Species recognition; mate choice; behaviour; Lake Tanganyika
Abstract :
[en] Cichlid radiations often harbour closely related species with overlapping niches and distribution ranges. Such species sometimes hybridise in nature, which raises the question how they can coexist. This also holds for the Tanganyika mouthbrooders Ophthalmotilapia ventralis and O. nasuta. Earlier studies found indications of asymmetrical hybridisation with females of O. ventralis accepting males of O. nasuta, but not the other way around. We hypothesised that this was due to differences in the capacity for species recognition. Given the higher propensity of O. ventralis females towards hybridisation, we expect a reduced ability for species recognition in O. ventralis females, compared to O. nasuta females. We staged two experiments, one focusing on 22 female O. nasuta and one on 21 female O. ventralis. These fish were placed in one half of a tank and briefly exposed to a conspecific or a heterospecific male, a conspecific female, or nothing (control). Female response was evaluated by scoring six tracking parameters and by noting the occurrence of ten discrete behaviours before and during the encounter. Females always responded to the presence of another fish by approaching it. Remarkably, for both O. nasuta and O. ventralis, we did not find a different response between encounters with conspecific males and females. However, in agreement with our hypothesis, females of O. nasuta behaved differently towards conspecific or heterospecific males, whereas females of O. ventralis did not. When presented with a heterospecific male, females of O. nasuta performed a lower number of ‘ram’ behaviours. Additionally, they never displayed the ‘flee’ behaviour, a component of the species’ mating repertoire that was seen in all but one of the presentations with a conspecific male. Our findings show that differences in species recognition at first encounter predict to a large degree the outcome of the mating process, even in the absence of mating behaviour.
Research center :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège
Disciplines :
Zoology
Author, co-author :
Van Steenberge, Maarten
Jublier, Noémie ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive
Kever, Loïc ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS)
Gresham, Sophie
Derycke, Sophie
Snoeks, Jos
Parmentier, Eric ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS)
Poncin, Pascal ; Université de Liège - ULiège > > Station scientifique des Hautes-Fagnes
Verheyen, Erik
Language :
English
Title :
The initial response of females towards congeneric males matches the propensity to hybridise in Ophthalmotilapia
Publication date :
13 April 2022
Journal title :
Belgian Journal of Zoology
ISSN :
0777-6276
eISSN :
2295-0451
Publisher :
Royal Belgian Institute of Natural Sciences (RBINS)
Amorim M.C.P., Knight M.E., Stratoudakis Y. & Turner G.F. (2004). Differences in sounds made by courting males of three closely related Lake Malawi cichlids. Journal of Fishery Biology 65 (5): 1358–1371. https://doi.org/10.1111/j.0022-1112.2004.00535.x
Anderson M.J. (2006). Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62 (1): 245–253. https://doi.org/10.1111/j.1541-0420.2005.00440.x
Arnold S.J., Verrell P.A. & Tilley S.G. (1996). The evolution of asymmetry in sexual isolation: A model and a test case. Evolution 50: 1024–1033. https://doi.org/10.1111/j.1558-5646.1996.tb02343.x
Baerends G.P. & Baerends-Van Roon J.M. (1950). An Introduction to the Study of the Ethology of the Cichlid Fishes. E.J. Brill, Leiden, The Netherlands.
Barlow G.W. (2002). How behavioural studies contribute to the species problem: a piscine perspective. Fish and Fisheries 3 (3): 197–212. https://doi.org/10.1046/j.1467-2979.2002.00083.x
Blais J., Plenderleith M., Rico C., Taylor M.I., Seehausen O., Van Oosterhout C. & Turner G.F. (2009). Assortative mating among Lake Malawi cichlid fish populations is not simply predictable from male nuptial colour. BMC Ecology and Evolution 9: article 53. https://doi.org/10.1186/1471-2148-9-53
Crapon De Caprona M.D. & Ryan M.J. (1990). Conspecific mate recognition in swordtails, Xiphophorus nigrensis and X. pygmaeus (Poeciliidae): olfactory and visual cues. Animal Behaviour 39 (2): 290–296. https://doi.org/10.1016/S0003-3472(05)80873-5
Danley P.D. & Kocher T.D. (2001). Speciation in rapidly diverging systems: lessons from Lake Malawi. Molecular Ecology 10: 1075–1086. https://doi.org/10.1046/j.1365-294X.2001.01283.x
Decaestecker E. (2022). Experimental evidence for asymmetrical species recognition in East African Ophthalmotilapia cichlids. Peer Community in Zoology 100010. https://doi.org/10.24072/pci.zool.100010
Egger B., Obermüller B., Eigner E., Sturmbauer C. & Sefc K.M. (2008). Assortative mating preferences between colour morphs of the endemic Lake Tanganyika cichlid genus Tropheus. Hydrobiologia. 615: 37–48. https://doi.org/10.1007/978-1-4020-9582-5_3
Friard O. & Gamba M. (2016). BORIS: A Free, Versatile open-source event-logging software for video / audio coding and live observations. Methods in Ecology and Evolution 7 (11): 1–6. https://doi.org/10.1111/2041-210X.12584
Gonzalez-Voyer A., Fitzpatrick J.L. & Kolm N. (2008). Sexual selection determines parental care patterns in cichlid fishes. Evolution 62 (8): 2015–2026. https://doi.org/10.1111/j.1558-5646.2008.00426.x
Haesler M.P., Lindeyer C.M., Otti O., Bonfils D., Heg D. & Taborsky M. (2011). Female mouthbrooders in control of pre-and postmating sexual selection. Behavioral Ecology 22 (5): 1033– 1041. https://doi.org/10.1093/beheco/arr087
Hammer Ø., Harper D.A. & Ryan P.D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4 (1): 9 pp. Available from http://palaeo-electronica.org/2001_1/past/issue1_01.htm [accessed 24 March 2022].
Hanssens M., Snoeks J. &Verheyen E. (1999).Amorphometric revision of the genus Ophthalmotilapia (Teleostei, Cichlidae) from Lake Tanganyika (East Africa). Zoological Journal of the Linnean Society 125 (4): 487–512. https://doi.org/10.1111/j.1096-3642.1999.tb00602.x
Ho J., Tumkaya T., Aryal S., Choi H. & Claridge-Chang. A (2019). Moving beyond P values: data analysis with estimation graphics. Nature Methods 16 (7): 565–566. https://doi.org/10.1038/s41592-019-0470-3
Hohenlohe P.A. &Arnold S.J. (2010). Dimensionality of mate choice, sexual isolation, and speciation. Proceedings of the National Academy of Sciences 107 (38): 16583–16588. https://doi.org/10.1073/pnas.1003537107
Immler S. & Taborsky M. (2009). Sequential polyandry affords post-mating sexual selection in the mouths of cichlid females. Behavioral Ecology and Sociobiology 63 (8): 1219–1230. https://doi.org/10.1007/s00265-009-0744-3
Jiggins C.D., Salazar C., Linares M. & Mavarez J. (2008). Hybrid trait speciation and Heliconius butterflies. Philosophical Transactions of the Royal Society B. 363 (1506): 3047–3054. https://doi.org/10.1098/rstb.2008.0065
Jordan R., Kellogg K., Juanes F. & Stauffer J. (2003). Evaluation of female mate choice cues in a group of Lake Malawi mbuna (Cichlidae). Copeia 2003 (1): 181–186. https://doi.org/b7gv39
Kéver L., Parmentier E., Derycke S., Verheyen E., Snoeks J., Van Steenberge M. & PONCIN P. (2018). Limited possibilities for prezygotic barriers in the reproductive behaviour of sympatric Ophthalmotilapia species (Teleostei, Cichlidae). Zoology 126: 71–81. https://doi.org/10.1016/j.zool.2017.12.001
Kidd M.R., Danley P.D. & Kocher T.D. (2006). Adirect assay of female choice in cichlids: all the eggs in one basket. Journal of Fish Biology 68 (2): 373–384. https://doi.org/10.1111/j.0022-1112.2006.00896.x
Koblmüller S., Duftner N., Sefc K.M., Aibara M., Stipacek M., Blanc M., Egger B. & Sturmbauer C. (2007). Reticulate phylogeny of gastropod-shell-breeding cichlids from Lake Tanganyika-the result of repeated introgressive hybridisation. BMC Ecology and Evolution 7: article number 7. https://doi.org/10.1186/1471-2148-7-7
Kocher T.D. (2004). Adaptive evolution and explosive speciation: the cichlid fish model. Nature Reviews Genetics 5 (4): 288–298. https://doi.org/10.1038/nrg1316
Konings A. (2019). Tanganyika Cichlids in their Natural Habitat. 4th edition. Cichlid Press, El Paso, TX.
Kozak G.M. & Boughman J.W. (2009). Learned conspecific mate preference in a species pair of sticklebacks. Behavioral Ecology 20: 1282–1288. https://doi.org/10.1093/beheco/arp134
Kozak G.M., Reisland M. & Boughmann J.W. (2009). Sex differences in mate recognition and conspecific preference in species with mutual mate choice. Evolution 63: 353–365. https://doi.org/10.1111/j.1558-5646.2008.00564.x
Luttbeg B., Towner M.C., Wandesforde-Smith A., Mangel M. & Foster S.A. (2001). State-dependent mate-assessment and mate-selection behavior in female threespine sticklebacks (Gasterosteus aculeatus, Gasterosteiformes: Gasterosteidae). Ethology 107 (6): 545–558. https://doi.org/10.1046/j.1439-0310.2001.00694.x
Mayr E. (1982). The Growth of Biological Thought: Diversity, Evolution and Inheritance. Harvard University Belknap Press, Cambridge, MA.
Marques D.A., Meier J.I. & Seehausen O. (2019). A combinatorial view on speciation and adaptive radiation. Trends in Ecology and Evolution 34 (6): 531–544. https://doi.org/10.1016/j.tree.2019.02.008
Mcelroy D.M. & Kornfeld I. (1990). Sexual selection, reproductive behaviour, and speciation in the mbuna species fock of Lake Malawi (Pisces: Cichlidae). Environmental Biology of Fishes 28: 273–284. https://doi.org/10.1007/bf00751041
Mendelson T.C. & Shaw K.L. (2012). The (mis)concept of species recognition. Trends in Ecology and Evolution 27 (8): 421–427. https://doi.org/10.1016/j.tree.2012.04.001
Moran M.D. (2003). Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100 (2): 403–405. https://doi.org/10.1034/j.1600-0706.2003.12010.x
Morita M., Awata S., Yorifuji M., Ota K., Kohda M. & Ochi H. (2014). Bower-building behaviour is associated with increased sperm longevity in Tanganyikan cichlids. Journal of Evolutionary Biology 27 (12): 2629–2643. https://doi.org/10.1111/jeb.12522
Naish K.A. & Ribbink A.J. (1990). A preliminary investigation of sex change in Pseudotropheus lombardoi (Pisces: Cichlidae). Environmental Biology of Fishes 28: 285–294. https://doi.org/10.1007/978-94-009-2065-1_18
Nakagawa S. (2004). A farewell to Bonferroni: the problem of low statistical power and publication bias. Behavioral. Ecology 15: 1044–1045. https://doi.org/10.1093/beheco/arh107
Nelissen M.H.J. (1978). Sound production by some Tanganyikan cichlid fishes and a hypothesis for the evolution of their communication mechanisms. Behaviour 64 (1–2): 137–147. https://doi.org/10.1163/156853978X00477
Nevado B., Fazalova V., Backeljau T., Hanssens M. & Verheyen E. (2011). Repeated unidirectional introgression of nuclear and mitochondrial DNA between four congeneric Tanganyikan cichlids. Molecular Biology and Evolution 28 (8): 2253–2267. https://doi.org/10.1093/molbev/msr043
Oksanen J.F., Blanchet G., Friendly M., Kindt R., Legendre P., Mcglinn D., Minchin P.R., O’hara R.B., Simpson G.L., Solymos P.M., Stevens H.H., Szoecs E. & Wagner H. (2017). Vegan: Community Ecology Package. R package version 2.4-5.
Oliveira R.F. (2012). Social plasticity in fish: integrating mechanisms and function. Journal of Fish Biology 81: 2127–2150. https://doi.org/10.1111/j.1095-8649.2012.03477.x
Panfili J., Thior D., Ecoutin J.-M., Ndiaye P. & ALBARET J.-J. (2006). Influence of salinity on the size at maturity for fish species reproducing in contrasting West African estuaries. Journal of Fish Biology 69 (1): 95–113. https://doi.org/10.1111/j.1095-8649.2006.01069.x
Peters H.M. (1975). Hermaphroditism in cichlid fishes. In: Reinboth R. (ed.) Intersexuality in the Animal Kingdom: 228–235. Springer-Verlag, Berlin. https://doi.org/10.1007/978-3-642-66069-6_22
Phelps S.M., Rand A.S. & Ryan M.J. (2006). A cognitive framework for mate choice and species recognition. The American Naturalist 167 (1): 28–42. https://doi.org/10.1086/498538
Plenderleith M., Van Oosterhout C., Robinson R.L. & Turner G.F. (2005). Female preference for conspecific males based on olfactory cues in a Lake Malawi cichlid fish. Biology Letters 1 (4): 411–414. https://doi.org/10.1098/rsbl.2005.0355
Poll M. (1986). Classification des cichlidae du Lac Tanganyika: Tribus, genres et espèces. Bulletin de l’Académie royale de la Belgique 8: 1–163.
R Core Team (2017). R: A Language and Environment for Statistical Computing. R foundation for statistical computing, Vienna, Austria.
Ronco F., Büscher H.H., Indermauer A. & Salzburger W. (2020). The taxonomic diversity of the cichlid fish fauna of ancient Lake Tanganyika, East Africa. Journal of Great Lakes Research 46: 1067–1078. https://doi.org/10.1016/j.jglr.2019.05.009
Roux C., Fraïsse C., Romiguier J., Anciaux Y., Galtier N. & Bierne N. (2016). Shedding light on the grey zone of speciation along a continuum of genomic divergence. PLoS Biology 14 (12): e2000234. https://doi.org/10.1371/journal.pbio.2000234
Rüber L., Meyer A., Sturmbauer C. & Verheyen E. (2001). Population structure in two sympatric species of the Lake Tanganyika cichlid tribe Eretmodini: evidence for introgression. Molecular Ecology 10 (5): 1207–1225. https://doi.org/10.1046/j.1365-294x.2001.01259.x
Salzburger W. (2018). Understanding explosive diversification through cichlid fish genomics. Nature Reviews Genetics 19: 705–717. https://doi.org/10.1038/s41576-018-0043-9
Salzburger W., Braasch I. & Meyer A. (2007). Adaptive sequence divergence in a colour gene involved in the formation of the characteristic egg-dummies of male Haplochromis cichlid fishes. BMC Biology 5: article number 51. https://doi.org/10.1186/1741-7007-5-51
Schneider C.A., Rasband W.S. & Eliceiri K.W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9 (7): 671–675. https://doi.org/10.1038/nmeth.2089
Seehausen O. (2004). Hybridisation and adaptive radiation. Trends in Ecology and Evolution 19 (4): 198–207. https://doi.org/10.1016/j.tree.2004.01.003
Seehausen O. & Van Alphen J.J.M. (1998). The effect of male coloration on female mate choice in closely related Lake Victoria cichlids (Haplochromis nyererei complex). Behavioral Ecology and Sociobiology 42: 1–8.
Seehausen O., Terai Y., Magalhaes I.S., Carleton K.L., Mrosso H.D.J., Miyagi R., Van Der Sluijs I., Schneider M.V., Maan M.E., Tachida H., Imai H. & Okada N. (2008). Speciation through sensory drive in cichlid fish. Nature 455: 620–626. https://doi.org/10.1038/nature07285
Sefc K.M., Mattersdorfer K., Ziegelbecker A., Neuhüttler N., Steiner O., Goessler W. & Koblmüller S. (2017). Shifting barriers and phenotypic diversification by hybridisation. Ecology Letters 20 (5): 651–662. https://doi.org/10.1111/ele.12766
Sommer-Trembo C., Plath M., Gismann J., Helfrich C. & Bierbach D. (2017). Context-dependent female mate choice maintains variation in male sexual activity. Royal Society Open Science 4: 170303. https://doi.org/10.1098/rsos.170303
Strecker U. & Kodric-Brown A. (1999). Mate recognition systems in a species flock of Mexican pupfish. Journal of Evolutionary Biology 12 (5): 927–935. https://doi.org/10.1046/j.1420-9101.1999.00096.x
Sturmbauer C., Fuchs C., Harb G., Damm E., Duftner N., Maderbacher M., Koch M. & Koblmüller S. (2008). Abundance, distribution, and territory areas of rock-dwelling Lake Tanganyika cichlid fish species. Hydrobiologia 615 (1): 57–68. https://doi.org/10.1007/978-1-4020-9582-5_5
Sullivan B.K. (2009). Mate recognition, species boundaries and the fallacy of “species recognition”. Open Zoology 2: 86–90. https://doi.org/10.2174/1874336601002009086
Svensson E.I., Karlsson K., Friberg M. & Eroukhmanoff F. (2007). Gender differences in species recognition and the evolution of asymmetric sexual isolation. Current Biology 17 (22): 1943–1947. https://doi.org/10.1016/j.cub.2007.09.038
Tinbergen N. (1948). Social releasers and the experimental method required for their study. Wilson Bulletin 60 (1): 6–51.
Theis A., Salzburger W. & Egger B. (2012). The function of anal fin egg-spots in the cichlid fish Astatotilapia burtoni. PLoS ONE 7 (1): e29878. https://doi.org/10.1371/journal.pone.0029878
Thomas G.H. & SzéKely T. (2005). Evolutionary pathways in shorebird breeding systems: sexual conflict, parental care, and chick development. Evolution 59 (10): 2222–2230. https://doi.org/10.1111/j.0014-3820.2005.tb00930.x
Trivers R.L. (1972). Parental investment and sexual selection. In: Campbell B (ed.) Sexual Selection and the Descent of Man 1871–1971: 136–179. Aldine Publishing Company, Chicago.
Turner G.F., Seehausen O., Knight M.E., Allender C.J. & Robinson R.L. (2001). How many species of cichlid fishes are there in African lakes. Molecular Ecology 10 (3): 793–806. https://doi.org/10.1046/j.1365-294x.2001.01200.x
Van Oppen M.J.H., Turner G.F., Rico C., Robinson R.L., Deutsch J.C., Genner M.J. & Hewitt G.M. (1998). Assortative mating among rock-dwelling cichlid fishes supports high estimates of species richness from Lake Malawi. Molecular Ecology 7 (8): 991–1001. https://doi.org/10.1046/j.1365-294x.1998.00417.x
Verrell P.A. (1990). Frequency of interspecific mating in salamanders of the plethodontid genus Desmognathus: different experimental designs may yield different results. Journal of Zoology 221 (3): 441–451. https://doi.org/10.1111/j.1469-7998.1990.tb04012.x
Verzijden M.N. & Ten Cate C. (2007). Early learning influences species assortative mating preferences in Lake Victoria cichlid fish. Biology letters 3 (2): 134–136. https://doi.org/10.1098/rsbl.2006.0601
Verzijden M.N., Korthof R.E.M. & Ten Cate C. (2008). Females learn from mothers and males learn from others. The effect of mother and siblings on the development of female mate preferences and male aggression biases in Lake Victoria cichlids, genus Mbipia. Behavioral Ecology and Sociobiology 62: 1359–1368. https://doi.org/10.1007/s00265-008-0564-x
Werner N.Y. & Lotem A. (2003). Choosy males in a haplochromine cichlid: first experimental evidence for male mate choice in a lekking species. Animal Behaviour 66 (2): 293–298. https://doi.org/10.1006/anbe.2003.2208
Wirtz P. (1999). Mother species-father species: unidirectional hybridization in animals with female choice. Animal Behaviour 58: 1–12. https://doi.org/10.1006/anbe.1999.1144
Wong B.M.B. & Jennions M.D. (2003). Costs influence male mate choice in a freshwater fish. Proceedings of the Royal Society, B-Biological Sciences 270 (Suppl. 1): S36–S38. https://doi.org/10.1098/rsbl.2003.0003
Zoppoth P., Koblmüller S. & Sefc K.M. (2013). Male courtship preferences demonstrate discrimination against allopatric colour morphs in a cichlid fish. Journal of Evolutionary Biology 26 (3): 577–586. https://doi.org/10.1111/jeb.12074
