Animal Science and Zoology; Ecology, Evolution, Behavior and Systematics
Abstract :
[en] Abstract
During courtship, prezygotic barriers are thought to maintain the diversity of species since differences in phenotypic traits and reproductive behaviours are likely to be involved in maintaining species boundaries. However, introgressive hybridization has been reported in many different taxa and the resulting hybrids usually possess phenotypic features, including behaviours, that are intermediate between those of the parents. The outcome of hybrids may depend on the interactions between the intrinsic viability of the hybrids, the ecological environment of the species, and the fitness of hybrids in that ecological context. In cichlids, the mechanism of hybridization is increasingly documented as an important factor in their evolutionary radiation since it may provide novel gene combinations that promote speciation and adaptive radiation by generating new transgressive phenotypes. Cichlid species are separated mostly by pre-mating isolating mechanisms. Like colour patterns, acoustic communication is involved in sexual selection, but this pattern has been much less studied and the outcome of hybridization on acoustic features has never been examined. To gain novel insights into the evolution of their acoustic communication behaviour, we performed a hybrid cross between Chindongo saulosi and Maylandia estherae. Qualitative examination of courtship showed that the three groups possess the same sequence of behaviours. However, sounds produced during courtship showed specific signatures since all three groups differ at the level of sound duration and pulse period, with both features being intermediate in hybrids in comparison to the two parent species. Colour patterns in hybrids were also different from those of the parent species. These results show that hybridization can affect at least two kinds of prezygotic barriers, which may be important in the cichlid evolutionary process. However, playback experiments are required to test the strength of these features in sexual selection.
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège
Disciplines :
Zoology
Author, co-author :
Parmentier, Eric ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Raick, Xavier ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS)
Leblanc, Nicolas; Laboratory of Functional and Evolutionary Morphology, FOCUS, University of Liège, Institut de Chimie - B6C, Sart Tilman , 4000 Liège , Belgium
Santoni-Guichard, Ghjuvan; Laboratory of Functional and Evolutionary Morphology, FOCUS, University of Liège, Institut de Chimie - B6C, Sart Tilman , 4000 Liège , Belgium
Banse, Marine ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS)
Da, Sié Jean de Dieu; Laboratory of Functional and Evolutionary Morphology, FOCUS, University of Liège, Institut de Chimie - B6C, Sart Tilman , 4000 Liège , Belgium
Van Damme, Arthur ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS)
Language :
English
Title :
Acoustic innovations in courtship sounds generated by hybridization in cichlid fish
This study was supported by a grant from the University of Liège (FOCUS) and by a grant from the F.R.S.-FNRS (T.0192.20–PDR).
Abbott R, Albach D, Ansell S et al. Hybridization and speciation. Journal of Evolutionary Biology 2013;26:229–46.
Akian DD, Yao K, Parmentier E et al. Acoustic signals produced by Nile tilapia Oreochromis niloticus and black-chinned tilapia Sarotherodon melanotheron during intra- and interspecific pairings. Zoology (Jena, Germany)2020;143:125831.
Amorim MCP. Diversity of sound production in fish. Diversity 2006;1:71–105.
Amorim MCP, Almada VC. The outcome of male-male encounters affects subsequent sound production during courtship in the cichlid fish Oreochromis mossambicus. Animal Behaviour 2005;69:595–601.
Amorim MCP, Knight ME, Stratoudakis Y et al. Differences in sounds made by courting males of three closely related Lake Malawi cichlid species. Journal of Fish Biology 2004;65:1358–71.
Amorim MCP, Simões JM, Fonseca PJ et al. Species differences in courtship acoustic signals among five Lake Malawi cichlid species (Pseudotropheus spp.). Journal of Fish Biology 2008;72:1355–68.
Amorim MCP, Vasconcelos RO, Fonseca PJ. 2015. Fish sounds and mate choice. In: Ladich F (ed.), Sound Communication in Fishes. Vienna: Springer Vienna, 1–33.
Amorim MCP, Fonseca PJ, Mathevon N et al. Assessment of fighting ability in the vocal cichlid Metriaclima zebra in face of incongruent audiovisual information. Biology Open 2019;8:bio043356.
Barton NH. The role of hybridization in evolution. Molecular Ecology 2001;10:551–68.
Bertucci F, Beauchaud M, Attia J et al. Sounds modulate males’ aggressiveness in a cichlid fish. Ethology 2010;116:1179–88.
Bertucci F, Attia J, Beauchaud M et al. Sounds produced by the cichlid fish Metriaclima zebra allow reliable estimation of size and provide information on individual identity. Journal of Fish Biology 2012;80:752–66.
Burke JM, Arnold ML. Genetics and the fitness of hybrids. Annual Review of Genetics 2001;35:31–52.
Connaughton MA, Taylor MH, Fine ML. Effects of fish size and temperature on weakfish disturbance calls: Implications for the mechanism of sound generation. Journal of Experimental Biology 2000;203:1503–1512.
Couldridge VCK, Alexander GJ. Color patterns and species recognition in four closely related species of Lake Malawi cichlid. Behavioral Ecology 2002;13:59–64.
Doherty JA, Gerhardt HC. Acoustic communication in hybrid treefrogs: sound production by males and selective phonotaxis by females. Journal of Comparative Physiology A 1984;154:319–30.
Dussenne M, Delcourt J, Poncin P et al. Impact of temperature-induced sex reversal on behavior and sound production in Nile tilapia (Oreochromis niloticus). . Hormones and Behavior 2022;142:105173.
Fitzpatrick BM. Rates of evolution of hybrid inviability in birds and mammals. Evolution 2004;58:1865–70.
Genner MJ, Turner GF. Ancient hybridization and phenotypic novelty within Lake Malawi’s cichlid fish radiation. Molecular Biology and Evolution2012;29:195–206.
Gerhardt HC, Guttman S, Karlin AA. Natural hybrids between Hyla cinerea and Hyla gratiosa: morphology, vocalization and electrophoretic analysis. Copeia 1980;1980:577–84.
Gerlai R. Mate choice and hybridization in Lake Malawi cichlids, SciaenochromisfryeriandCynotilapiaafra.Ethology2007;113:673–85.
Gerwin J, Urban S, Meyer A et al. Of bars and stripes: a Malawi cichlid hybrid cross provides insights into genetic modularity and evolution of modifier loci underlying colour pattern diversification. Molecular Ecology 2021;30:4789–803.
Grant PR, Grant RB. Hybridization of bird species. Science 1992;256:193–7.
Kagawa K, Takimoto G. Hybridization can promote adaptive radiation by means of transgressive segregation. Ecology Letters 2018;21:264–74.
Keller I, Wagner CE, Greuter L et al. Population genomic signatures of divergent adaptation, gene flow and hybrid speciation in the rapid radiation of Lake Victoria cichlid fishes. Molecular Ecology 2013;22:2848–63.
Kéver L, Parmentier E, Derycke S et al. Limited possibilities for prezygotic barriers in the reproductive behaviour of sympatric Ophthalmotilapia species (Teleostei, Cichlidae). Zoology 2018;126:71–81.
Kocher TD. Adaptive evolution and explosive speciation: the cichlid fish model. Nature Reviews. Genetics 2004;5:288–98.
Kornfield I, Smith PF. African cichlid fishes: model systems for evolutionary biology. Annual Review of Ecology and Systematics 2000;31:163–96.
Ladich F. 2015. Acoustic signalling in female fish. In: Ladich F (ed.), Sound Communication in Fishes. Vienna: Springer Vienna, 149–173.
Lobel PS. Acoustic behaviour of cichlid fishes. Journal of Aquariculture & Aquatic Sciences 2001;9:167–86.
Longrie N, Fine ML, Parmentier E. Innate sound production in the cichlid Oreochromis niloticus. Journal of Zoology 2008;275:413–7.
Longrie N, Van Wassenbergh S, Vandewalle P et al. Potential mechanism of sound production in Oreochromis niloticus (Cichlidae). The Journal of Experimental Biology 2009;212:3395–402.
Longrie N, Poncin P, Denoël M et al. Behaviours associated with acoustic communication in Nile Tilapia (Oreochromis niloticus). PLoS One 2013;8:e61467.
Looby A, Cox K, Bravo S et al. A quantitative inventory of global soniferous fish diversity. Reviews in Fish Biology and Fisheries 2022;32:581–95.
Maan ME, Sefc KM. Colour variation in cichlid fish: developmental mechanisms, selective pressures and evolutionary consequences. SeminarsinCell & DevelopmentalBiology2013;24:516–28.
Mallet J. Hybrid speciation. Nature 2007;446:279–83.
Maruska KP, Boyle KS, Dewan LR et al. Sound production and spectral hearing sensitivity in the Hawaiian sergeant damselfish, Abudefduf abdominalis. The Journal of Experimental Biology 2007;210:3990–4004.
Maruska KP, Ung US, Fernald RD. The African cichlid fish Astatotilapia burtoniuses acoustic communication for reproduction: Sound production,hearing,andbehavioralsignificance.PLoSOne2012;7:e37612–13.
McElroy DM, Kornfield I. Sexual selection, reproductive behavior, and speciation in the mbuna species flock of Lake Malawi (Pisces, Cichlidae). Environmental Biology of Fishes 1990;28:273–84.
Myrberg AA, Ha SJ, Shamblott MJ. The sounds of bicolor damselfish (Pomacentrus partitus): Predictors of body size and a spectral basis for individual recognition and assessment. Journal of the Acoustical Society of America 1993;94:3067–70. https://doi.org/10.1121/1.407267.
Myrberg AAJ, Kramer E, Heinecke P. Sound production by cichlid fishes. Science 1965;149:555–8.
Parmentier E, Fine ML. 2016. Fish sound production: Insights. In Suthers RA, Tecumseh F, Fay RR, Popper AN (eds.), Vertebrate Sound Production and Acoustic Communication. Springer Handbook of Auditory Research book series (SHAR), Vol. 53. Switzerland: Springer, Cham, 19–46.
Panhuis TM, Butlin R, Zuk M et al. Sexual selection and speciation. TrendsinEcology & Evolution2001;16:364–71.
Raick X, Huby A, Kurchevski G et al. Yellow-eyed piranhas produce louder sounds than red-eyed piranhas in an invasive population of Serrasalmus marginatus. Journal of Fish Biology 2020;97(6):1676–80.
Raick X, Rountree R, Kurchevski G etal. Acoustic homogeneity in the piranha Serrasalmusmaculatus. JournalofFishBiology2021;98:1303–07.
Rüber L, Meyer A, Sturmbauer C et al. Population structure in two sympatric species of the Lake Tanganyika cichlid tribe Eretmodini: evidence for introgression. Molecular Ecology 2001;10:1207–25.
Seehausen O. Hybridization and adaptive radiation. Trends in Ecology & Evolution 2004;19:198–207.
Seehausen O, van Alphen JJM. The effect of male coloration on female mate choice in closely related lake victoria cichlids (Haplochromis nyererei complex). Behavioral Ecology and Sociobiology 1998;42:1–8.
Seehausen O, Mayhew PJ, Van Alphen JJM. Evolution of color patterns in East African cichlid fish. Journal of Evolutionary Biology 1999;12:514–34.
Selz OM, Seehausen O. Interspecific hybridization can generate functional novelty in cichlid fish. Proceedings of the Royal Society B: BiologicalSciences2019;286:20191621.
Simões JM, Duarte IG, Fonseca PJ et al. Acoustic behaviour in Malawian Cichlids (Pseudotropheus, Cichlidae): Potential cues for species recognition and intraspecific communication. Razprave IV razreda SAZU, Advances in Bioacoustics II 2006;47:229–36.
Smith GR. Analysis of several hybrid cyprinid fishes from Western North America. Copeia 1973;1973:395–410.
Smith AR, van Staaden MJ. The association of visual and acoustic courtship behaviors in African cichlid fishes. Marine and Freshwater BehaviourandPhysiology2009;42:211–6.
Stelkens RB, Schmid C, Seehausen O. Hybrid breakdown in cichlid fish. PLoS One 2015;10:e0127207.
Tea YK, Hobbs JPA, Vitelli F et al. Angels in disguise: sympatric hybridization in the marine angelfishes is widespread and occurs between deeply divergent lineages. Proceedings of the Royal Society B: Biological Sciences 2020;287:20201459.
Venesky MD, Andraso GM, Ropski SJ. Behavior of male Kenyi cichlids, Pseudotropheus lombardoi, in response to visual and olfactory cues from females. Bios 2005;76:77–83.
Verzijden MN, Van Heusden J, Bouton N et al. Sounds of male Lake Victoria cichlids vary within and between species and affect female mate preferences. Behavioral Ecology 2010;21:548–55.
Weisel GF. The osteology of Mylocheilus caurinum × Ptychocheilus oregonense, a cyprinid hybrid, compared with its parental species forty-seven figures. Journal of Morphology 1955;96:333–57.
