Ultrasonic vocalizations in house mice depend upon genetic relatedness of mating partners and correlate with subsequent reproductive success

Doris Nicolakis1, Maria Adelaide Marconi1, Sarah M. Zala1, Dustin J. Penn1
1Konrad Lorenz Institute of Ethology, Department of Interdisciplinary Life Sciences, University of Veterinary Medicine, Vienna, Savoyenstraße 1a, 1160, Vienna, Austria

Tóm tắt

Abstract Background

Courtship vocalizations are used by males of many species to attract and influence the behavior of potential mating partners. Our aim here was to investigate the modulation and reproductive consequences of courtship ultrasonic vocalizations (USVs) in wild-derived house mice (Mus musculus musculus). The courtship USVs of male mice are surprisingly complex and are composed of a variety of different syllable types. Our specific aims were to test whether (1) the emission of courtship USVs depends upon the kinship of a potential mating partner, and (2) whether USV emission during courtship affects the pairs’ subsequent reproductive success.

Results

We experimentally presented males with an unfamiliar female that was either genetically related or unrelated, and we recorded USV emission, first while the sexes were separated by a perforated partition and then during direct interactions, after removing the partition. USVs were detected by the Automatic Mouse Ultrasound Detector (A-MUD) and manually classified into 15 syllable types. The mice were kept together to test whether and how courtship vocalizations predict their subsequent reproductive success. We found that the mice significantly increased their amount of vocalizations (vocal performance) and number of syllable types (vocal repertoire) after the partition was removed and they began interacting directly. We show that unrelated pairs emitted longer and more complex USVs compared to related pairs during direct interactions. Unrelated pairs also had a greater reproductive success compared to related pairs, and in addition we found a negative correlation between the mean length and amount of vocalizations with the latency to their first litter.

Conclusion

Our study provides evidence that house mice modulate the emission of courtship USVs depending upon the kinship of potential mating partners, and that courtship USVs correlate with reproductive success.

Từ khóa


Tài liệu tham khảo

Searcy WA, Andersson M. Sexual selection and the evolution of song. Annu Rev Ecol Syst. 1986;17:507–33.

Kroodsma DE, Byers BE. The function(s) of bird song. Am Zool. 1991;31:318–28.

Brockway BF. Stimulation of ovarian development and egg laying by male courtship vocalization in budgerigars (Melopsittacus undulatus). Anim Behav. 1965;13:575–8.

Dunning JL, Pant S, Bass A, Coburn Z, Prather JF. Mate choice in adult female Bengalese finches: females express consistent preferences for individual males and prefer female-directed song performances. PLoS One. 2014;9:e89438.

Clutton-Brock T, McAuliffe K. Female mate choice in mammals. Q Rev Biol. 2009;84:3–27.

Holy TE, Guo Z. Ultrasonic songs of male mice. PLoS Biol. 2005;3:e386.

Musolf K, Penn DJ. Ultrasonic vocalizations in house mice: a cryptic mode of acoustic communication. In Evolution of the House Mouse. Volume 3. Edited by Macholán M, Baird SJE, Munclinger P, Piálek J. Cambridge: Cambridge University Press; 2012: 253-77: Cambridge Studies in Morphology and Molecules: New Paradigms in Evolutionary Biology.

Portfors CV. Types and functions of ultrasonic vocalizations in laboratory rats and mice. J Am Assoc Lab Anim Sci. 2007;46:28–34.

Portfors CV, Perkel DJ. The role of ultrasonic vocalizations in mouse communication. Curr Opin Neurobiol. 2014;28:115–20.

Asaba A, Hattori T, Mogi K, Kikusui T. Sexual attractiveness of male chemicals and vocalizations in mice. Front Neurosci. 2014;8:231.

Scattoni ML, Crawley J, Ricceri L. Ultrasonic vocalizations: a tool for behavioural phenotyping of mouse models of neurodevelopmental disorders. Neurosci Biobehav Rev. 2009;33:508–15.

Chabout J, Sarkar A, Patel SR, Radden T, Dunson DB, Fisher SE, Jarvis ED. A Foxp2 mutation implicated in human speech deficits alters sequencing of ultrasonic vocalizations in adult male mice. Front Behav Neurosci. 2016;10:197.

Fernández-Vargas M. Vocal signals of sexual motivation in male and female rodents. Curr Sex Health Rep. 2018;10:315–28.

Matsumoto YK, Okanoya K. Phase-specific vocalizations of male mice at the initial encounter during the courtship sequence. PLoS One. 2016;11:e0147102.

Zala SM, Reitschmidt D, Noll A, Balazs P, Penn DJ. Sex-dependent modulation of ultrasonic vocalizations in house mice (Mus musculus musculus). PLoS One. 2017;12:e0188647.

Hammerschmidt K, Radyushkin K, Ehrenreich H, Fischer J. Female mice respond to male ultrasonic ‘songs’ with approach behaviour. Biol Lett. 2009;5:589–92.

Musolf K, Hoffmann F, Penn DJ. Ultrasonic courtship vocalizations in wild house mice, Mus musculus. Anim Behav. 2010;79:757–64.

Asaba A, Osakada T, Touhara K, Kato M, Mogi K, Kikusui T. Male mice ultrasonic vocalizations enhance female sexual approach and hypothalamic kisspeptin neuron activity. Horm Behav. 2017;94:53–60.

Chabout J, Sarkar A, Dunson DB, Jarvis ED. Male mice song syntax depends on social contexts and influences female preferences. Front Behav Neurosci. 2015;9:76.

Musolf K, Meindl S, Larsen AL, Kalcounis-Rueppell MC, Penn DJ. Ultrasonic vocalizations of male mice differ among species and females show Assortative preferences for male calls. PLoS One. 2015;10:e0134123.

Kanno K, Kikusui T. Effect of Sociosexual experience and aging on number of courtship ultrasonic vocalizations in male mice. Zool Sci. 2018;35:208–14.

Hoffmann F, Musolf K, Penn DJ. Freezing urine reduces its efficacy for eliciting ultrasonic vocalizations from male mice. Physiol Behav. 2009;96:602–5.

Hoffmann F, Musolf K, Penn DJ. Ultrasonic courtship vocalizations in wild house mice: spectrographic analyses. J Ethol. 2012;30:173–80.

von Merten S, Hoier S, Pfeifle C, Tautz D. A role for ultrasonic vocalisation in social communication and divergence of natural populations of the house mouse (Mus musculus domesticus). PLoS One. 2014;9:e97244.

Wang H, Liang S, Burgdorf J, Wess J, Yeomans J. Ultrasonic vocalizations induced by sex and amphetamine in M2, M4, M5 muscarinic and D2 dopamine receptor knockout mice. PLoS One. 2008;3:e1893.

Hanson JL, Hurley LM. Female presence and estrous state influence mouse ultrasonic courtship vocalizations. PLoS One. 2012;7:e40782.

Neunuebel JP, Taylor AL, Arthur BJ, Egnor SER. Female mice ultrasonically interact with males during courtship displays. eLife 2015;4:e06203.

Warren MR, Spurrier MS, Roth ED, Neunuebel JP. Sex differences in vocal communication of freely interacting adult mice depend upon behavioral context. PLoS One. 2018;13:e0204527.

Heckman JJ, Proville R, Heckman GJ, Azarfar A, Celikel T, Englitz B. High-precision spatial localization of mouse vocalizations during social interaction. Sci Rep. 2017;7:3017.

White NR, Prasad M, Barfield RJ, Nyby JG. 40- and 70-kHz vocalizations of mice (Mus musculus) during copulation. Physiol Behav. 1998;63:467–73.

Penn DJ, Frommen JG. Kin recognition: an overview of conceptual issues, mechanisms and evolutionary theory. In: Kappeler P, editor. Animal Behavior: Evolution and Mechanisms. Springer: Berlin Heidelberg; 2010. p. 55–85.

Winn BE, Vestal BM. Kin recognition and choice of males by wild female house mice (Mus musculus). J Comp Psychol. 1986;100:72–5.

Zinck L, Lima SQ. Mate Choice in Mus musculus Is Relative and Dependent on the Estrous State. PLoS One. 2013;8:e66064-e.

Suzuki H, Togashi M, Moriguchi Y, Adachi J. Relationship between age-related decline in fertility and In Vitro fertilization rate in IVCS mice. J Reprod Develop. 1994;40:107–16.

Hoffmann F, Musolf K, Penn DJ. Spectrographic analyses reveal signals of individuality and kinship in the ultrasonic courtship vocalizations of wild house mice. Physiol Behav. 2012;105:766–71.

Pomerantz SM, Nunez AA, Bean NJ. Female behavior is affected by male ultrasonic vocalizations in house mice. Physiol Behav. 1983;31:91–6.

Byers SL, Wiles MV, Dunn SL, Taft RA. Mouse estrous cycle identification tool and images. PLoS One. 2012;7:e35538.

Zala SM, Reitschmidt D, Noll A, Balazs P, Penn DJ. Automatic mouse ultrasound detector (A-MUD): a new tool for processing rodent vocalizations. PLoS One. 2017;12:e0181200.

Scattoni ML, Gandhy SU, Ricceri L, Crawley JN. Unusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism. PLoS One. 2008;3:e3067.

Scattoni ML, Ricceri L, Crawley JN. Unusual repertoire of vocalizations in adult BTBR T+tf/J mice during three types of social encounters. Genes Brain Behav. 2011;10:44–56.

Grimsley JMS, Sheth S, Vallabh N, Grimsley CA, Bhattal J, Latsko M, Jasnow A, Wenstrup JJ. Contextual modulation of vocal behavior in mouse: newly identified 12 kHz "mid-frequency" vocalization emitted during restraint. Front Behav Neurosci. 2016;10:38.

R Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2018. [http://www.R-project.org/].

Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, et al: vegan: Community Ecology Package; R package version 2.5–2; 2018. [http://CRAN.R-project.org/package=vegan].

Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecology. 2001;26:32–46.

Anderson MJ. Permutational Multivariate Analysis of Variance (PERMANOVA). In: Balakrishnan N, Colton T, Everitt B, Piegorsch W, Ruggeri F, Teugels JL, editors. Wiley StatsRef: Statistics Reference Online; 2017. p. 1–15. 1–15.

Clarke KR, Warwick RM. Change in marine communities: an approach to statistical analysis and interpretation. 2nd ed. Plymouth: Primer-E Ltd.; 2001.