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Genetic data reveal fine-scale ecological segregation between larval plethodontid salamanders in replicate contact zones

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Abstract

Contact zones present unique opportunities to investigate ecological divergence, reproductive barriers, and gene flow between species. The two-lined salamander (Eurycea bislineata) species complex is a group of semiaquatic plethodontid salamanders with a reticulate evolutionary history that reflects the reorganization of river drainage basins. Although evidence for widespread, ancient introgression suggests an absence of reproductive isolating mechanisms in the early evolutionary history of the group, modern contact zones reveal a broader diversity of outcomes—with some putative species pairs occurring in sympatry and others exhibiting narrow hybrid zones. Here, we used RADcap data to investigate gene flow and ecological divergence in replicate contact zones between two species in the Appalachian foothills. Our results demonstrate that gene flow between these species is absent or rare, and larvae show strong, fine-scale ecological segregation among riffles, runs, and pools in streams. These results reinforce the more ambiguous conclusions of previous studies that suggested the evolutionary distinctiveness of these two species and underscore the importance of ecological factors in shaping local distributions.

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Availability of data and material

All sequence reads are available from the NCBI SRA (PRJNA630450), and all other data files and results from analyses are available from the Dryad Digital Repository (https://doi.org/10.5061/dryad.brv15dv6s).

References

  • Alexandrino J, Baird SJ, Lawson L et al (2005) Strong selection against hybrids at a hybrid zone in the Ensatina ring species complex and its evolutionary implications. Evolution 59:1334–1347

    PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B et al (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Bayona-Vásquez NJ, Glenn TC, Kieran TJ et al (2019) Adapterama III: Quadruple-indexed, double/triple-enzyme RADseq libraries (2RAD/3RAD). PeerJ 7:e7724

    Article  PubMed  PubMed Central  Google Scholar 

  • Beugin MP, Gayet T, Pontier D et al (2018) A fast likelihood solution to the genetic clustering problem. Methods Ecol Evol 9:1006–1016

    Article  PubMed  PubMed Central  Google Scholar 

  • Camp CD, Marshall JL, Landau KR et al (2000) Sympatric occurrence of two species of the two-lined salamander (Eurycea bislineata) complex. Copeia 2000:572–578

    Article  Google Scholar 

  • Camp CD, Wooten JA, Corbet CM et al (2013) Ecological interactions between two broadly sympatric, cryptic species of dusky salamander (genus Desmognathus). Copeia 2013:499–506

    Article  Google Scholar 

  • Catchen J, Hohenlohe PA, Bassham S et al (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22:3124–3140

    Article  PubMed  PubMed Central  Google Scholar 

  • Chatfield MWH, Kozak KH, Fitzpatrick BM et al (2010) Patterns of differential introgression in a salamander hybrid zone: inferences from genetic data and ecological niche modelling. Mol Ecol 19:4265–4282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark L (2017) lvclark/R_genetics_conv: R_genetics_conv 1.1. Zenodo. Available from https://doi.org/10.5281/zenodo.846816 (accessed April 2020)

  • de Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886

    Article  PubMed  Google Scholar 

  • Devitt TJ, Baird SJ, Moritz C (2011) Asymmetric reproductive isolation between terminal forms of the salamander ring species Ensatina eschscholtzii revealed by fine-scale genetic analysis of a hybrid zone. BMC Evol Biol 11:245

    Article  PubMed  PubMed Central  Google Scholar 

  • Eaton DAR, Overcast I (2020) ipyrad: Interactive assembly and analysis of RADseq datasets. Bioinformatics 36:2592–2594

    Article  CAS  PubMed  Google Scholar 

  • Fitzpatrick B, Placyk J Jr, Niemiller ML et al (2008) Distinctiveness in the face of gene flow: hybridization between specialist and generalist gartersnakes. Mol Ecol 17:4107–4117

    Article  PubMed  Google Scholar 

  • Goodman SN (1999) Toward evidence-based medical statistics. 2: the bayes factor. Ann Intern Med 130:1005–1013

    Article  CAS  PubMed  Google Scholar 

  • Goudet J (2005) Hierfstat, a package for R to compute and test hierarchical F- statistics. Mol Ecol Notes 5:184–186

    Article  Google Scholar 

  • Guttman SI, Karlin AA (1986) Hybridization of cryptic species of two-lined salamanders (Eurycea bislineata complex). Copeia 1986:96–108

    Article  Google Scholar 

  • Hardin G (1960) The competitive exclusion principle. Science 131:1292–1297

    Article  CAS  PubMed  Google Scholar 

  • Harrison RG (1990) Hybrid zones: windows on evolutionary process. Oxford Surv Evol Biol 7:69–128

    Google Scholar 

  • Hewitt GM (1988) Hybrid zones—natural laboratories for evolutionary studies. Trends Ecol Evol 3:158–549167

    Article  CAS  PubMed  Google Scholar 

  • Highton R, Peabody RB (2000) Geographic protein variation and speciation in salamanders of the Plethodon jordani and Plethodon glutinosus complexes in the southern Appalachian Mountains with the description of four new species. In: Bruce RC, Jaeger RG, Houck LD (eds) The Biology of Plethodontid Salamanders. Springer, New York, pp 31–93

    Chapter  Google Scholar 

  • Hoffberg SL, Kieran TJ, Catchen JM et al (2016) RADcap: sequence capture of dual-digest RADseq libraries with identifiable duplicates and reduced missing data. Mol Ecol Res 16:1264–1278

    Article  CAS  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363

    Article  PubMed  Google Scholar 

  • Howell T, Switzer V (1953) Intergrades of the Two-Lined Salamander, Eurycea bislineata, in Georgia. Herpetologica 9:152

    Google Scholar 

  • Jacobs JF (1987) A preliminary investigation of geographic variation and systematics of the two-lined salamander, Eurycea bislineata (Green). Herpetologica 43:423–446

    Google Scholar 

  • Jaeger RG (1971) Competitive exclusion as a factor influencing the distributions of two species of terrestrial salamanders. Ecology 52:632–637

    Article  PubMed  Google Scholar 

  • Jockusch EL, Wake DB (2002) Falling apart and merging: diversification of slender salamanders (Plethodontidae: Batrachoseps) in the American West. Biol J Lin Soc 76:361–391

    Article  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 

  • Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773–795

    Article  Google Scholar 

  • Kozak KH (2003) Sexual isolation and courtship behavior in salamanders of the Eurycea bislineata species complex, with comments on the evolution of the mental gland and pheromone delivery behavior in the Plethodontidae. Southeast Nat 2:281–292

    Article  Google Scholar 

  • Kozak KH, Montanucci RR (2001) Genetic variation across a contact zone between montane and lowland forms of the two-lined salamander (Eurycea bislineata) species complex: a test of species limits. Copeia 2001:25–34

    Article  Google Scholar 

  • Kozak KH, Blaine RA, Larson A (2006) Gene lineages and eastern North American palaeodrainage basins: phylogeography and speciation in salamanders of the Eurycea bislineata species complex. Mol Ecol 15:191–207

    Article  CAS  PubMed  Google Scholar 

  • Kuchta SR, Parks DS, Mueller RL et al (2009) Closing the ring: historical biogeography of the salamander ring species Ensatina eschscholtzii. J Biogeogr 36:982–995

    Article  Google Scholar 

  • Linck E, Battey C (2019) Minor allele frequency thresholds strongly affect population structure inference with genomic datasets. Mol Ecol Res 19:639–647

    Article  CAS  Google Scholar 

  • MacArthur RH, Wilson EO (1967) The Theory of Island Biogeography. Princeton University Press, Princeton

    Google Scholar 

  • Marshall JL (2000). Alternative mechanisms of character divergence: theoretical and empirical consideration. Dissertation, University of Louisiana at Lafayette

  • Paradis E, Schliep K (2019) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528

    Article  CAS  PubMed  Google Scholar 

  • Petranka JW (1998) Salamanders of the United States and Canada. Smithsonian Institution Press, Washington DC

    Google Scholar 

  • Pierson TW (2019). Organization of genetic and reproductive behavioral diversity in the two-lined salamander (Eurycea bislineata) species complex. Dissertation, University of Tennessee Knoxville

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2019) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Sattler PW, Brophy TR (2019) Distribution, Hybridization, and Taxonomic Status of Two-lined Salamanders (Eurycea bislineata complex) in Virginia and West Virginia. Banisteria 52:28–36

    Google Scholar 

  • Sever DM, Dundee HA, Sullivan CD (1976) A new Eurycea (Amphibia: Plethodontidae) from southwestern North Carolina. Herpetologica 32:26–29

    Google Scholar 

  • Wake DB (2006) Problems with species: patterns and processes of species formation in salamanders. Ann Mo Bot Gard 93:8–23

    Article  Google Scholar 

  • Wake DB (2009) What salamanders have taught us about evolution. Annu Rev Ecol Evol Syst 40:333–352

    Article  Google Scholar 

  • Walls SC (2009) The role of climate in the dynamics of a hybrid zone in Appalachian salamanders. Glob Change Biol 15:1903–1910

    Article  Google Scholar 

  • Weisrock DW, Hime PM, Nunziata SO et al (2018) Surmounting the large-genome “problem” for genomic data generation in salamanders. In: Hohenlohe P, Rajora OP (eds) Population Genomics. Springer, New York, pp 1–28

    Google Scholar 

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Acknowledgements

We thank Ken Kozak for aiding with the initial sample collection for the design of RADcap loci and for general guidance throughout this research. We thank Natalia Bayona-Vásquez, Joel Corush, Allison Devault, Travis Glenn, and Troy Kieran for aid in experimental design and laboratory assistance. We thank Natalia Bayona-Vásquez, Cyndi Carter, Troy Kieran, and Alexander Miele for aid in the field.

Funding

Funding was provided by the North Carolina Herpetological Society and the University of Tennessee Knoxville’s Department of Ecology and Evolutionary Biology Research Funds, and TWP was supported by a National Science Foundation Graduate Research Fellowship (DGE-1452154).

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Authors and Affiliations

  1. Department of Ecology, Evolution, and Organismal Biology, Kennesaw State University, Kennesaw, GA, USA

    Todd W. Pierson

  2. Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN, USA

    Todd W. Pierson & Benjamin M. Fitzpatrick

  3. Department of Biology, Piedmont College, Demorest, GA, USA

    Carlos D. Camp

Authors
  1. Todd W. Pierson
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  2. Benjamin M. Fitzpatrick
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  3. Carlos D. Camp
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Contributions

All authors conceived of and designed the study and analyses. TWP and CDC collected data in the field. TWP conducted all laboratory work, analyzed data, and wrote the manuscript. All authors edited the manuscript and approved the final version.

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Correspondence to Todd W. Pierson.

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The authors declare no conflicts of interest or competing interests.

Ethical approval

This research was approved under an animal use protocol from the University of Tennessee Knoxville IACUC (#2482-0916), and collections were permitted by the Chattahoochee National Forest and in compliance with all local, state, and federal wildlife laws and regulations. The authors declare no conflicts of interest.

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Pierson, T.W., Fitzpatrick, B.M. & Camp, C.D. Genetic data reveal fine-scale ecological segregation between larval plethodontid salamanders in replicate contact zones. Evol Ecol 35, 309–322 (2021). https://doi.org/10.1007/s10682-020-10099-1

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