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Fertilization success suggests random pairing in frogs with regard to body size

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Abstract

Size-assortative mating is a pattern of non-random pairing among individuals that has been presumed to arise due to the enhanced reproductive success that may accrue from mating with an individual of similar size. Its proximal mechanism may be female choice for similarly sized mates and/or large-male advantage during bouts of direct male-male competition. The hallmark for the occurrence of size-assortative mating is a significant correlation between female and male body sizes in mated pairs. In this study, we investigated the mating pattern of the emerald glass frog, Espadarana prosoblepon, whose mating system is purportedly based on female choice and therefore is a suitable study system for testing hypotheses of size-assortative mating. We specifically tested whether E. prosoblepon males found in amplexus were larger than solitary males, indicating a large-male advantage in mating and whether either larger males or size-matched pairs of frogs had a higher proportion of their eggs fertilized, consistent with a benefit to size-assortative mating. We found no evidence for any of these relationships in E. prosoblepon despite a positive correlation between female size and clutch size. Males in amplexus were not larger than unmated males, and male size did not predict the proportion of fertilized eggs. Our evidence thus indicates that the mating pattern of E. prosoblepon is random with respect to body size, in conformity with a growing body of evidence that body size is likely not a significant factor influencing mating patterns in anurans.

Significance statement

Size-assortative mating occurs when similarly sized individuals mate together more often than expected by chance. Studies addressing this question test for a correlation between female and male sizes within mating pairs, but few studies test whether mating with similarly sized individuals provides proximate benefits. Size-assortative mating should occur in species where mate choice is possible to occur, in which individuals can discriminate and choose to mate with similarly sized individuals. In frogs, many previous studies have searched for size-assortative mating, but evidence for its occurrence or selective advantage remains scant. We used the emerald glass frog, Espadarana prosoblepon, as a study system to test the predictions of size-assortative mating. We found that both mating preference and fertilization success are random with respect to body size.

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Availability of data and material

The datasets generated and/or analyzed during the current study are available within the article and its supplementary materials.

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References

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton

  • Andersson S, Örnborg J, Andersson M (1998) Ultraviolet sexual dimorphism and assortative mating in blue tits. Proc R Soc Lond B 265:445–450

    Article  Google Scholar 

  • Arak A (1983) Male-male competition and mate choice in anuran amphibians. In: Bateson P (ed) Mate choice. Cambridge University Press, Cambridge, pp 181–210

    Google Scholar 

  • Arnqvist G, Rowe L, Krupa JJ, Sih A (1996) Assortative mating by size: a meta-analysis of mating patterns in water striders. Evol Ecol 10:265–284

    Article  Google Scholar 

  • Basto-Riascos MC, López-Caro J, Vargas-Salinas F (2017) Reproductive ecology of the glass frog Espadarana prosoblepon (Anura: Centrolenidae) in an urban forest of the Central Andes of Colombia. J Nat Hist 51:2535–2550

    Article  Google Scholar 

  • Bastos RP, Haddad CFB (1996) Breeding activity of the neotropical treefrog Hyla elegans (Anura, Hylidae). J Herpetol 30:355–360

    Article  Google Scholar 

  • Bourne GR (1993) Proximate costs and benefits of mate acquisition at leks of the frog Ololygon rubra. Anim Behav 45:1051–1059

    Article  Google Scholar 

  • Briggs VS (2008) Mating patterns of red-eyed treefrogs, Agalychnis callidryas and A. moreletii. Ethology 114:489–498

    Article  Google Scholar 

  • Byrne PG, Roberts JD, Simmons LW (2002) Sperm competition selects for increased testes mass in Australian frogs. J Evol Biol 15:347–355

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Crespi BJ (1989) Causes of assortative mating in arthropods. Anim Behav 38:980–1000

    Article  Google Scholar 

  • Davies NB, Halliday TR (1977) Optimal mate selection in the toad Bufo Bufo. Nature 269:56–58

    Article  Google Scholar 

  • Dickerson BR, Willson MF, Bentzen P, Quinn TP (2004) Size-assortative mating in salmonids: negative evidence for pink salmon in natural conditions. Anim Behav 68:381–385

    Article  Google Scholar 

  • Dittrich C, Rodríguez A, Segev O, Drakulić S, Feldhaar H, Vences M, Rödel MO (2018) Temporal migration patterns and mating tactics influence size-assortative mating in Rana temporaria. Behav Ecol 29:418–428

    Article  PubMed  PubMed Central  Google Scholar 

  • Emerson SB (1997) Testis size variation in frogs: testing the alternatives. Behav Ecol Sociobiol 41:227–235

    Article  Google Scholar 

  • Fan XL, Lin ZH, Ji X (2013) Male size does not correlate with fertilization success in two bufonid toads that show size-assortative mating. Curr Zool 59:740–746

    Article  Google Scholar 

  • Friedl TW, Klump GM (2005) Sexual selection in the lek-breeding European treefrog: body size, chorus attendance, random mating and good genes. Anim Behav 70:1141–1154

    Article  Google Scholar 

  • Gerhardt HC (1994) The evolution of vocalization in frogs and toads. Annu Rev Ecol Evol S 25:293–324

    Article  Google Scholar 

  • Gingras B, Boeckle M, Herbst CT, Fitch WT (2013) Call acoustics reflect body size across four clades of anurans. J Zool 289:143–150

    Article  Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • Goyes Vallejos J, Ramirez-Soto K (2020) Causes of embryonic mortality in Espadarana prosoblepon (Anura: Centrolenidae) from Costa Rica. Phyllomedusa 19:83–92

    Article  Google Scholar 

  • Green DM (2015) Implications of female body-size variation for the reproductive ecology of an anuran amphibian. Ethol Ecol Evol 27:173–184

    Article  Google Scholar 

  • Green DM (2019) Rarity of size-assortative mating in animals: assessing the evidence with anuran amphibians. Am Nat 193:279–295

    Article  PubMed  Google Scholar 

  • Han X, Fu J (2013) Does life history shape sexual size dimorphism in anurans? A comparative analysis. BMC Evol Biol 13:1–11

    Article  Google Scholar 

  • Harari AR, Handler AM, Landolt PJ (1999) Size-assortative mating, male choice and female choice in the curculionid beetle Diaprepes abbreviatus. Anim Behav 58:1191–1200

    Article  CAS  PubMed  Google Scholar 

  • Howard RD, Kluge AG (1985) Proximate mechanisms of sexual selection in wood frogs. Evolution 39:260–277

    Article  PubMed  Google Scholar 

  • Jacobson SK (1985) Reproductive behavior and male mating success in two species of glass frogs (Centrolenidae). Herpetologica 41:396–404

    Google Scholar 

  • Jennions MD, Passmore NI (1993) Sperm competition in frogs: testis size and a ‘sterile male’ experiment on Chiromantis xerampelina (Rhacophoridae). Biol J Linn Soc 50:211–220

    Google Scholar 

  • Jiang Y, Bolnick DI, Kirkpatrick M (2013) Assortative mating in animals. Am Nat 181:E125–E138

    Article  PubMed  Google Scholar 

  • Kusano T, Toda M, Fukuyama K (1991) Testes size and breeding systems in Japanese anurans with special reference to large testes in the treefrog, Rhacophorus arboreus (Amphibia: Rhacophoridae). Behav Ecol Sociobiol 29:27–31

    Article  Google Scholar 

  • Liao WB, Lu X (2011) Proximate mechanisms leading to large male-mating advantage in the Andrew’s toad, Bufo andrewsi. Behaviour 148:1087–1102

    Article  Google Scholar 

  • Lu X, Ma X, Fan L, Hu Y, Lang Z, Li Z, Fang B, Guo W (2016) Reproductive ecology of a Tibetan frog Nanorana parkeri (Anura: Ranidae). J Nat Hist 50:2769–2782

    Article  Google Scholar 

  • Lüpold S, de Boer RA, Evans JP, Tomkins JL, Fitzpatrick JL (2020) How sperm competition shapes the evolution of testes and sperm: a meta-analysis. Phil Trans R Soc B 375:20200064

    Article  PubMed  PubMed Central  Google Scholar 

  • Márquez-M de Orense R, Tejedo-Madueño M (1990) Size-based mating pattern in the tree frog Hyla arborea. Herpetologica 46:176–182

    Google Scholar 

  • Meuche I, Brusa O, Linsenmair KE, Keller A, Pröhl H (2013) Only distance matters–non-choosy females in a poison frog population. Front Zool 10:29

    Article  PubMed  PubMed Central  Google Scholar 

  • Mobley KB, Abou Chakra M, Jones AG (2014) No evidence for size-assortative mating in the wild despite mutual mate choice in sex-role-reversed pipefishes. Ecol Evol 4:67–78

    Article  PubMed  Google Scholar 

  • Moura RR, Gonzaga MO, Pinto SN, Vasconcellos-Neto J, Requena GS (2021) Assortative mating in space and time: patterns and biases. Ecol Lett 24:1089–1102. https://doi.org/10.1111/ele.13690

    Article  Google Scholar 

  • Nali RC, Zamudio KR, Haddad CFB, Prado CPA (2014) Size-dependent selective mechanisms on males and females and the evolution of sexual size dimorphism in frogs. Am Nat 184:727–740

    Article  PubMed  Google Scholar 

  • Ng TP, Williams GA, Davies MS, Stafford R, Rolán-Alvarez E (2016) Sampling scale can cause bias in positive assortative mating estimates: evidence from two intertidal snails. Biol J Linn Soc 119:414–419

    Article  Google Scholar 

  • Ortiz-Ross X, Thompson ME, Salicetti-Nelson E, Donnelly MA (2020) Oviposition site selection in three glass frog species. Copeia 108:333–340

    Article  Google Scholar 

  • Pettitt BA, Bourne GR, Bee MA (2020) Females prefer the calls of better fathers in a Neotropical frog with biparental care. Behav Ecol 31:152–163

    Google Scholar 

  • R Development Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org

  • Reynolds RG, Fitzpatrick BM (2007) Assortative mating in poison-dart frogs based on an ecologically important trait. Evolution 61:2253–2259

    Article  PubMed  Google Scholar 

  • Robertson JGM (1990) Female choice increases fertilization success in the Australian frog, Uperoleia laevigata. Anim Behav 39:639–645

    Article  Google Scholar 

  • Rueger T, Gardiner NM, Jones GP (2016) Size matters: male and female mate choice leads to size-assortative pairing in a coral reef cardinalfish. Behav Ecol 27:1585–1591

    Google Scholar 

  • Rueger T, Gardiner NM, Jones GP (2018) Site fidelity facilitates pair formation in aggregations of coral reef cardinalfish. Oecologia 186:425–434

  • Ryan MJ (1988) Constraints and patterns in the evolution of anuran acoustic communication. In: Fritzsch B, Hethington T, Ryan M, Wilczynski W, Walkowiak W (eds) The Evolution of the Amphibian Auditory System. John Wiley, New York, pp 37–677

    Google Scholar 

  • Ryan MJ, Keddy-Hector A (1992) Directional patterns of female mate choice and the role of sensory biases. Am Nat 139:S4–S35

    Article  Google Scholar 

  • Savage JM (2002) The amphibians and reptiles of Costa Rica: a herpetofauna between two continents, between two seas. University of Chicago Press, Chicago

  • Shine R, O’connor D, LeMaster MP, Mason RT (2001) Pick on someone your own size: ontogenetic shifts in mate choice by male garter snakes result in size-assortative mating. Anim Behav 61:1133–1141

    Article  Google Scholar 

  • Sullivan BK, Ryan MJ, Verrell PA (1995) Female choice and mating system structure. In: H. Heatwole and B. K. Sullivan (eds) Amphibian biology. Surrey Beatty, Baulkham Hills, Australia, pp 469–517

  • Székely D, Székely P, Denoël M, Cogălniceanu D (2018) Random size-assortative mating despite size-dependent fecundity in a Neotropical amphibian with explosive reproduction. Ethology 124:218–226

    Article  Google Scholar 

  • Tonini JFR, Provete DB, Maciel NM, Morais AR, Goutte S, Toledo LF, Pyron RA (2020) Allometric escape from acoustic constraints is rare for frog calls. Ecol Evol 10:3686–3695

    Article  PubMed  PubMed Central  Google Scholar 

  • Valencia-Aguilar A, Zamudio KR, Haddad CFB, Bogdanowicz SM, Prado CPA (2020) Show me you care: female mate choice based on egg attendance rather than male or territorial traits. Behav Ecol 31:1054–1064

    Article  Google Scholar 

  • Wells KD (1977) The social behaviour of anuran amphibians. Anim Behav 25:666–693

    Article  Google Scholar 

  • Wells, KD (2007) The ecology and behavior of amphibians. University of Chicago Press, Chicago

  • Wogel H, Abrunhosa PA, Pombal JP (2005) Breeding behaviour and mating success of Phyllomedusa rohdei (Anura, Hylidae) in south-eastern Brazil. J Nat Hist 39:2035–2045

    Article  Google Scholar 

  • Yang Y, Richards-Zawacki CL (2021) Male–male contest limits the expression of assortative mate preferences in a polymorphic poison frog. Behav Ecol 32:151–158

    Article  Google Scholar 

  • Zhang L, Sheng Y, Yuan X, Yu F, Zhong X, Liao J, Liu Z, Chen W (2020) Proximate mechanisms responsible for random mating by size in the Himalayan toad Duttaphrynus himalayanus. Anim Biol 71:183–195

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Darko Cotoras, Rodolfo Quiros Flores, and Scott Walter for their invaluable support (logistic and otherwise). We thank Karim Ramirez-Soto for his help during fieldwork. We thank two anonymous reviewers whose comments greatly improved our manuscript.

Funding

Funding for this study was provided by the US National Science Foundation (grant number HRD-1712757) and the Organization for Tropical Studies which supported JGV, JG, ADHF, and RV during the NSF Louis Stokes Alliances for Minority Participation Research Experience for Undergraduate Program in 2018 and 2019 at Las Cruces Biological Station, Costa Rica.

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Authors and Affiliations

  1. Division of Biological Sciences, University of Missouri, Columbia, MO, 65211, USA

    Johana Goyes Vallejos

  2. University of Rhode Island, Kingston, RI, 02881, USA

    Johniah Gomez

  3. Environmental Sciences Department, University of Puerto Rico – Rio Piedras, San Juan de Puerto Rico, 00925, Puerto Rico

    Abner D. Hernández-Figueroa

  4. Department of Biology and Physical Sciences, Passaic County Community College, Paterson, NJ, 07505, USA

    Rebecca Vera

  5. Redpath Museum, McGill University, Montreal, QC, H3A 0C4, Canada

    David M. Green

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  1. Johana Goyes Vallejos
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Correspondence to Johana Goyes Vallejos.

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This research was conducted under the Ministerio del Ambiente y Energía de Costa Rica (MINAE) and Sistema Nacional de Areas de Conservación (SINAC) Scientific Research Permit Number R-SINAC-PNI-ACLAP-031–2018/2019 and followed the guidelines of the Animal Behavior Society (ABS) for the treatment of animals in behavioral research.

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Goyes Vallejos, J., Gomez, J., Hernández-Figueroa, A.D. et al. Fertilization success suggests random pairing in frogs with regard to body size. Behav Ecol Sociobiol 75, 140 (2021). https://doi.org/10.1007/s00265-021-03081-6

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