Longhui ZHAO,Jichao WANG,Yanlin CAI,et al.Behavioral and Neurogenomic Responses to Acoustic and Visual Sexual Cues are Correlated in Female Torrent Frogs[J].Asian Herpetological Research(AHR),2021,12(1):88-99.[doi:10.16373/j.cnki.ahr.200063]
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Behavioral and Neurogenomic Responses to Acoustic and Visual Sexual Cues are Correlated in Female Torrent Frogs
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Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]

Issue:
2021 VoI.12 No.01
Page:
88-99
Research Field:
Publishing date:
2021-03-25

Info

Title:
Behavioral and Neurogenomic Responses to Acoustic and Visual Sexual Cues are Correlated in Female Torrent Frogs
Author(s):
Longhui ZHAO123 Jichao WANG4 Yanlin CAI13 Jianghong RAN2 Steven E. BRAUTH5 Yezhong TANG1 and Jianguo CUI1*
1 Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, Sichuan, China
2 Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610041, Sichuan, China
3 University of the Chinese Academy of Sciences, Beijing 100049, China
4 Key Laboratory for Tropical Plant and Animal Ecology of Ministry of Education, College of Life Sciences, Hainan Normal University, Haikou 571158, Hainan, China
5 Department of Psychology, University of Maryland, College Park, Maryland 27042, USA
Keywords:
energy metabolism multimodal communication little torrent frogs neurogenomic states sexual traits
PACS:
-
DOI:
10.16373/j.cnki.ahr.200063
Abstract:
Diverse animal species use multimodal communication signals to coordinate reproductive behavior. Despite active research in this field, the brain mechanisms underlying multimodal communication remain poorly understood. Similar to humans and many mammalian species, anurans often produce auditory signals accompanied by conspicuous visual cues (e.g., vocal sac inflation). In this study, we used video playbacks to determine the role of vocal-sac inflation in little torrent frogs (Amolops torrentis). Then we exposed females to blank, visual, auditory, and audiovisual stimuli and analyzed whole brain tissue gene expression changes using RNA-seq. The results showed that both auditory cues (i.e., male advertisement calls) and visual cues were attractive to female frogs, although auditory cues were more attractive than visual cues. Females preferred simultaneous bimodal cues to unimodal cues. The hierarchical clustering of differentially expressed genes showed a close relationship between neurogenomic states and momentarily expressed sexual signals. We also found that the Gene Ontology terms and KEGG pathways involved in energy metabolism were mostly increased in blank contrast versus visual, acoustic, or audiovisual stimuli, indicating that brain energy use may play an important role in response to these stimuli. In sum, behavioral and neurogenomic responses to acoustic and visual cues are correlated in female little torrent frogs.

References:

Alvarez M., Schrey A. W., Richards C. L. 2015. Ten years of transcriptomics in wild populations: what have we learned about their ecology and evolution? Mol Ecol, 24: 710–725
Anders S., Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol, 11: R106
Avey M. T., Phillmore L. S., MacDougall-Shackleton S. A. 2005. Immediate early gene expression following exposure to acoustic and visual components of courtship in zebra finches. Behav Brain Res, 165: 247–253
Bahrick L. E., Lickliter R., Flom R. 2004. Intersensory redundancy guides the development of selective attention, perception, and cognition in infancy. Curr Dir Psychol Sci, 13: 99–102
Bailey D. J., Rosebush J. C., Wade J. 2002. The hippocampus and caudomedial neostriatum show selective responsiveness to conspecific song in the female zebra finch. J Neurobiol, 52: 43–51
Balakrishnan C. N., Chapus C., Brewer M. S., Clayton D. F. 2013. Brain transcriptome of the violet-eared waxbill Uraeginthus granatina and recent evolution in the songbird genome. Open Biol, 3: 130063
Balakrishnan C. N., Lin Y. C., London S. E., Clayton D. F. 2012. RNA-seq transcriptome analysis of male and female zebra finch cell lines. Genomics, 100: 363–369
Balakrishnan C. N., Mukai M., Gonser R. A., Wingfield J. C., London S. E., Tuttle E. M., Clayton D. F. 2014. Brain transcriptome sequencing and assembly of three songbird model systems for the study of social behavior. PeerJ, 2: e396
Bee M. A. 2015. Treefrogs as animal models for research on auditory scene analysis and the cocktail party problem. Int J of Psychophysiol, 95: 216–237
Bell A. M., Robinson G. E. 2011. Behavior and the dynamic genome. Science, 332: 1161–1162
Burmeister S. S., Mangiamele L. A., Lebonville C. L. 2008. Acoustic modulation of immediate early gene expression in the auditory midbrain of female túngara frogs. Brain Res, 1190: 105–114
Cardoso S. D., Teles M. C., Oliveira R. F. 2015. Neurogenomic mechanisms of social plasticity. J Exp Biol, 218: 140–149
Chandrasekaran S., Ament S. A., Eddy J. A., Rodriguez-Zas S. L., Schatz B. R., Price N. D., Robinson G. E. 2011. Behavior-specific changes in transcriptional modules lead to distinct and predictable neurogenomic states. P Natl Acad Sci USA, 108: 18020–18025
Chew S. J., Mello C., Nottebohm F., Jarvis E., Vicario D. S. 1995. Decrements in auditory responses to a repeated conspecific song are long-lasting and require two periods of protein synthesis in the songbird forebrain. P Natl Acad Sci USA, 92: 3406–3410
Clayton D. F. 2000. The genomic action potential. Neurobiol Learn Mem, 74: 185–216
Dong S., Replogle K. L., Hasadsri L., Imai B. S., Yau P. M., Rodriguez-Zas S., Southey B. R., Sweedler J. V., Clayton D. F. 2009. Discrete molecular states in the brain accompany changing responses to a vocal signal. P Natl Acad Sci USA, 106: 11364–11369
Driver J. 1996. Enhancement of selective listening by illusory mislocation of speech sounds due to lip-reading. Nature, 381: 66
Frankl-Vilches C., Kuhl H., Werber M., Klages S., Kerick M., Bakker A., de Oliveira E. H. C., Reusch C., Capuano F., Vowinckel J., Leitner S., Ralser M., Timmermann B., Gahr M. 2015. Using the canary genome to decipher the evolution of hormone-sensitive gene regulation in seasonal singing birds. Genome Biol, 16: 19
Gomez D., Richardson C., Lengagne T., Plenet S., Joly P., Lena J., Thery M. 2009. The role of nocturnal vision in mate choice: females prefer conspicuous males in the European tree frog (Hyla arborea). P Roy Soc B-Biol Sci, 276: 2351–2358
Grabherr M. G., Haas B. J., Yassour M., Levin J. Z., Thompson D. A., Amit I., Adiconis X., Fan L., Raychowdhury R., Zeng Q., Chen Z., Mauceli E., Hacohen N., Gnirke A., Rhind N., di Palma F., Birren B. W., Nusbaum C., Lindblad-Toh K., Friedman N., Regev A. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol, 29: 644–652
Halfwerk W., Varkevisser J., Simon R., Mendoza E., Scharff C., Riebel K. 2019. Toward testing for multimodal perception of mating signals. Front Ecol Evol, 7: 1–7
Hebets E. A., Papaj D. R. 2004. Complex signal function: developing a framework of testable hypotheses. Behav Ecol Sociobiol, 57: 197–214
Hoke K. L., Ryan M. J., Wilczynski W. 2007. Integration of sensory and motor processing underlying social behaviour in túngara frogs. P Roy Soc B-Biol Sci, 274: 641–649
Kruse A. A., Stripling R., Clayton D. F. 2004. Context-specific habituation of the zenk gene response to song in adult zebra finches. Neurobiol Learn Mem, 82: 99–108
Li B., Dewey C. N. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12: 323
Lovell P. V., Clayton D. F., Replogle K. L., Mello C. V. 2008. Birdsong “transcriptomics”: neurochemical specializations of the oscine song system. PLoS ONE, 3: e3440
McDonald J. J., Teder-SaElejaErvi W. A., Hillyard S. A. 2000. Involuntary orienting to sound improves visual perception. Nature, 407: 906
McGurk H., MacDonald J. 1976. Hearing lips and seeing voices. Nature, 264: 746
Narins P. M., Grabul D. S., Soma K. K., Gaucher P., Hodl W. 2005. Cross-modal integration in a dart-poison frog. P Natl Acad Sci USA, 102: 2425–2429
Narins P. M., Hodl W., Grabul D. S. 2003. Bimodal signal requisite for agonistic behavior in a dart-poison frog, Epipedobates femoralis. P Natl Acad Sci USA, 100: 577–580
Partan S. R. 2013. Ten unanswered questions in multimodal communication. Behav Ecol Sociobiol, 67: 1523–1539
Partan S. R., Marler P. 1999. “Communication goes multimodal.” Science, 283: 1272–1273
Partan S. R., Marler P. 2005. Issues in the classification of multimodal communication signals. Am Nat, 166: 231–245
Pauly G. B., Bernal X. E., Rand A. S., Ryan M. J. 2006. The vocal sac increases call rate in the túngara frog, Physalaemus pustulosus. Physiol Biochem Zool, 79: 708–719
Preininger D., Boeckle M., Freudmann A., Starnberger I., Sztatecsny M., Hodl W. 2013a. Multimodal signaling in the Small Torrent Frog (Micrixalus saxicola) in a complex acoustic environment. Behav Ecol Sociobiol, 67: 1449–1456
Preininger D., Stiegler M. J., Gururaja K. V., Vijayakumar S. P., Torsekar V. R., Sztatecsny M., Hodl W. 2013b. Getting a kick out of it: Multimodal signalling during male–male encounters in the foot-flagging frog Micrixalus aff. saxicola from the Western Ghats of India. Curr Sci, 105(12): 1735–1740
Raichle M. E. 2015. The restless brain: how intrinsic activity organizes brain function. Philos Trans R Soc Lond B Biol Sci, 370: 20140172
Richardson C., Popovici J., Bellvert F., Lengagne T. 2009. Conspicuous colouration of the vocal sac of a nocturnal chorusing treefrog: carotenoid-based? Amphibia-Reptilia, 30: 576–580
Rittschof C. C., Schirmeier S. 2018. Insect models of central nervous system energy metabolism and its links to behavior. Glia, 66: 1160–1175
Robinson G. E., Fernald R. D., Clayton D. F. 2008. Genes and social behavior. Science, 322: 896–900
Rosenthal G. G., Rand A. S., Ryan M. J. 2004. The vocal sac as a visual cue in anuran communication: an experimental analysis using video playback. Anim Behav, 68: 55–58
Rowe C. 1999. Receiver psychology and the evolution of multicomponent signals. Anim Behav, 58: 921–931
Ryan M. J., Page R. A., Hunter K. L., Taylor R. C. 2018. ‘Crazy love’: nonlinearity and irrationality in mate choice. Anim Behav, 147: 189–198
Stange N., Page R. A., Ryan M. J., Taylor R. C. 2017. Interactions between complex multisensory signal components result in unexpected mate choice responses. Anim Behav, 134: 239–247
Starnberger I., Preininger D., H?dl W. 2014a. The anuran vocal sac: a tool for multimodal signalling. Anim Behav, 97: 281–288
Starnberger I., Preininger D., Hodl W. 2014b. From uni- to multimodality: towards an integrative view on anuran communication. J Comp Physiol A, 200: 777–787
Storey J. D., Tibshirani R. 2003. Statistical significance for genomewide studies. P Natl Acad Sci USA, 100: 9440–9445
Stripling R., Volman S. F., Clayton D. F. 1997. Response modulation in the zebra finch caudal neostriatum: relationship to nuclear gene regulation. J Neurosci, 17: 3883–3893
Taylor R. C., Klein B. A., Stein J., Ryan M. J. 2008. Faux frogs: multimodal signalling and the value of robotics in animal behaviour. Anim Behav, 76: 1089–1097
Taylor R. C., Page R. A., Klein B. A., Ryan M. J., Hunter K. L. 2017. Perceived synchrony of frog multimodal signal components is influenced by content and order. Integr Comp Biol, 57: 902–909
Taylor R. C., Ryan M. J. 2013. Interactions of multisensory components perceptually rescue túngara frog mating signals. Science, 341: 273–274
Terleph T. A., Tremere L. A. 2006. The use of immediate early genes as mapping tools for neuronal activation: concepts and methods. In Pinaud R. and Tremere L. A. (Eds), Immediate Early Genes in Sensory Processing, Cognitive Performance and Neurological Disorders, Springer, Boston, 1–10
Toth A. L., Varala K., Henshaw M. T., Rodriguez-Zas S. L., Hudson M. E., Robinson G. E. 2010. Brain transcriptomic analysis in paper wasps identifies genes associated with behaviour across social insect lineages. P Roy Soc B-Biol Sci, 277: 2139–2148
Wolf C., Linden D. E. 2012. Biological pathways to adaptability—interactions between genome, epigenome, nervous system and environment for adaptive behavior. Genes Brain Behav, 11: 3–28
Zayed A., Robinson G. E. 2012. Understanding the relationship between brain gene expression and social behavior: lessons from the honey bee. Annu Rev Genet, 46: 591–615
Zhao L., Wang J., Yang Y., Zhu B., Brauth S. E., Tang Y., Cui J. 2017a. An exception to the matched filter hypothesis: A mismatch of male call frequency and female best hearing frequency in a torrent frog. Ecol Evol, 7: 419–428
Zhao L., Zhu B., Wang J., Brauth S. E., Tang Y., Cui J. 2017b. Sometimes noise is beneficial: stream noise informs vocal communication in the little torrent frog Amolops torrentis. J Ethol, 35: 259–267

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Last Update: 2021-03-25