Rapid character displacement of different call parameters in closely related treefrogs (Hyla cinerea and H. gratiosa)

  • Noah M. Gordon
  • Madison Z. Ralph
  • Kane D. Stratman
Original Article

Abstract

When the range of similar species begins to overlap, niche separation may develop to maintain species boundaries. Reproductive traits are often subject to these adjustments, particularly when there is selection against hybrids. Shifts in range overlap can result in call interference, increased hybridization, and reduced mating success. Previous research has shown that these conditions can drive reproductive character displacement (RCD). Consistent with RCD, green tree frogs (Hyla cinerea) call at higher frequencies and perch higher in syntopy with their sister species (barking tree frogs, Hyla gratiosa), relative to allotopy. However, the time needed for these changes to occur and the corresponding effects on H. gratiosa remain unclear. We investigated if RCD is detectable in populations of these two species after 8 years or less of syntopy. We found an elevated high-frequency peak in calls of syntopic H. cinerea, while an increase in call duration was detected in syntopic H. gratiosa. Our results suggest that RCD can occur rapidly, in a manner consistent with the plasticity-first model, and that traits improving signal detection may be the first to respond to the pressures of syntopy and selection against hybrids.

Significance statement

Related species are expected to change their mating signals when breeding together to avoid mating with the wrong species. Green tree frogs change their mating calls when they breed in the same ponds as barking tree frogs, but it remains unclear how fast these changes can take place, or if there are any changes in barking tree frogs. We analyzed calls and perch locations within areas of recent (<8 years) range overlap in ponds where these species breed together and ponds where only one breeds. We found that when the two frogs co-occur, green tree frogs call at higher frequencies and barking tree frogs increase their calling duration. These changes were in the same direction, but diminished relative to ponds where they have lived together for long periods. Our results demonstrate that behavioral changes to avoid hybridization can occur in as few as 8 years.

Keywords

Reproductive character displacement Anura Communication Range expansion Hybrid avoidance 

References

  1. Albert AY, Schluter D (2004) Reproductive character displacement of male stickleback mate preference: reinforcement or direct selection? Evolution 58:1099–1107CrossRefPubMedGoogle Scholar
  2. Bargielowski IE, Lounibos LP, Carrasquilla MC (2013) Evolution of resistance to satyrization through reproductive character displacement in populations of invasive dengue vectors. Proc Natl Acad Sci USA 110:2888–2892CrossRefPubMedPubMedCentralGoogle Scholar
  3. Blair WF (1958) Mating call in the speciation of anuran amphibians. Am Nat 92:27CrossRefGoogle Scholar
  4. Blair WF (1974) Character displacement in frogs. Integr Comp Biol 14:1119–1125Google Scholar
  5. Brown WL, Wilson EO (1956) Character displacement. Syst Zool 5:49–65CrossRefGoogle Scholar
  6. Brumm H, Slabbekoorn H (2005) Acoustic communication in noise. Adv Stud Behav 35:151–209CrossRefGoogle Scholar
  7. Doebeli M (1996) An explicit genetic model for ecological character displacement. Ecology 77:510–520CrossRefGoogle Scholar
  8. Garroway CJ, Bowman J, Cascaden TJ, Holloway GL, Mahan CG, Malcolm JR, Steele MA, Turner G, Wilson PJ (2010) Climate change induced hybridization in flying squirrels. Glob Chang Biol 16:113–121CrossRefGoogle Scholar
  9. Gerhardt HC (1974) The vocalizations of some hybrid treefrogs: acoustic and behavioral analyses. Behaviour 49:130–151CrossRefGoogle Scholar
  10. Gerhardt HC (1976) Significance of two frequency bands in long distance vocal communication in the green treefrog. Nature 261:692–693CrossRefGoogle Scholar
  11. Gerhardt HC (1994) Reproductive character displacement of female mate choice in the grey treefrog, Hyla chrysoscelis. Anim Behav 47:959–969CrossRefGoogle Scholar
  12. Gerhardt HC (1999) Reproductive character displacement and other sources of selection on acoustic communication systems. In: Hauser MD, Konishi M (eds) The design of animal communication. Massachusetts Institute of Technology Press, Boston, pp 515–534Google Scholar
  13. Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans: common problems and diverse solutions. University of Chicago Press, ChicagoGoogle Scholar
  14. Gerhardt HC, Mudry KM (1980) Temperature effects on frequency preferences and mating call frequencies in the green treefrog, Hyla cinerea (Anura: Hylidae). J Comp Physiol 137:1–6CrossRefGoogle Scholar
  15. Gerhardt HC, Guttman SI, Karlin AA (1980a) Accuracy of sound localization in a miniature dendrobatid frog. Naturwissenschaften 67:362–363CrossRefGoogle Scholar
  16. Gerhardt HC, Guttman SI, Karlin AA (1980b) Natural hybrids between Hyla cinerea and Hyla gratiosa: morphology, vocalization and electrophoretic analysis. Copeia 1980:577–584CrossRefGoogle Scholar
  17. Gingras B, Boeckle M, Herbst CT, Fitch WT (2013) Call acoustics reflect body size across four clades of anurans. J Zool 289:143–150CrossRefGoogle Scholar
  18. Goldberg E, Lande R (2006) Ecological and reproductive character displacement of an environmental gradient. Evolution 60:1344–1357PubMedGoogle Scholar
  19. Grafe TU (1996) The function of call alternation in the African reed frog (Hyperolius marmoratus): precise call timing prevents auditory masking. Behav Ecol Sociobiol 38:149–158CrossRefGoogle Scholar
  20. Grant PR, Grant BR (2006) Evolution of character displacement in Darwin’s finches. Science 313:224–226CrossRefPubMedGoogle Scholar
  21. Higgie M, Blows MW (2008) The evolution of reproductive character displacement conflicts with how sexual selection operates within a species. Evolution 62:1192–1203CrossRefPubMedGoogle Scholar
  22. Higgie M, Chenoweth S, Blows MW (2000) Natural selection and the reinforcement of mate recognition. Science 290:519–521CrossRefPubMedGoogle Scholar
  23. Höbel G (2015) Sexual differences in responses to cross-species call interference in the green treefrog (Hyla cinerea). Behav Ecol Sociobiol 69:695–705CrossRefGoogle Scholar
  24. Höbel G, Gerhardt HC (2003) Reproductive character displacement in the acoustic communication system of green tree frogs (Hyla cinerea). Evolution 57:894–904CrossRefPubMedGoogle Scholar
  25. Höbel G, Gerhardt HC (2007) Sources of selection on signal timing in a tree frog. Ethology 113:973–982CrossRefGoogle Scholar
  26. Kentucky Department of Fish and Wildlife Resources (2014) Species information. County observation(s) for Amphibia. Green treefrog (Hyla cinerea). Commonwealth of Kentucky, http://app.fw.ky.gov/speciesinfo/speciesListCounty.asp?strScientificName=Hyla+cinerea&strGroup=5
  27. Leary CJ (2001) Investigating opposing patterns of character displacement in release and advertisement vocalizations of Bufo fowleri and Bufo americanus (Anura; Bufonidae). Can J Zool 79:1577–1585CrossRefGoogle Scholar
  28. Lemmon EM (2009) Diversification of conspecific signals in sympatry: geographic overlap drives multidimensional reproductive character displacement in frogs. Evolution 63:1155–1170CrossRefPubMedGoogle Scholar
  29. Lemmon AR, Smadja C, Kirkpatrick M (2004) Reproductive character displacement is not the only possible outcome of reinforcement. J Evol Biol 17:177–183CrossRefPubMedGoogle Scholar
  30. Lodato MJ, Engbrecht NJ, Klueh-Mundy S, Walker Z (2015) The green treefrog, Hyla cinerea in Indiana. Proc Indiana Acad Sci 123:179–195Google Scholar
  31. Loftus-Hills JJ, Littlejohn MJ (1992) Reinforcement and reproductive character displacement in Gastrophryne carolinensis and G. olivacea (Anura: Microhylidae): a reexamination. Evolution 46:896–906CrossRefPubMedGoogle Scholar
  32. Mecham JS (1960) Introgressive hybridization between two southeastern treefrogs. Evolution 14:445–457CrossRefGoogle Scholar
  33. Muhlfeld CC, Kovach RP, Jones LA, Al-Chokhachy R, Boyer MC, Leary RF, Lowe WH, Luikart G, Allendorf FW (2014) Invasive hybridization in a threatened species is accelerated by climate change. Nat Clim Chang 4:620–624CrossRefGoogle Scholar
  34. Okamoto KW, Grether GF (2013) The evolution of species recognition in competitive and mating contexts: the relative efficacy of alternative mechanisms of character displacement. Ecol Lett 16:670–678CrossRefPubMedGoogle Scholar
  35. Oldham RS, Gerhardt HC (1975) Behavioral isolating mechanisms of the treefrogs Hyla cinerea and H. gratiosa. Copeia 1975:223–231CrossRefGoogle Scholar
  36. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42CrossRefPubMedGoogle Scholar
  37. Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891CrossRefGoogle Scholar
  38. Pfennig KS (2003) A test of alternative hypotheses for the evolution of reproductive isolation between spadefoot toads: support for the reinforcement hypothesis. Evolution 57:2842–2851CrossRefPubMedGoogle Scholar
  39. Pfennig KS, Pfennig DW (2009) Character displacement: ecological and reproductive responses to a common evolutionary problem. Q Rev Biol 84:253–276CrossRefPubMedPubMedCentralGoogle Scholar
  40. Pfennig DW, Pfennig KS (2010) Character displacement and the origins of diversity. Am Nat 176:S26–S44CrossRefPubMedPubMedCentralGoogle Scholar
  41. Pfennig DW, Pfennig KS (2012) Development and evolution of character displacement. Ann N Y Acad Sci 1256:89–107CrossRefPubMedPubMedCentralGoogle Scholar
  42. Pfennig KS, Ryan MJ (2006) Reproductive character displacement generates reproductive isolation among conspecific populations: an artificial neural network study. Proc R Soc Lond B 273:1361–1368CrossRefGoogle Scholar
  43. Richardson C, Léna JP, Joly P, Lengagne T (2008) Are leaders good mates? A study of call timing and male quality in a chorus situation. Anim Behav 76:1487–1495CrossRefGoogle Scholar
  44. Sætre GP, Cuevas A, Hermansen JS, Elgvin TO, Fernández LP, Sæther SA, Cascio Sætre CL, Eroukhmanoff F (2017) Rapid polygenic response to secondary contact in a hybrid species. Proc R Soc B 284:20170365CrossRefPubMedGoogle Scholar
  45. Schlefer EK, Romano MA, Guttman SI, Ruth SB (1986) Effects of twenty years of hybridization in a disturbed habitat on Hyla cinerea and Hyla gratiosa. J Herpetol 20:210–221CrossRefGoogle Scholar
  46. Slatkin M (1980) Ecological character displacement. Ecology 61:163–177CrossRefGoogle Scholar
  47. Stuart YE, Campbell TS, Hohenlohe PA, Reynolds RG, Revell LJ, Losos JB (2014) Rapid evolution of a native species following invasion by a congener. Science 346:463–466CrossRefPubMedGoogle Scholar
  48. Taper ML, Case TJ (1985) Quantitative genetic models for the coevolution of character displacement. Ecology 66:355–371CrossRefGoogle Scholar
  49. Van der Putten WH (2012) Climate change, aboveground-belowground interactions, and species' range shifts. Annu Rev Ecol Evol Syst 43:365–383CrossRefGoogle Scholar
  50. Waddington CH (1953) Genetic assimilation of an acquired character. Evolution 7:118–126CrossRefGoogle Scholar
  51. Walkowiak W (2007) Call production and neural basis of vocalization. In: Narins PM, Feng AS, Fay RR, Popper AN (eds) Hearing and sound communication in amphibians. Springer, New York, pp 87–112Google Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Noah M. Gordon
    • 1
  • Madison Z. Ralph
    • 1
  • Kane D. Stratman
    • 1
    • 2
  1. 1.Department of BiologyUniversity of EvansvilleEvansvilleUSA
  2. 2.Department of Biological SciencesUniversity of WisconsinMilwaukeeUSA

Personalised recommendations