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Local preference encoded by complex signaling: mechanisms of mate preference in the red-eyed treefrog (Agalychnis callidryas)

  • Kristine KaiserEmail author
  • Chloe Boehlke
  • Edauri Navarro-Pérez
  • Andres Vega
  • Steven Dudgeon
  • Jeanne M. Robertson
Original Article

Abstract

The Central American red-eyed treefrog (Agalychnis callidryas) is a nocturnal/crepuscular frog that exhibits high population-level phenotypic variation in a suite of traits generally important in anuran communication. Females of this species demonstrate a preference for local over non-local males, although the contribution of different communication modes to mate choice remains untested. We performed eight sets of experiments at La Selva Biological Station (Costa Rica) to test the relative roles of male advertisement call and flank-stripe pattern on female mate choice. For each trial, we used pre-recorded calls for acoustic signals and/or 3D-printed, hand-painted models for visual stimulus. Females selected conspecifics over heterospecifics when presented with either acoustic or visual stimuli only, indicating that both evolve as species-specific signals used for mate discrimination. Bayesian modeling showed that females chose local males over non-locals based on unimodal; responses to multimodal signals varied. Female mate choice in this species is likely nuanced and subject to the constraints of the local environment in which animals are signaling. Our data show that at least two traits that vary among populations are important for mate selection.

Significance statement

Evolution shapes animal communication in diverse ways to accommodate complicated signaling contexts, including environmental noise, the presence of eavesdroppers, and changing landscapes. Among species that use complex signals or signals in multiple modalities, understanding the role of signaling traits in reproductive behavior and their concomitant shifts between populations can shed light on lineage divergence, speciation, and the forces shaping communication. We used choice tests with Agalychnis callidryas to determine which traits lead to local-male mate preference. We found that both call and stripe are each sufficient to allow this nocturnal frog to choose mates in absence of the other stimulus. Multimodal signals were marginally better than call—but not color—alone. This may be a result of statistical noise or preliminary evidence of asymmetric use of traits across a complex landscape. These results suggest that call and color may encode both redundant information and multiple messages to receivers in this species: either is sufficient to elicit mate choice (redundant), but together, they enhance local mate preference (multiple messages). Further tests on how other communication modalities inform behavior will add to our understanding of complex signaling and lineage divergence among differentiated populations in this species.

Keywords

Communication Multimodal signaling Phenotypic variation Population divergence 

Notes

Acknowledgments

We thank Carissa Ganong, Leticia Classen, La Selva Biological Station and the Organization for Tropical Studies for their tremendous field support. Cindy Hitchcock created and painted the models and Bingbing Li and Shaojie Fei generated 3D printed models. Two anonymous reviewers greatly improved this manuscript.

Funding

This study was funded in part by the Louis Stokes Alliances for Minority Participation Research Experience for Undergraduates program at La Selva Biological Station (National Science Foundation grant number 1619683).

Compliance with ethical standards

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. This research was approved by the IACUC at CSUN (1516-015a) and conducted by permission from the Ministerio de Ambiente y Energia (SINAC-SE-GCUS-PI-R-061-2015).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

265_2018_2597_MOESM1_ESM.docx (318 kb)
ESM 1 (DOCX 318 kb)
265_2018_2597_MOESM2_ESM.xlsx (36 kb)
ESM 2 (XLSX 35 kb)

References

  1. Akopyan M, Kaiser K, Owen C, Savant N, Dudgeon S, Vega A, Robertson JM (2017) Melodic males and flashy females: geographic variation in male and female reproductive behavior in red-eyed treefrogs (Agalychnis callidryas). Ethology 124:54–64CrossRefGoogle Scholar
  2. Arnold ML (2015) Divergence with genetic exchange. Oxford University Press, OxfordCrossRefGoogle Scholar
  3. Auld HL, Pusiak RJP, Godin J-GJ (2016) Independent mating preferences for male body size and coloration in female Trinidadian guppies. Ethology 122:597–608CrossRefGoogle Scholar
  4. Bailey NW, Zuk M (2012) Socially flexible female choice differs among populations of the Pacific field cricket: geographical variation in the interaction coefficient psi (psi). Proc R Soc Lond B 279:3589–3596CrossRefGoogle Scholar
  5. Barbosa F, Rebar D, Greenfield MD (2016) Female preference functions drive interpopulation divergence in male signalling: call diversity in the bushcricket Ephippiger diurnus. J Evol Biol 29:2219–2228CrossRefGoogle Scholar
  6. Burmeister S, Wilczynski W, Ryan MJ (1999) Temporal call changes and prior experience affect graded signalling in the cricket frog. Anim Behav 57:611–618CrossRefGoogle Scholar
  7. Caldwell MS, Johnston GR, McDaniel JG, Warkentin KM (2010) Vibrational signaling in the agonistic interactions of red-eyed treefrogs. Curr Biol 20:1012–1017CrossRefGoogle Scholar
  8. Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595CrossRefGoogle Scholar
  9. Cayuela H, Lengagne T, Joly P, Léna J-P (2017) Females trade off the uncertainty of breeding resource suitability with male quality during mate choice in an anuran. Anim Behav 123:179–185CrossRefGoogle Scholar
  10. Dapper AL, Baugh AT, Ryan MJ (2011) The sounds of silence as an alarm cue in túngara frogs, Physalaemus pustulosus. Biotropica 43:380–385CrossRefGoogle Scholar
  11. Darwin C (1871) The descent of man and selection in relation to sex. Murray, LondonGoogle Scholar
  12. Darwin C (1872) The expression of the emotions in man and animals. Murray, LondonCrossRefGoogle Scholar
  13. Davis LR, Klonoski K, Rutschow HL, van Wijk KJ, Sun Q, Haribal MM, Saporito RA, Vega A, Rosenblum EB, Zamudio KR, Robertson JM (2016) Host defense skin peptides vary with color pattern in the highly polymorphic red-eyed treefrog. Front Ecol Evol 4:97CrossRefGoogle Scholar
  14. Duellman W (1970) The Hylid frogs of middle America. University of Kansas, LawrenceGoogle Scholar
  15. Duellman WE, Trueb L (1986) Biology of amphibians. Johns Hopkins University Press, BaltimoreGoogle Scholar
  16. Farris HE, Rand AS, Ryan MJ (2002) The effects of spatially separated call components on phonotaxis in túngara frogs: evidence for auditory grouping. Brain Behav Evol 60:181–188CrossRefGoogle Scholar
  17. Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans: common problems and diverse solutions. University of Chicago Press, ChicagoGoogle Scholar
  18. Gerhardt HC, Dyson ML, Tanner SD (1996) Dynamic properties of the advertisement calls of gray tree frogs: patterns of variability and female choice. Behav Ecol 7:7–18CrossRefGoogle Scholar
  19. Gomes D, Halfwerk W, Taylor R, Ryan M, Page R (2017) Multimodal weighting differences by bats and their prey: probing natural selection pressures on sexually selected traits. Anim Behav 134:99–102CrossRefGoogle Scholar
  20. Gomez D, Richardson C, Lengagne T, Plenet S, Joly P, Lena JP, Thery M (2009) The role of nocturnal vision in mate choice: females prefer conspicuous males in the European tree frog (Hyla arborea). Proc R Soc Lond B 276:2351–2358CrossRefGoogle Scholar
  21. Gomez D, Richardson C, Thery M, Lengagne T, Lena JP, Plenet S, Joly P (2011) Multimodal signals in male European treefrog (Hyla arborea) and the influence of population isolation on signal expression. Biol J Linn Soc 103:633–647CrossRefGoogle Scholar
  22. Hardy EJ, Bumm LA, Schlupp I (2017) Social function of a variable lateral stripe in Xiphophorus hellerii? Ethology 123:875–884CrossRefGoogle Scholar
  23. Hebets EA, Papaj DR (2005) Complex signal function: developing a framework of testable hypotheses. Behav Ecol Sociobiol 57:197–214Google Scholar
  24. Hebets EA, Vink CJ (2007) Experience leads to preference: experienced females prefer brush-legged males in a population of syntopic wolf spiders. Behav Ecol 18:1010–1020CrossRefGoogle Scholar
  25. Higham JP, Hebets EA (2013) An introduction to multimodal communication. Behav Ecol Sociobiol 67:1381–1388CrossRefGoogle Scholar
  26. Hödl W, Amézquita A (2001) Visual signaling in anuran amphibians. In: Ryan MJ (ed) Anuran communication. Smithsonian Institution Press, Washington DC, pp 121–141Google Scholar
  27. Jacobs LE, Vega A, Dudgeon S, Kaiser K, Robertson JM (2017) Local not vocal: assortative female choice in divergent populations of red-eyed treefrogs, Agalychnis callidryas (Hylidae: Phyllomedusinae). Biol J Linn Soc 120:171–178Google Scholar
  28. Kaiser K, Scofield DG, Alloush M, Jones RM, Marczak S, Martineau K, Oliva MA, Narins P (2011) When sounds collide: the effect of anthropogenic noise on a breeding assemblage of frogs in Belize, Central America. Behaviour 148:215–232CrossRefGoogle Scholar
  29. Laird KL, Clements P, Hunter KL, Taylor RC (2016) Multimodal signaling improves mating success in the green tree frog (Hyla cinerea), but may not help small males. Behav Ecol Sociobiol 70:1517–1525CrossRefGoogle Scholar
  30. Lande R (1981) Models of speciation by sexual selection on polygenic traits. Proc Natl Acad Sci U S A 78:3721–3725CrossRefGoogle Scholar
  31. Lea AM, Ryan MJ (2015) Irrationality in mate choice revealed by túngara frogs. Science 349:964–966CrossRefGoogle Scholar
  32. Maan ME, Hofker KD, van Alphen JJ, Seehausen O (2006) Sensory drive in cichlid speciation. Am Nat 167:947–954CrossRefGoogle Scholar
  33. Madden JR (2006) Interpopulation differences exhibited by spotted bowerbirds Chlamydera maculata across a suite of male traits and female preferences. Ibis 148:425–435CrossRefGoogle Scholar
  34. Narins PM, Hödl W, Grabul DS (2003) Bimodal signal requisite for agonistic behavior in a dart-poison frog, Epipedobates femoralis. Proc Natl Acad Sci U S A 100:577–580CrossRefGoogle Scholar
  35. Narins P, Feng AS, Fay RR (2006) Hearing and sound communication in amphibians. Springer-Verlag, New YorkCrossRefGoogle Scholar
  36. Paluh DJ, Hantak MM, Saporito RA (2014) A test of aposematism in the dendrobatid poison frog Oophaga pumilio: the importance of movement in clay model experiments. J Herpetol 48:249–254CrossRefGoogle Scholar
  37. Panhuis TM, Butlin R, Zuk M, Tregenza T (2001) Sexual selection and speciation. Trends Ecol Evol 16:364–371CrossRefGoogle Scholar
  38. Partan S, Marler P (1999) Communication goes multimodal. Science 283:1272–1273Google Scholar
  39. Partan SR, Marler P (2005) Issues in the classification of multimodal communication signals. Am Nat 166:231–245CrossRefGoogle Scholar
  40. Pomiankowski A, Iwasa Y (1998) Runaway ornament diversity caused by Fisherian sexual selection. Proc Natl Acad Sci U S A 95:5106–5111CrossRefGoogle Scholar
  41. Preininger D, Boeckle M, Freudmann A, Starnberger I, Sztatecsny M, Hödl W (2013a) Multimodal signaling in the small torrent frog (Micrixalus saxicola) in a complex acoustic environment. Behav Ecol Sociobiol 67:1449–1456CrossRefGoogle Scholar
  42. Preininger D, Boeckle M, Sztatecsny M, Hödl W (2013b) Divergent receiver responses to components of multimodal signals in two foot-flagging frog species. PLoS One 8:e55367CrossRefGoogle Scholar
  43. Pyburn WF Breeding behavior of the leaf-frogs Phyllomedusa callidryas and Phyllomedusa dacnicolor in Mexico. Copeia 1970, 1970:209–218Google Scholar
  44. Ramer JD, Jenssen TA, Hurst CJ Size-related variation in the advertisement call of Rana clamitans (Anura: Ranidae), and its effect on conspecific males. Copeia 1983, 1983:141–155Google Scholar
  45. Rand AS, Ryan MJ, Wilczynski W (1992) Signal redundancy and receiver permissiveness in acoustic mate recognition by the túngara frog, Physalaemus pustulosus. Am Zool 32:81–90CrossRefGoogle Scholar
  46. Richardson C, Gomez D, Durieux R, Thery M, Joly P, Lena JP, Plenet S, Lengagne T (2010) Hearing is not necessarily believing in nocturnal anurans. Biol Lett 6:633–635CrossRefGoogle Scholar
  47. Robertson JM, Greene HW (2017) Bright colour patterns as social signals in nocturnal frogs. Biol J Linn Soc 121:849–857CrossRefGoogle Scholar
  48. Robertson JM, Robertson A (2008) Spatial and temporal patterns of phenotypic variation in a Neotropical frog. J Biogeogr 35:830–843CrossRefGoogle Scholar
  49. Robertson JM, Vega A (2011) Genetic and phenotypic variation in a colourful treefrog across five geographic barriers. J Biogeogr 38:2122–2135CrossRefGoogle Scholar
  50. Robertson JM, Zamudio KR (2009) Genetic diversification, vicariance, and selection in a polytypic frog. J Hered 100:715–731CrossRefGoogle Scholar
  51. Robertson JM, Duryea MC, Zamudio KR (2009) Discordant patterns of evolutionary differentiation in two Neotropical treefrogs. Mol Ecol 18:1375–1395CrossRefGoogle Scholar
  52. Robertson JM, Nava Landeros R, Vega A, Kaiser K (2018) Uniformity in premating reproductive isolation along an intraspecific cline. Curr Zool 64:641–652CrossRefGoogle Scholar
  53. Ryan MJ, Perrill SA, Wilczynski W (1992) Auditory tuning and call frequency predict population-based mating preferences in the cricket frog, Acris crepitans. Am Nat 139:1370–1383CrossRefGoogle Scholar
  54. Savage JM (2002) The amphibians and reptiles of Costa Rica: a Herpetofauna between two continents, between two seas. University of Chicago Press, ChicagoGoogle Scholar
  55. Savage JM, Heyer WR (1967) Variation and distribution in the tree-frog genus Phyllomedusa in Costa Rica, Central America: with 6 figures. Stud Neotropical Fauna Environ 5:111–131Google Scholar
  56. Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, UrbanaGoogle Scholar
  57. Smith MJ, Roberts JD (2003) An experimental examination of female preference patterns for components of the male advertisement call in the quacking frog, Crinia georgiana. Behav Ecol Sociobiol 55:144–150CrossRefGoogle Scholar
  58. Stange N, Page RA, Ryan MJ, Taylor RC (2017) Interactions between complex multisensory signal components result in unexpected mate choice responses. Anim Behav 134:239–247CrossRefGoogle Scholar
  59. Starnberger I, Poth D, Peram PS, Schulz S, Vences M, Knudsen J, Barej MF, Rödel MO, Walzl M, Hödl W (2013) Take time to smell the frogs: vocal sac glands of reed frogs (Anura: Hyperoliidae) contain species-specific chemical cocktails. Biol J Linn Soc 110:828–838CrossRefGoogle Scholar
  60. Starnberger I, Preininger D, Hödl W (2014a) The anuran vocal sac: a tool for multimodal signalling. Anim Behav 97:281–288CrossRefGoogle Scholar
  61. Starnberger I, Preininger D, Hödl W (2014b) From uni- to multimodality: towards an integrative view on anuran communication. J Comp Physiol A 200:777–787CrossRefGoogle Scholar
  62. Symes LB (2018) Spatial and temporal variation in three call traits and preferences of the tree cricket Oecanthus forbesi. Behav Ecol Sociobiol 72:35CrossRefGoogle Scholar
  63. Tanner JC, Ward JL, Shaw RG, Bee MA (2017) Multivariate phenotypic selection on a complex sexual signal. Evolution 71:1742–1754CrossRefGoogle Scholar
  64. Taylor RC, Klein BA, Stein J, Ryan MJ (2008) Faux frogs: multimodal signalling and the value of robotics in animal behaviour. Anim Behav 76:1089–1097CrossRefGoogle Scholar
  65. Uy JAC, Safran RJ (2013) Variation in the temporal and spatial use of signals and its implications for multimodal communication. Behav Ecol Sociobiol 67:1499–1511CrossRefGoogle Scholar
  66. Vásquez T, Pfennig KS (2007) Looking on the bright side: females prefer coloration indicative of male size and condition in the sexually dichromatic spadefoot toad, Scaphiopus couchii. Behav Ecol Sociobiol 62:127–135CrossRefGoogle Scholar
  67. Ward JL, McLennan DA (2009) Mate choice based on complex visual signals in the brook stickleback, Culaea inconstans. Behav Ecol 20:1323–1333CrossRefGoogle Scholar
  68. Weaver W (1953) Recent contributions to the mathematical theory of communication. Et Cetera 10:261–281Google Scholar
  69. Wells KD (2010) The ecology and behavior of amphibians. University of Chicago Press, ChicagoGoogle Scholar
  70. West-Eberhard MJ (1983) Sexual selection, social competition, and speciation. Q Rev Biol 58:155–183CrossRefGoogle Scholar
  71. Wollerman L (1998) Stabilizing and directional preferences of female Hyla ebraccata for calls differing in static properties. Anim Behav 55:1619–1630CrossRefGoogle Scholar
  72. Zhu B, Wang J, Zhao L, Sun Z, Brauth SE, Tang Y, Cui J (2016) Bigger is not always better: females prefer males of mean body size in Philautus odontotarsus. PLoS One 11:e0149879CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Kristine Kaiser
    • 1
    Email author
  • Chloe Boehlke
    • 2
  • Edauri Navarro-Pérez
    • 3
  • Andres Vega
    • 4
  • Steven Dudgeon
    • 1
  • Jeanne M. Robertson
    • 1
  1. 1.Department of BiologyCalifornia State University, NorthridgeNorthridgeUSA
  2. 2.Department of BiologyFort Lewis CollegeDurangoUSA
  3. 3.Department of Environmental ScienceUniversity of Puerto Rico, Río PiedrasSan JuanPuerto Rico
  4. 4.AMBICORTibasCosta Rica

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