not available energy, affects the expression of a sexually selected ultraviolet (UV) color trait in male European green lizards. PLoS One. 2012;7:e34359. Ball GF, Balthazart J. Hormonal regulation of brain circuits mediating male sexual behavior in birds. Physiol Behav. 2004;83:329–46. Beck LA, O’Bryant EL, Wade JS. Sex and seasonal differences in morphology of limbic forebrain nuclei in the green anole lizard. Brain Res. 2008;1227:68–75. Been LE, Petrulis A. Chemosensory and hormone information are relayed directly between the medial amygdala, posterior bed nucleus of the stria terminalis, and medial preoptic area in male Syrian hamsters. Horm Behav. 2011;59:536–48. Bruce LL, Neary TJ. The limbic system of tetrapods: a comparative analysis of cortical and amygdalar populations. Brain Behav Evol. 1995;46:224–34. Bula PA, Wright LK, Zani PA. Geographic variation in lizard hind-limb morphology in relation to predation: no evidence for an evolutionary basis. Evol Ecol Res. 2014;16:663–87. Bupesh M, Legaz I, Abellán A, Medina L. Multiple telencephalic and extratelencephalic embryonic domains contribute neurons to the medial extended amygdala. J Comp Neurol. 2010;519:1505–25. Calisi RM, Bentley GE. Lab and field experiments: are they the same animal? Horm Behav. 2009;56:1–10. Candolin U. Predation risk affects courtship and attractiveness of competing threespine stickleback males. Behav Ecol Sociobiol. 1997;41(2):81–7. Canteras NS, Simerly RB, Swanson LW. Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol. 1995;360:213–45. Cooke BM. Steroid-dependent plasticity in the medial amygdala. Neuroscience. 2006;138:997–1005. Cooke BM, Breedlove SM, Jordan CL. Both estrogen receptors and androgen receptors contribute to testosterone-induced changes in the morphology of the medial amygdala and sexual arousal in male rats. Horm Behav. 2003;43:336–46. Cooke BM, Hegstrom CD, Breedlove SM. Photoperiod-dependent response to androgen in the medial amygdala of the Siberian hamster, Phodopus sungorus. J Biol Rhythms. 2002;17:147–54. Cooke BM, Hegstrom CD, Keen A, Breedlove SM. Photoperiod and social cues influence the medial amygdala but not the bed nucleus of the stria terminalis in the Siberian hamster. Neurosci Lett. 2001;312:9–12. Cooke BM, Tabibnia G, Breedlove SM. A brain sexual dimorphism controlled by adult circulating androgens. Proc Natl Acad Sci U S A. 1999;96:7538–40. Coolen LM, Peters HJ, Veening JG. Distribution of Fos immunoreactivity following mating versus anogenital investigation in the male rat brain. Neuroscience. 1997;77:1151–61. Coolen LM, Wood RI. Bidirectional connections of the medial amygdaloid nucleus in the Syrian hamster brain: simultaneous anterograde and retrograde tract tracing. J Comp Neurol. 1998;399:189–209. Coolen LM, Wood RI. Testosterone stimulation of the medial preoptic area and medial amygdala in the control of male hamster sexual behavior: redundancy without amplification. Behav Brain Res. 1999;98:143–53. Crews D, Morgentaler A. Effects of intracranial implantation of oestradiol and dihydrotestosterone on the sexual behaviour of the lizard Anolis carolinensis. J Endocrinol. 1979;82:373–81. Denardo DF, Licht P. Effects of corticosterone on social behavior of male lizards. Horm Behav. 1993;27:184–99. Duvarci S, Paré D. Glucocorticoids enhance the excitability of principal basolateral amygdala neurons. J Neurosci. 2007;27:4482–91. Eifler DA, Eifler MA, Harris BR. Foraging under the risk of predation in desert grassland whiptail lizards (Aspidoscelis uniparens). J Ethol. 2008;26:219–23. Ellis L. Dominance and reproductive success among nonhuman animals: a cross-species comparison. Ethol Sociobiol. 1995;16(4):257–333. Endler JA. Natural selection on color patterns in Poecilia reticulata. Evolution. 1980;34(1):76–91. Endler JA. Predation, light intensity and courtship behaviour in Poecilia reticulata (Pisces: Poeciliidae). Anim Behav. 1987;35(5):1376–85. Endler JA. Multiple-trait coevolution and environmental gradients in guppies. Trends Ecol Evol. 1995;10:22–9. Fisher DN, Kilgour RJ, Siracusa ER, Foote JR, Hobson EA, Montiglio PO, et al. Anticipated effects of abiotic environmental change on intraspecific social interactions. Biol Rev Camb Philos Soc. 2021;96(6):2661–93. Fiske P, Rintamäki PT, Karvonen E. Mating success in lekking males: a meta-analysis. Behav Ecol. 1998;9(4):328–38. Forsgren E, Amundsen T, Borg AA, Bjelvenmark J. Unusually dynamic sex roles in a fish. Nature. 2004;429:551–4. García-López M, Abellán A, Legaz I, Rubenstein JL, Puelles L, Medina L. Histogenetic compartments of the mouse centromedial and extended amygdala based on gene expression patterns during development. J Comp Neurol. 2008;506:46–74. Giery ST, Layman CA. Interpopulation variation in a condition-dependent signal: predation regime affects signal intensity and reliability. Am Nat. 2015;186(2):187–95. Greenberg N. A forebrain atlas and stereotaxic technique for the lizard, Anolis carolinensis. J Morphol. 1982;174:217–36. Greenberg N, Scott M, Crews D. Role of the amygdala in the reproductive and aggressive behavior of the lizard (Anolis carolinensis). Physiol Behav. 1984;32:147–51. Gundersen HJ, Jensen EB. The efficiency of systematic sampling in stereology and its prediction. J Microsc. 1987;147:229–63. Gundersen HJ, Jensen EB, Kiêu K, Nielsen J. The efficiency of systemic sampling in stereology: reconsidered. J Microsc. 1999;193:199–211. Head ML, Lindholm AK, Brooks R. Operational sex ratio and density do not affect directional selection on male sexual ornaments and behavior. Evolution. 2007;62:135–44. Head ML, Wong BB, Brooks R. Sexual display and mate choice in an energetically costly environment. PLoS One. 2010;5:e15279. Hoops D, Desfilis E, Ullmann JFP, Janke AL, Stait-Gardner T, Devenyi GA, et al. A 3D MRI-based atlas of a lizard brain. J Comp Neurol. 2018;526:2511–47. Hull EM, Dominguez JM. Sexual behavior in male rodents. Horm Behav. 2007;52:45–55. Hunt J, Brooks R, Jennions MD, Smith MJ, Bentsen CL, Bussière LF. High-quality male field crickets invest heavily in sexual display but die young. Nature. 2004;432:1024–7. Husak JF, Macedonia JM, Fox SF, Sauceda RC. Predation cost of conspicuous male coloration of collared lizards (Crotaphytus collaris): an experimental test using clay-covered model lizards. Ethol. 2006;112:572–80. Ishii KK, Touhara K. Neural circuits regulating sexual behaviors via the olfactory system in mice. Neurosci Res. 2018;140:59–76. Jirotkul M. Operational sex ratio influences female preference and male-male competition in guppies. Anim Behav. 1999;58:287–94. Johnson MA, Wade J. Neuroendocrinology of reptilian reproductive behavior. In: Norris DO, Lopez KH, editors. Hormones and reproduction of vertebrates. Academic Press; 2011. p. 39–61. Johnson S, Candolin U. Predation cost of a sexual signal in the threespine stickleback. Behav Ecol. 2017;28(4):1160–5. Kabelik D, Weiss SL, Moore MC. Steroid hormones alter neuroanatomy and aggression independently in the tree lizard. Physiol Behav. 2008;93:492–501. Keogh JS, Noble DW, Wilson EE, Whiting MJ. Activity predicts male reproductive success in a polygynous lizard. PLoS One. 2012;7:e38856. Kverková K, Polonyiová A, Kubička L, Nĕmec P. Individual and age-related variation of cellular brain composition in a squamate reptile. Biol Lett. 2020;16:20200280. Laberge F, Mühlenbrock-Lenter S, Grunwald W, Roth G. Evolution of the amygdala: new insights from studies in amphibians. Brain Behav Evol. 2006;67:177–87. LaDage LD, Maged RM, Forney MV, Roth TC II, Sinervo B, Pravosudov VV, et al. Interaction between territoriality, spatial environment, and hippocampal neurogenesis in male side-blotched lizards. Behav Neurosci. 2013;127:555–65. LaDage LD, Riggs BJ, Sinervo B, Pravosudov VV. Dorsal cortex volume in male side-blotched lizards (Uta stansburiana) is associated with different space use strategies. Anim Behav. 2009;78:91–6. LaDage LD, Roth TC II, Downs CJ, Sinervo B, Pravosudov VV. Increased testosterone decreases medial cortical volume and neurogenesis in territorial side-blotched lizards (Uta stansburiana). Front Neurosci. 2017;11:97. LaDage LD, Roth TC, Sinervo B, Pravosudov VV. Environmental experiences influence cortical volume in territorial and nonterritorial side-blotched lizards, Uta stansburiana. Anim Behav. 2016;115:11–8. Lanuza E, Martínez-Marcos A, Martínez-García F. What is the amygdala? A comparative approach. Trends Neurosci. 1999;22:207–8. Lehman MN, Winans SS, Powers JB. Medial nucleus of the amygdala mediates chemosensory control of male hamster sexual behavior. Science. 1980;210:557–60. Lovelock DF, Deak T. Acute stress imposed during adolescence yields heightened anxiety in Sprague Dawley rats that persists into adulthood: sex differences and potential involvement of the medial amygdala. Brain Res. 2019;1723:146392. Lovern MB, Holmes MM, Fuller CO, Wade J. Effects of testosterone on the development of neuromuscular systems and their target tissues involved in courtship and copulation in green anoles (Anolis carolinensis). Horm Behav. 2004;45:295–305. Lovern MB, Wade J. Maternal plasma and egg yolk testosterone concentrations during embryonic development in green anoles (Anolis carolinensis). Gen Comp Endocrinol. 2001;124:226–35. MacLeod KJ, McCormick GL, Langkilde T. Glucocorticoids do not influence a secondary sexual trait or its behavioral expression in eastern fence lizards. Sci Rep. 2019;9:5229. Magnhagen C. Predation risk as a cost of reproduction. Trends Ecol Evol. 1991;6:183–6. Maras PM, Petrulis A. Chemosensory and steroid-responsive regions of the medial amygdala regulate distinct aspects of opposite-sex odor preference in male Syrian hamsters. Eur J Neurosci. 2006;24:3541–52. Marcuzzo S, Dall’oglio A, Ribeiro MF, Achaval M, Rasia-Filho AA. Dendritic spines in the posterodorsal medial amygdala after restraint stress and ageing in rats. Neurosci Lett. 2007;424:16–21. Marshall KL, Philpot KE, Stevens M. Conspicuous male coloration impairs survival against avian predators in Aegean wall lizards, Podarcis erhardii. Ecol Evol. 2015;5:4115–31. Martins EP, Ossip-Klein AG, Zúñiga-Vega JJ, García CV, Campos SM, Hews DK. Evolving from static to dynamic signals: evolutionary compensation between two communicative signals. Anim Behav. 2015;102:223–9. Medina L, Abellan A, Desfilis E. Evolving Views on the Pallium. Brain Behav Evol. 2021;96:181–199. Medina L, Abellan A, Desfilis E. A Never-Ending Search for the Evolutionary Origin of the Neocortex: Rethinking the Homology Concept. Brain Behav Evol. 2013;81:150–153. Medina L, Bupesh M, Abellán A. Contribution of genoarchitecture to understanding forebrain evolution and development, with particular emphasis on the amygdala. Brain Behav Evol. 2011;78:216–36. Michelangeli M, Tuomainen U, Candolin U, Wong BBM. Habitat alteration influences male signalling effort in the Australian desert goby. Behav Ecol. 2015;26(4):1164–9. Moga MM, Geib BM, Zhou D, Prins GS. Androgen receptor-immunoreactivity in the forebrain of the eastern fence lizard (Sceloporus undulatus). Brain Res. 2000;879:174–82. Neal JK, Wade J. Androgen receptor expression and morphology of forebrain and neuromuscular systems in male green anoles displaying individual differences in sexual behavior. Horm Behav. 2007;52:228–36. Newman SW. The medial extended amygdala in male reproductive behavior: a node in the mammalian social behavior network. Ann N Y Acad Sci. 1999;877:242–57. Oberlander JG, Schlinger BA, Clayton NS, Saldanha CJ. Neural aromatization accelerates the acquisition of spatial memory via an influence on the songbird hippocampus. Horm Behav. 2004;45:250–8. O’Bryant EL, Wade J. Seasonal and sexual dimorphisms in the green anode forebrain. Horm Behav. 2002;41:384–395. Oka K, Kohno S, Urushitani H, Guillette LJ Jr, Ohta Y, Iguchi T, et al. Molecular cloning and characterization of the corticoid receptors from the American alligator. Mol Cell Endocrinol. 2013;365:153–61. Ossip-Drahos AG, Oyola Morales JR, Vital-García C, Zúñiga-Vega JJ, Hews DK, Martins EP. Shaping communicative colour signals over evolutionary time. R Soc Open Sci. 2016;3:160728. Parker WS, Pianka ER. Comparative ecology of populations of the lizard Uta stansburiana. Copeia. 1975;1975(4):615–32. Pearson AK, Tsui HW, Licht P. Effect of temperature on spermatogenesis, on the production and action of androgens and on the ultrastructure of gonadotropic cells in the lizard Anolis carolinensis. J Exp Zool. 1976;195(2):291–303. Peters RA, Evans CS. Design of the Jacky dragon visual display: signal and noise characteristics in a complex moving environment. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2003;189:447–59. Pfaff DW, Schwanzel-Fukuda M, Parhar IS, Lauber AH, McCarthy LM, Kow LM. GnRH neurons and other cellular and molecular mechanisms for simple mammalian reproductive behaviors. Recent Prog Horm Res. 1994;49:1–25. Pitkänen A, Jolkkonen E, Kemppainen S. Anatomic heterogeneity of the rat amygdaloid complex. Folia Morphol. 2000;59:1–24. Powers AS. Plasticity and adult neurogenesis in amphibians and reptiles: more questions than answers. Brain Behav Evol. 2016;87(3):175–83. Raam T, Hong W. Organization of neural circuits underlying social behavior: a consideration of the medial amygdala. Curr Opin Neurobiol. 2021;68:124–36. Riters LV, Eens M, Pinxten R, Duffy DL, Balthazart J, Ball GF. Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris). Horm Behav. 2000;38:250–61. Roth TC, Brodin A, Smulders TV, LaDage LD, Pravosudov VV. Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus. Philos Trans R Soc Lond B Biol Sci. 2010;365:915–31. Równiak M, Bogus-Nowakowska K, Kalinowski D, Kozlowska A. The evolutionary trajectories of the individual amygdala nuclei in the common shrew, guinea pig, rabbit, fox and pig: a consequence of embryological fate and mosaic-like evolution. J Anat. 2021;240:489–502. Salvador A, Diaz JA, Veiga JP, Bloor P, Brown RP. Correlates of reproductive success in male lizards of the alpine species Iberolacerta cyreni. Behav Ecol. 2008;19:169–76. Sapolsky RM, Romero LM, Munck AU. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev. 2000;21:55–89. Schořálková T, Kratochvíl L, Kubička L. To fight or mate? Hormonal control of sex recognition, male sexual behavior and aggression in the gecko lizard. Horm Behav. 2018;97:18–24. Scotti MA, Rendon NM, Greives TJ, Romeo RD, Demas GE. Short-day aggression is independent of changes in cortisol or glucocorticoid receptors in male Siberian hamsters (Phodopus sungorus). J Exp Zool A Ecol Genet Physiol. 2015;323:331–41. Smith GD, Zani PA, French SS. Life-history differences across latitude in common side-blotched lizards (Uta stansburiana). Ecol Evol. 2019;9:5743–51. Simon VB. Not all signals are equal: male brown anole lizards (Anolis sagrei) selectively decrease pushup frequency following a simulated predatory attack. Ethology. 2007;113(8):793–801. Snell HL, Jennings RD, Snell HM, Harcourt S. Intrapopulation variation in predator-avoidance performance of Galapagos lava lizards: the interaction of sexual and natural selection. Evol Ecol. 1988;2:353–69. Steinberg DS, Losos JB, Schoener TW, Spiller DA, Kolbe JJ, Leal M. Predation-associated modulation of movement-based signals by a Bahamian lizard. Proc Natl Acad Sci U S A. 2014;111:9187–92. Sullivan BK, Kwiatkowski MA. Courtship displays in anurans and lizards: theoretical and empirical contributions to our understanding of costs and selection on males due to female choice. Funct Ecol. 2007;21(4):666–75. Summers CH, Larson ET, Ronan PJ, Hofmann PM, Emerson AJ, Renner KJ. Serotonergic responses to corticosterone and testosterone in the limbic system. Gen Comp Endocrinol. 2000;117:151–9. Swanson LW, Petrovich GD. What is the amygdala? Trends Neurosci. 1998;21:323–31. Swierk L, Boyer JFF, Chang J, Petelo M, Drobniak SM. Intrasexual variability of a conspicuous social signal influences attack rate of lizard models in an experimental test. Evol Ecol. 2021;35(1):131–46. Tarr RS. Role of the amygdala in the intraspecies aggressive behavior of the iguanid lizard, Sceloporus occidentalis. Physiol Behav. 1977;18:1153–8. Thaker M, Vanak AT, Lima SL, Hews DK. Stress and aversive learning in wild vertebrate: the role of corticosterone in mediating escape from a novel stressor. Am Nat. 2010;175:50–60. Thompson RR, Adkins-Regan E. Photoperiod affects the morphology of a sexually dimorphic nucleus within the preoptic area of male Japanese quail. Brain Res. 1994;667:201–8. Torsekar VR, Balakrishnan R. Sex differences in alternative reproductive tactics in response to predation risk in tree crickets. Funct Ecol. 2020;34(11):2326–37. Tosches MA. From cell types to an integrated understanding of brain evolution: the case of the cerebral cortex. Annu Rev Cell Dev Biol. 2021;37(1):495–517. Tosches MA, Yamawaki TM, Naumann RK, Jacobi AA, Tushev G, Laurent G. Evolution of pallium, hippocampus, and cortical cell types revealed by single-cell transcriptomics in reptiles. Science. 2018;360:881–8. Vervust B, Grbac I, Van Damme R. Differences in morphology, performance and behaviour between recently diverged populations of Podarcis sicula mirror differences in predation pressure. Nordic Soc Oikos. 2007;116:1343–52. Wade J, Crews D. The relationship between reproductive state and “sexually” dimorphic brain areas in sexually reproducing and parthenogenetic whiptail lizards. J Comp Neurol. 1991;309:507–14. Wade J, Huang JM, Crews D. Hormonal control of sex differences in the brain, behavior and accessory sex structures of whiptail lizards (Cnemidophorus species). J Neuroendocrinol. 1993;5:81–93. Weir LK, Grant JW, Hutchings JA. The influence of operational sex ratio on the intensity of competition for mates. Am Nat. 2011;177:167–76. Wingfield JC, Maney DL, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, et al. Ecological bases of hormone-behavior interactions: the “emergency life history stage. Int Comp Biol. 1998;38:191–206. Wood RI. Thinking about networks in the control of male hamster sexual behavior. Horm Behav. 1997;32:40–5. Wood RI, Coolen LM. Integration of chemosensory and hormonal cues is essential for sexual behavior in the male Syrian hamster: role of medial amygdaloid nucleus. Neurosci. 1997;78:1027–35. Wood RI, Newman SW. Integration of chemosensory and hormonal cues is essential for mating in the male Syrian hamster. J Neurosci. 1995;15:7261–9. Young LJ, Lopreato GF, Horan K, Crews D. Cloning and in situ hybridization analysis of estrogen receptor, progesterone receptor, and androgen receptor expression in the brain of whiptail lizards (Cnemidophorus uniparens and C. inornatus). J Comp Neurol. 1994;347:288–300. Zani PA, Tillman JL, Scoular KM. Geographic variation of movement and display behavior of side-blotched lizards (Uta stansburiana). J Herpetol. 2013;47:85–92. Article / Publication Details
Received: November 17, 2021
Accepted: April 28, 2022
Published online: May 10, 2022
Number of Print Pages: 11
Number of Figures: 4
Number of Tables: 0
ISSN: 0006-8977 (Print)
eISSN: 1421-9743 (Online)
For additional information: https://www.karger.com/BBE
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