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Epigenomic changes in the túngara frog (Physalaemus pustulosus): possible effects of introduced fungal pathogen and urbanization

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Abstract

Amphibian populations are being threatened by human related activities including the spread of the fungal pathogen, Batrachochytrium dendrobatidis (Bd) and urbanization. With growing losses in global amphibian biodiversity, it is essential to document how amphibian populations are responding to rapid environmental changes. While most evolutionary processes, e.g. changes in allelic frequencies, may be too slow to allow adequate response to environmental changes, epigenetic modifications can rapidly translate environmental changes into adaptive phenotypic responses. Epigenetic modifications come in multiple, non-exclusive forms, the most notable being DNA methylation. Here we sought to examine variation in the frequency of DNA methylation among four túngara frog populations distributed across Gamboa, Panama; which vary in both their level of fungal presence/prevalence and urbanization. DNA samples were collected from amplexed (male–female) pairs and frequency of DNA methylation was analyzed using a methylation-sensitive amplified fragment length polymorphism protocol. We found significant variation in DNA methylation among populations, and correlations between Bd infection status and methylation patterns. Urbanization, however, had no influences on the frequency of DNA methylation. These data suggest epigenetic modifications are substantially flexible across fine-scale, environmental gradients and there appears to be possible biologically relevant links between DNA methylation and Bd infection status. Our results provide a basis for future work investigating the causal role epigenetics have in mediating phenotypic response to human-induced, environmental changes.

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Availability of data and materials

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Asplen MK, Anfora G, Biondi A et al (2015) Invasion biology of spotted wing Drosophila (Drosophila suzukii): a global perspective and future priorities. J Pest Sci 88:469–494

    Article  Google Scholar 

  • Becker G, Zamudio KR (2011) Tropical amphibian populations experience higher disease risk in natural habitats. PNAS 108(24):9893–9898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bender J (2004) DNA methylation and epigenetics. Annu Rev Plant Biol 55(1):41–68

    Article  CAS  PubMed  Google Scholar 

  • Berger L, Speare R, Daszak P et al (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. PNAS 95(15):9031–9036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bird A (2007) Perceptions of epigenetics. Nature 447:396–398

    Article  CAS  PubMed  Google Scholar 

  • Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Lett 11(2):106–115

    PubMed  Google Scholar 

  • Burggren WW, Crews D (2014) Epigenetics in comparative biology: why we should pay attention. J Integr Comp Biol 54(1):7–20

    Article  Google Scholar 

  • Ellison A, Lopez CMR, Moran P et al (2015) Epigenetic regulation of sex ratios may explain natural variation in self-fertilization rates. Proc R Soc B 282(1819):20151900

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Foust CM, Preite V, Schrey AW et al (2016) Genetic and epigenetic differences associated with environmental gradients in replicate populations of two salt marsh perennials. Mol Ecol 25(8):1639–1652

    Article  CAS  PubMed  Google Scholar 

  • Gao L, Geng Y, Li B et al (2010) Genome-wide DNA methylation alterations of Alternanthera philoxeroides in natural and manipulated habitats: implications for epigenetic regulation of rapid responses to environmental fluctuation and phenotypic variation. Plant Cell Environ 33(11):1820–1827

    Article  CAS  PubMed  Google Scholar 

  • Greally JM (2018) A user's guide to the ambiguous word 'epigenetics'. Nat Rev Mol Cell Biol 19(4):207–208

    Article  CAS  PubMed  Google Scholar 

  • Gridi-Papp M, Rand AS, Ryan MJ (2006) Animal communication: complex call production in the túngara frog. Nature 441:38

    Article  CAS  PubMed  Google Scholar 

  • Halfwerk W, Jones PL, Taylor RC et al (2014) Risky ripples allow bats and frogs to eavesdrop on a multisensory sexual display. Science 343(6169):413–416

    Article  CAS  PubMed  Google Scholar 

  • Halfwerk W, Blaas M, Kramer L et al (2019) Adaptive changes in sexual signaling in response to urbanization. Nat Ecol Evol 3(3):374–383

    Article  PubMed  Google Scholar 

  • Hammond SA, Nelson CJ, Helbing CC (2016) Environmental influences on the epigenomes of herpetofauna and fish. Biochem Cell Biol 94:95–100

    Article  CAS  PubMed  Google Scholar 

  • Herrera CM, Bazaga P (2010) Epigenetic differentiation and relationship to adaptive genetic divergence in discrete populations of the violet Viola cazorlensis. New Phytol 187(3):867–876

    Article  CAS  PubMed  Google Scholar 

  • Herrera CM, Bazaga P (2011) Untangling individual variation in natural populations: ecological, genetic and epigenetic correlates of long-term inequality in herbivory. Mol Ecol 20(8):1675–1688

    Article  CAS  PubMed  Google Scholar 

  • Herrera CM, Bazaga P (2016) Genetic and epigenetic divergence between disturbed and undisturbed subpopulations of a Mediterranean shrub: a 20-year field experiment. Ecol Evol 187(3):3832–3847

    Article  Google Scholar 

  • Hof C, Araujo MB, Jetz W, Rahbeck C (2014) Additive threats from pathogens, climate and land-use change for global amphibian diversity. Nat Lett 480:516–519

    Article  CAS  Google Scholar 

  • Holland BR, Clarke AC, Meudt HM (2008) Optimizing automated AFLP scoring parameters to improve phylogenetic resolution. Syst Biol 57(3):347–366

    Article  PubMed  Google Scholar 

  • Hu J, Barrett RD (2017) Epigenetics in natural animal populations. J Evol Biol 30:1612–1632

    Article  CAS  PubMed  Google Scholar 

  • Jackson ST, Sax DF (2010) Balancing biodiversity in a changing environment: extinction debt, immigration credit and species turnover. Trends Ecol Evol 25(3):153–160

    Article  PubMed  Google Scholar 

  • Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33:245–254

    Article  CAS  PubMed  Google Scholar 

  • James TY, Toledo LF, Rödder D et al (2015) Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: lessons from the first 15 years of amphibian chytridiomycosis research. Ecol Evol 5(18):4079–4097

    Article  PubMed  PubMed Central  Google Scholar 

  • Jirtle RL, Skinner MK (2007) Environmental epigenomics and disease susceptibility. Nat Rev Genet 8:253–262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johannes F, Porcher E, Teixeira FK et al (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet 5(6):e1000530

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Johnson PTJ, Mckenzie VJ, Peterson AC et al (2011) Regional decline of an iconic amphibian associated with elevation, land-use change, and invasive species. Conserv Biol 25(3):556–566

    Article  PubMed  Google Scholar 

  • Jombart T, Ahmed I (2011) adegenet 1.3-1: New tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94

    Article  PubMed  PubMed Central  Google Scholar 

  • Kolby J, Daszak P (2016). The emerging amphibian fungal disease, chytridiomycosis: a key example of the global phenomenon of wildlife emerging infectious diseases. In: Scheld W, Hughes J, Whitley R (eds) Emerging infections, vol 10. ASM Press, Washington, DC

    Google Scholar 

  • Koo TK, Li MY (2016) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 15:155–163

    Article  PubMed  PubMed Central  Google Scholar 

  • Kosch TA, Bataille A, Didinger C et al (2016) MHC selection dynamics in pathogen-infected túngara frog (Physalaemus pustulosus) populations. Biol Lett 12:20160345

    Article  PubMed  PubMed Central  Google Scholar 

  • Lampert KP, Rand AS, Mueller UG, Ryan MJ (2003) Fine-scale genetic pattern and evidence for sex-biased dispersal in the túngara frog Physalaemus pustulosus. Mol Ecol 12(12):3325–3334

    Article  CAS  PubMed  Google Scholar 

  • Lankau R, Jørgensen PS, Harris DJ, Sih A (2011) Incorporating evolutionary principles into environmental management and policy. Evol Appl 4(2):315–325

    Article  PubMed  PubMed Central  Google Scholar 

  • Lappalainen T, Greally JM (2017) Associating cellular epigenetic models with human phenotypes. Nat Rev Genet 18(7):441–451

    Article  CAS  PubMed  Google Scholar 

  • Ledon-Rettig CC, Richards CL, Martin LB (2013) Epigenetics for behavioral ecologists. Behav Ecol 24:311–324

    Article  Google Scholar 

  • Liebl AL, Schrey AW, Richards CL, Martin LB (2013) Patterns of DNA methylation throughout a range expansion of an introduced songbird. Integr Comp Biol 53(2):351–358

    Article  CAS  PubMed  Google Scholar 

  • Liu S, Sun K, Jiang T et al (2012) Natural epigenetic variation in the female great roundleaf bat (Hipposideros armiger) populations. Mol Gene Genomics 287(8):643–650

    Article  CAS  Google Scholar 

  • McNew SM, Beck D, Sadler-Riggleman I et al (2017) Epigenetic variation between urban and rural populations of Darwin’s finches. BMC Evol Biol 17:183

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nilsson EE, Skinner MK (2015) Environmentally induced epigenetic transgenerational inheritance of disease susceptibility. Transl Res 165(1):12–17

    Article  CAS  PubMed  Google Scholar 

  • Nori J, Lemes P, Urbina-Cardona N et al (2015) Amphibian conservation, land-use changes and protected areas: a global overview. Biol Conserv 191:367–374

    Article  Google Scholar 

  • Palumbi S (2001) Humans as the world’s greatest evolutionary force. Science 293(5536):1786–1790

    Article  CAS  PubMed  Google Scholar 

  • Paradis E (2010) Pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26(3):419–420

    Article  CAS  PubMed  Google Scholar 

  • Pereira HM, Leadley PW, Proença V et al (2010) Scenarios for global biodiversity in the twenty-first century. Science 330(6010):1496–1501

    Article  CAS  PubMed  Google Scholar 

  • Perez-Figueroa A (2013) MSAP: a tool for the statistical analysis of methylation-sensitive amplified polymorphism data. Mol Ecol Resour 13(3):522–527

    Article  CAS  PubMed  Google Scholar 

  • Phillips BL, Puschendorf R (2013) Do pathogens become more virulent as they spread? Evidence from the amphibian declines in Central America. Proc R Soc B Biol Sci 280(1766):20131290

    Article  Google Scholar 

  • Platt A, Gugger PF, Pellegrini M, Sork VL (2015) Genome-wide signature of local adaptation linked to variable CpG methylation in oak populations. Mol Ecol 24(15):3823–3830

    Article  CAS  PubMed  Google Scholar 

  • Pounds JA, Crump ML (1994) Declines and climate amphibian the case disturbance: toad and the of the golden frog harlequin. Conserv Biol 8(1):72–85

    Article  Google Scholar 

  • Pounds JA, Fogden MPL, Savage JM, Gorman GC (1997) Tests of null models for amphibian declines on a tropical mountain. Conserv Biol 11(6):1307–1322

    Article  Google Scholar 

  • R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Robertson BA, Rehage JS, Sih A (2013) Ecological novelty and the emergence of evolutionary traps. Trends Ecol Evol 28(9):552–560

    Article  PubMed  Google Scholar 

  • Robinson B, Pfennig D (2013) Inducible competitors and adaptive diversification. Curr Zool 59(4):537–552

    Article  Google Scholar 

  • Rodríguez-Brenes S, Rodriguez D, Ibá R, Ryan MJ (2016) Spread of amphibian chytrid fungus across lowland populations of túngara frogs in Panamá. PLoS ONE 11(5):e0155745

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ryan MJ (1985) The túngara frog, a study in sexual selection and communication. University of Chicago Press, Chicago

    Google Scholar 

  • Savage AE, Terrell KA, Gratwicke B et al (2016) Reduced immune function predicts disease susceptibility in frogs infected with a deadly fungal pathogen. Conserv Physiol 4(1):cow011

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schrey AW, Alvarez M, Foust CM et al (2013) Ecological epigenetics: beyond MS-AFLP. Integr Comp Biol 53(2):340–350

    Article  PubMed  Google Scholar 

  • Sih A (2013) Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview. Anim Behav 85(5):1077–1088

    Article  Google Scholar 

  • Sih A, Stamps J, Yang LH, McElreath R, Ramenofsky M (2010) Behavior as a key component of integrative biology in a human-altered world. Integr Comp Biol 50(6):934–944

    Article  PubMed  Google Scholar 

  • Skinner MK (2014) Environmental stress and epigenetic transgenerational inheritance. BMC Med 12(153):1–5

    Google Scholar 

  • Smith TA, Martin MD, Nguyen M, Mendelson TC (2016) Epigenetic divergence as a potential first step in darter speciation. Mol Ecol 25(8):1883–1894

    Article  CAS  PubMed  Google Scholar 

  • Strimmer K (2008) fdrtool: a versatile R package for estimating local and tail area-based false discovery rates. Bioinformatics 24(12):1461–1462

    Article  CAS  PubMed  Google Scholar 

  • Taylor RC, Ryan MJ (2013) Interactions of multisensory components perceptually rescue túngara frog mating signals. Science 341(6143):273–274

    Article  CAS  PubMed  Google Scholar 

  • Vaiserman A (2015) Epidemiologic evidence for association between adverse environmental exposures in early life and epigenetic variation: a potential link to disease susceptibility? Clin Epigenet 7(1):96

    Article  CAS  Google Scholar 

  • Weaver ICG, Cervoni N, Champagne FA et al (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7(8):847–854

    Article  CAS  PubMed  Google Scholar 

  • Wenzel MA, Piertney SB (2014) Fine-scale population epigenetic structure in relation to gastrointestinal parasite load in red grouse (Lagopus lagopus scotica). Mol Ecol 23(17):4256–4273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whitfield PE, Gardner T, Vives SP et al (2002) Biological invasion of the Indo-Pacific lionfish Pterois volitans along the Atlantic coast of North America. Mar Ecol Prog Ser 235:289–297

    Article  Google Scholar 

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Acknowledgements

We thank Salisbury University for providing funding for equipment. We are grateful to Matthew Murphy, Paul Swim, and Tyler Bowling for their assistance with the MS-AFLP procedure. Rosalind Ludovici and Derek Coss assisted with data analysis. We would also like to thank two anonymous reviewers for their input during the drafting of this work.

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Authors and Affiliations

  1. Department of Entomology, University of Kentucky, 1100 South Limestone, S-225 Ag Science Center North, Lexington, KY, 40546, USA

    Mark J. Garcia

  2. Department of Integrative Biology, University of Texas, Austin, TX, 78712, USA

    Sofía Rodríguez-Brenes & Michael J. Ryan

  3. Department of Biological Sciences, Salisbury University, 1101 Camden Ave., Salisbury, MD, 21801, USA

    Mark J. Garcia, Ashley Kobisk, Laurie Adler, Ryan C. Taylor & Kimberly L. Hunter

  4. Smithsonian Tropical Research Institute, Balboa Ancon, Panama

    Michael J. Ryan & Ryan C. Taylor

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  1. Mark J. Garcia
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  3. Ashley Kobisk
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  4. Laurie Adler
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Correspondence to Mark J. Garcia.

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Ethical standards

Handling and toe clipping were performed in accordance with The American Society of Ichthyology and Herpetologists’ “Guidelines for Use of Live Amphibians and Reptiles in Field and Laboratory Research.” All experiments were conducted under Salisbury University’s Institutional Care and Use Committee (IACUC Protocol # SU 0036).

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Garcia, M.J., Rodríguez-Brenes, S., Kobisk, A. et al. Epigenomic changes in the túngara frog (Physalaemus pustulosus): possible effects of introduced fungal pathogen and urbanization. Evol Ecol 33, 671–686 (2019). https://doi.org/10.1007/s10682-019-10001-8

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