This paper is published by Wiley: see doi link hereabove to access the final published version. The links hereunder give access to the open access version.
All documents in ORBi are protected by a user license.
assortative mating; explosive breeder; fecundity; mate choice; sexual selection; Ceratophrys stolzmanni; aridity; amphibian; horned frog; body condition; age structure; skeletochronology; SSD; sexual size dimorphism; clutch size
Abstract :
[en] Sexual selection theory predicts that, when body size is correlated with fecundity, there should be fitness advantages for mate choice of the largest females. Moreover, because larger males are expected to monopolize the largest females, this should result in an assortative mating based on body size. Although such patterns could be expected in both explosive and prolonged breeders, non-assortative mating should be more widespread in species under time constraints. However, patterns of sexual selection are largely unexplored in explosive breeding species, and contrasting patterns have been found previously. We expect that the active choice of partners may be particularly risky when the time period during which sexual partners are available is severely limited. Therefore, to avoid missing an entire reproductive act, males and females should pair irrespective of traits, such as body size. We tested this hypothesis by investigating the mating patterns of the Pacific horned toad, Ceratophrys stolzmanni, a short-lived fossorial species inhabiting Neotropical dry forests. This species is particularly adequate to test our prediction because it reproduces explosively over the course of a single night per year. Although the number of eggs laid was proportional to the size of females, and individuals of both sexes showed variation in body size, there was no assortative mating based either on size, body condition or age of mates. Egg size was not influenced by either female size or clutch size. The larger body size of females compared to males is likely due to fecundity selection, i.e. the selective pressure that enhances reproductive output. Although we cannot dismiss the possibility that individuals could select their partners based on other criteria than those related to size or age, the results fit well our prediction, showing that the explosive breeding makes improbable an active choice of partners in both sexes and therefore favours a random mating pattern.
Research center :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Székely, Paul; Universidad Técnica Particular de Loja > Departamento de Ciencias Biológicas
Denoël, Mathieu ✱; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
Cogălniceanu, Dan ✱; Ovidius University Constanța > Faculty of Natural and Agricultural Sciences
✱ These authors have contributed equally to this work.
Language :
English
Title :
Random size-assortative mating despite size-dependent fecundity in a Neotropical amphibian with explosive reproduction
Publication date :
April 2018
Journal title :
Ethology
ISSN :
0179-1613
eISSN :
1439-0310
Publisher :
Blackwell Publishing, Berlin, Germany
Volume :
124
Issue :
4
Pages :
218-226
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE] WBI - Wallonie-Bruxelles International [BE] Romanian National Authority for Scientific Research and Innovation (ANCS) SENESCYT - Secretaría de Educación Superior Ciencia Tecnología e Innovación [EC]
Ah-King, M., & Gowaty, P. A. (2016). A conceptual review of mate choice: Stochastic demography, within-sex phenotypic plasticity, and individual flexibility. Ecology and Evolution, 6, 4607–4642. https://doi.org/10.1002/ece3.2197
Arak, A. (1983). Male-male competition and mate choice in anuran amphibians. In P. Bateson (Ed.), Mate choice (pp. 181–210). Cambridge, UK: Cambridge University Press.
Băncilă, R. I., Hartel, T., Plăiaşu, R., Smets, J., & Cogălniceanu, D. (2010). Comparing three body condition indices in amphibians: A case study of yellow-bellied toad Bombina variegata. Amphibia-Reptilia, 31, 558–562. https://doi.org/10.1163/017353710x518405
Bastos, R. P., & Haddad, C. F. (1996). Breeding activity of the neotropical treefrog Hyla elegans (Anura, Hylidae). Journal of Herpetology, 30, 355–360. https://doi.org/10.2307/1565172
Berven, K. A., & Chadra, B. G. (1988). The relationship among egg size, density and food level on larval development in the wood frog (Rana sylvatica). Oecologia, 75, 67–72. https://doi.org/10.1007/BF00378815
Böll, S., & Linsenmair, K. E. (1998). Size-dependent male reproductive success and size-assortative mating in the midwife toad Alytes obstetricans. Amphibia-Reptilia, 19, 75–89. https://doi.org/10.1163/156853898X00340
Bowcock, H., Brown, G., & Shine, R. (2013). Sexual selection in cane toads Rhinella marina: A male's body size affects his success and his tactics. Current Zoology, 59, 747–753. https://doi.org/10.1093/czoolo/59.6.747
Brockmann, H. J. (1990). Mating behavior of horseshoe crabs, Limulus polyphemus. Behaviour, 114, 206–220. https://doi.org/10.1163/156853990X00121
Bush, S. L., Dyson, M. L., & Halliday, T. R. (1996). Selective phonotaxis by males in the Majorcan midwife toad. Proceedings of the Royal Society of London Series B: Biological Sciences, 263, 913–917. https://doi.org/10.1098/rspb.1996.0135
Castanet, J., & Smirina, E. (1990). Introduction to the skeletochronological method in amphibians and reptiles. Annales des Sciences Naturelles - Zoologie et Biologie Animale, 11, 191–196.
Castellano, S. (2009). Unreliable preferences, reliable choice and sexual selection in leks. Animal Behaviour, 77, 225–232. https://doi.org/10.1016/j.anbehav.2008.09.017
Castellano, S., & Cermelli, P. (2011). Sampling and assessment accuracy in mate choice: A random-walk model of information processing in mating decision. Journal of Theoretical Biology, 274, 161–169. https://doi.org/10.1016/j.jtbi.2011.01.001
Chajma, P., & Vojar, J. (2016). The effect of size-assortative mating on fertilization success of the common toad (Bufo bufo). Amphibia-Reptilia, 37, 389–395. https://doi.org/10.1163/15685381-00003069
Cogălniceanu, D., Székely, P., Székely, D., Roşioru, D., Băncilă, R. I., & Miaud, C. (2013). When males are larger than females in ectotherms: Reproductive investment in the eastern spadefoot toad Pelobates syriacus. Copeia, 2013, 699–706. https://doi.org/10.1643/ce-12-053
Colleoni, E., Denoël, M., Padoa-Schioppa, E., Scali, S., & Ficetola, G. F. (2014). Rensch's rule and sexual dimorphism in salamanders: Patterns and potential processes. Journal of Zoology, London, 293, 143–151. https://doi.org/10.1111/jzo.12137
Cunningham, C. J., Courage, M. G., & Quinn, T. P. (2013). Selecting for the phenotypic optimum: Size-related trade-offs between mortality risk and reproductive output in female sockeye salmon. Functional Ecology, 27, 1233–1243. https://doi.org/10.1111/1365-2435.12112
Dechaume-Moncharmont, F.-X., Brom, T., & Cézilly, F. (2016). Opportunity costs resulting from scramble competition within the choosy sex severely impair mate choosiness. Animal Behaviour, 114, 249–260. https://doi.org/10.1016/j.anbehav.2016.02.019
Denoël, M., Hervant, F., Schabetsberger, R., & Joly, P. (2002). Short- and long term advantages of an alternative ontogenetic pathway. Biological Journal of the Linnean Society, 77, 105–112. https://doi.org/10.1046/j.1095-8312.2002.00095.x
Duellman, W. E., & Lizana, M. (1994). Biology of a sit-and-wait predator, the leptodactylid frog Ceratophrys cornuta. Herpetologica, 50, 51–64.
Duellman, W. E., & Trueb, L. (1994). Biology of amphibians. Baltimore, MD: Johns Hopkins University Press.
Dziminski, M. A., & Alford, R. A. (2005). Patterns and fitness consequences of intraclutch variation in egg provisioning in tropical Australian frogs. Oecologia, 146, 98–109. https://doi.org/10.1007/s00442-005-0177-2
Edward, D. A. (2015). The description of mate choice. Behavioral Ecology, 26, 301–310. https://doi.org/10.1093/beheco/aru142
Elmberg, J. (1987). Random mating in a boreal population of European common frogs Rana temporaria. Ecography, 10, 193–195. https://doi.org/10.1111/j.1600-0587.1987.tb00758.x
Felton, A., Alford, R. A., Felton, A., & Schwarzkopf, L. (2006). Multiple mate choice criteria and the importance of age for male mating success in the microhylid frog, Cophixalus ornatus. Behavioral Ecology and Sociobiology, 59, 786–795. https://doi.org/10.1007/s00265-005-0124-6
Ficetola, G. F., & De Bernardi, F. (2009). Offspring size and survival in the frog Rana latastei: From among-population to within-clutch variation. Biological Journal of the Linnean Society, 97, 845–853. https://doi.org/10.1111/j.1095-8312.2009.01229.x
Gottsberger, B., & Gruber, E. (2004). Temporal partitioning of reproductive activity in a neotropical anuran community. Journal of Tropical Ecology, 20, 271–280. https://doi.org/10.1017/S0266467403001172
Greene, A. E., & Funk, W. C. (2009). Sexual selection on morphology in an explosive breeding amphibian, the columbia spotted frog (Rana luteiventris). Journal of Herpetology, 43, 244–251. https://doi.org/10.1670/08-112R.1
Han, X., & Fu, J. (2013). Does life history shape sexual size dimorphism in anurans? A comparative analysis. BMC Evolutionary Biology, 13, 27. https://doi.org/10.1186/1471-2148-13-27
Hartmann, M. T., Hartmann, P. A., & Haddad, C. F. B. (2010). Reproductive modes and fecundity of an assemblage of anuran amphibians in the Atlantic rainforest, Brazil. Iheringia. Série Zoologia, 100, 207–215. https://doi.org/10.1590/S0073-47212010000300004
Hase, K., & Shimada, M. (2014). Female polyandry and size-assortative mating in isolated local populations of the Japanese common toad Bufo japonicus. Biological Journal of the Linnean Society, 113, 236–242. https://doi.org/10.1111/bij.12339
Howard, R. D. (1978). The influence of male-defended oviposition sites on early embryo mortality in bullfrogs. Ecology, 59, 789–798. https://doi.org/10.2307/1938783
Howard, R. D., & Kluge, A. G. (1985). Proximate mechanisms of sexual selection in wood frogs. Evolution, 39, 260–277. https://doi.org/10.2307/2408361
Howard, R. D., Whiteman, H. H., & Schueller, T. I. (1994). Sexual selection in American toads: A test of a good-genes hypothesis. Evolution, 48, 1286–1300. https://doi.org/10.2307/2410386
Jakob, E. M., Marshall, S. D., & Uetz, G. W. (1996). Estimating fitness: A comparison of body condition indices. Oikos, 77, 61–67. https://doi.org/10.2307/3545585
Jorge, J., Sales, R., Kokubum, M., & Freire, E. (2015). On the natural history of the Caatinga horned frog, Ceratophrys joazeirensis (Anura: Ceratophryidae), a poorly known species of northeastern Brazil. Phyllomedusa, 14, 147–156. https://doi.org/10.11606/issn.2316-9079.v14i2p147-156
Knopp, T., & Merilä, J. (2009). Multiple paternity in the moor frog, Rana arvalis. Amphibia-Reptilia, 30, 515–521. https://doi.org/10.1163/156853809789647112
Kokko, H., Brooks, R., Jennions, M. D., & Morley, J. (2003). The evolution of mate choice and mating biases. Proceedings of the Royal Society of London Series B: Biological Sciences, 270, 653–664. https://doi.org/10.1098/rspb.2002.2235
Kokko, H., Jennions, M. D., & Brooks, R. (2006). Unifying and testing models of sexual selection. Annual Review of Ecology, Evolution, and Systematics, 37, 43–66. https://doi.org/10.1146/annurev.ecolsys.37.091305.110259
Liao, W. B., & Lu, X. (2009). Male mate choice in the Andrew's toad Bufo andrewsi: A preference for larger females. Journal of Ethology, 27, 413–417. https://doi.org/10.1007/s10164-008-0135-7
Lovich, J. E., & Gibbons, J. W. (1992). A review of techniques for quantifying sexual size dimorphism. Growth Development and Aging, 56, 269–281.
Lu, X., Chen, W., Zhang, L., & Ma, X. (2010). Mechanical constraint on size-assortative paring success in a temperate frog: An experimental approach. Behavioural Processes, 85, 181–184. https://doi.org/10.1016/j.beproc.2010.07.001
Lu, X., Ma, X., Li, Y., & Fan, L. (2009). Breeding behavior and mating system in relation to body size in Rana chensinensis, a temperate frog endemic to northern China. Journal of Ethology, 27, 391–400. https://doi.org/10.1007/s10164-008-0132-x
Mangold, A., Trenkwalder, K., Ringler, M., Hödl, W., & Ringler, E. (2015). Low reproductive skew despite high male-biased operational sex ratio in a glass frog with paternal care. BMC Evolutionary Biology, 15, 181. https://doi.org/10.1186/s12862-015-0469-z
Marco, A., Kiesecker, J. M., Chivers, D. P., & Blaustein, A. R. (1998). Sex recognition and mate choice by male western toads, Bufo boreas. Animal Behaviour, 55, 1631–1635. https://doi.org/10.1006/anbe.1997.0711
McCauley, S. J., Bouchard, S. S., Farina, B. J., Isvaran, K., Quader, S., Wood, D. W., & St. Mary, C. M. (2000). Energetic dynamics and anuran breeding phenology: Insights from a dynamic game. Behavioral Ecology, 11, 429–436. https://doi.org/10.1093/beheco/11.4.429
Meuche, I., Brusa, O., Linsenmair, K. E., Keller, A., & Pröhl, H. (2013). Only distance matters – non-choosy females in a poison frog population. Frontiers in Zoology, 10, 29. https://doi.org/10.1186/1742-9994-10-29
Monroe, M. J., South, S. H., & Alonzo, S. H. (2015). The evolution of fecundity is associated with female body size but not female-biased sexual size dimorphism among frogs. Journal of Evolutionary Biology, 28, 1793–1803. https://doi.org/10.1111/jeb.12695
Nali, R. C., Zamudio, K. R., Haddad, C. F. B., & Prado, C. P. A. (2014). Size-dependent selective mechanisms on males and females and the evolution of sexual size dimorphism in frogs. The American Naturalist, 184, 727–740. https://doi.org/10.1086/678455
Olive, P. J. W. (1992). The adaptive significance of seasonal reproduction in marine invertebrates: The importance of distinguishing between models. Invertebrate Reproduction & Development, 22, 165–174. https://doi.org/10.1080/07924259.1992.9672269
Olson, D. H., Blaustein, A. R., & O'Hara, R. K. (1986). Mating pattern variability among western toad (Bufo boreas) populations. Oecologia, 70, 351–356. https://doi.org/10.1007/BF00379496
Ortiz, D. A., Almeida-Reinoso, D., & Coloma, L. A. (2013). Notes on husbandry, reproduction and development in the Pacific horned frog Ceratophrys stolzmanni (Anura: Ceratophryidae), with comments on its amplexus. International Zoo Yearbook, 47, 151–162. https://doi.org/10.1111/j.1748-1090.2012.00193.x
Perry, G., Wallace, M. C., Perry, D., Curzer, H., & Muhlberger, P. (2011). Toe clipping of amphibians and reptiles: Science, ethics, and the law. Journal of Herpetology, 45, 547–555. https://doi.org/10.1670/11-037.1
Pfennig, K. S. (2000). Female spadefoot toads compromise on mate quality to ensure conspecific matings. Behavioral Ecology, 11, 220–227. https://doi.org/10.1093/beheco/11.2.220
Pianka, E. R. (1970). On r- and K-Selection. The American Naturalist, 104, 592–597.
Pincheira-Donoso, D., & Tregenza, T. (2011). Fecundity selection and the evolution of reproductive output and sex-specific body size in the Liolaemus lizard adaptive radiation. Evolutionary Biology, 38, 197–207. https://doi.org/10.1007/s11692-011-9118-7
Rausch, A. M., Sztatecsny, M., Jehle, R., Ringler, E., & Hödl, W. (2014). Male body size and parental relatedness but not nuptial colouration influence paternity success during scramble competition in Rana arvalis. Behaviour, 151, 1869–1884. https://doi.org/10.1163/1568539X-00003220
Reading, C. J. (2001). Non-random pairing with respect to past breeding experience in the common toad (Bufo bufo). Journal of Zoology, 255, 511–518. https://doi.org/10.1017/S0952836901001595
Reynolds, J. D., & Gross, M. R. (1990). Costs and benefits of female mate choice: Is there a lek paradox? The American Naturalist, 136, 230–243. https://doi.org/10.1086/285093
Rollinson, N., & Rowe, L. (2016). The positive correlation between maternal size and offspring size: Fitting pieces of a life-history puzzle. Biological Reviews, 91, 1134–1148. https://doi.org/10.1111/brv.12214
Ron, S. R., Guayasamin, J. M., Yanez-Muñoz, M. H., Merino-Viteri, A., Ortiz, D. A. & Nicolalde, D. A. (2016). AmphibiaWebEcuador. Museo de Zoología, Pontificia Universidad Católica del Ecuador. Retrieved from http://zoologia.puce.edu.ec/vertebrados/anfibios/FichaEspecie.aspx?Id=1216
Schalk, C. M., & Saenz, D. (2016). Environmental drivers of anuran calling phenology in a seasonal neotropical ecosystem. Austral Ecology, 41, 16–27. https://doi.org/10.1111/aec.12281
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671. https://doi.org/10.1038/nmeth.2089
Schwartz, J. J., Huth, K., & Hutchin, T. (2004). How long do females really listen? Assessment time for female mate choice in the grey treefrog, Hyla versicolor. Animal Behaviour, 68, 533–540. https://doi.org/10.1016/j.anbehav.2003.09.016
Seidel, B. (1999). Water-wave communication between territorial male Bombina variegata. Journal of Herpetology, 33, 457–462. https://doi.org/10.2307/1565643
Shine, R. (1979). Sexual selection and sexual dimorphism in the Amphibia. Copeia, 1979, 297–306. https://doi.org/10.2307/1443418
Sinsch, U. (2015). Review: Skeletochronological assessment of demographic life-history traits in amphibians. The Herpetological Journal, 25, 5–13.
Sinsch, U., & Dehling, J. M. (2017). Tropical anurans mature early and die young: Evidence from eight Afromontane Hyperolius species and a meta-analysis. PLoS ONE, 12, e0171666. https://doi.org/10.1371/journal.pone.0171666
Sullivan, B. K. (1989). Mating system variation in Woodhouse's toad (Bufo woodhousii). Ethology, 83, 60–68. https://doi.org/10.1111/j.1439-0310.1989.tb00519.x
Sullivan, B. K., Ryan, M. J. & Verrell, P. A. (1995). Female choice and mating system structure. In Heatwole, H. (Ed.), Amphibian biology (pp. 469–517). Chipping Norton, UK: Surrey Beatty & Sons.
Székely, D., Denoël, M., Székely, P., & Cogălniceanu, D. (2017). Pond drying cues and their effects on growth and metamorphosis in a fast developing amphibian. Journal of Zoology, 303, 129–135. https://doi.org/10.1111/jzo.12468
Székely, P., Székely, D., Armijos-Ojeda, D., Jara-Guerrero, A., & Cogălniceanu, D. (2016). Anfibios de un bosque seco tropical: Reserva Ecológica Arenillas, Ecuador. Ecosistemas, 25, 24–34. https://doi.org/10.7818/ECOS.2016.25-2.04
Székely, D., Székely, P., Stănescu, F., Cogălniceanu, D., & Sinsch, U. (2018). Breed fast, die young - Demography of a poorly known fossorial frog from the xeric Neotropics. Salamandra, 54, 37–44.
Telford, S. R., Dyson, M. L., & Passmore, N. I. (1989). Mate choice occurs only in small choruses of painted reed frogs Hyperolius marmoratus. Bioacoustics, 2, 47–53. https://doi.org/10.1080/09524622.1989.9753113
Ursprung, E. V. A., Ringler, M. A. X., Jehle, R., & Hödl, W. (2011). Strong male/male competition allows for nonchoosy females: High levels of polygynandry in a territorial frog with paternal care. Molecular Ecology, 20, 1759–1771. https://doi.org/10.1111/j.1365-94X.2011.05056.x
Vargas Salinas, F. (2006). Breeding behavior and colonization success of the cuban treefrog Osteopilus septentrionalis. Herpetologica, 62, 398–408. https://doi.org/10.1655/0018-0831(2006)62[398:BBACSO]2.0.CO;2
Vieites, D. R., Nieto-Roman, S., Barluenga, M., Palanca, A., Vences, M., & Meyer, A. (2004). Post-mating clutch piracy in an amphibian. Nature, 431, 305–308. https://doi.org/10.1038/nature02879
Wells, K. D. (1977). The social behaviour of anuran amphibians. Animal Behaviour, 25, 666–693. https://doi.org/10.1016/0003-3472(77)90118-X
Wells, K. D. (2010). The ecology and behavior of amphibians. Chicago, IL: University of Chicago Press.
Wiley, R. H., & Poston, J. (1996). Perspective: Indirect mate choice, competition for mates, and coevolution of the sexes. Evolution, 50, 1371–1381. https://doi.org/10.2307/2410875
Woodward, B. D. (1986). Paternal effects on juvenile growth in Scaphiopus multiplicatus (the New Mexico spadefoot toad). The American Naturalist, 128, 58–65. https://doi.org/10.1086/284539
Woodward, B. D., Travis, J., & Mitchell, S. (1988). The effects of the mating system on progeny performance in Hyla crucifer (Anura: Hylidae). Evolution, 42, 784–794. https://doi.org/10.1111/j.1558-5646.1988.tb02496.x
Yu, T. L., Li, H. J., & Lu, X. (2013). Mating patterns of from three populations along an altitudinal gradient on the Tibetan Plateau. Animal Biology, 63, 131–138. https://doi.org/10.1163/15707563-00002400
