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Type: Article
Published: 2023-03-30
Page range: 351-378
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Unraveling Siren (Caudata: Sirenidae) systematics and description of a small, seepage specialist

1Fish and Wildlife Research Institute, Florida Fish and Wildlife Conservation Commission, 1105 SW Williston Road, Gainesville, FL, USA.
1Fish and Wildlife Research Institute, Florida Fish and Wildlife Conservation Commission, 1105 SW Williston Road, Gainesville, FL, USA.
1Fish and Wildlife Research Institute, Florida Fish and Wildlife Conservation Commission, 1105 SW Williston Road, Gainesville, FL, USA.
Amphibia Sirenidae phylogeny Siren sphagnicola new species Gulf Coastal Plain

Abstract

For approximately four decades, scientists have known of the existence of several undescribed species of Siren in the southeastern United States Coastal Plain. One of these species, S. reticulata, was recently described, but a small, seepage-dwelling species has remained undescribed until now. To resolve outstanding questions concerning the phylogeny of Siren, we collected sequence and morphometric data from specimens across the range of Siren. We found S. lacertina and S. reticulata to represent strongly supported monophyletic groups, with S. reticulata having a sister relationship to all other Siren. Additionally, we found five distinct mtDNA lineages within what has been recognized as S. intermedia. Siren lacertina and type-locality S. intermedia (lineage A) are sister mtDNA lineages, whereas S. intermedia lineages B and C show a high level of mitogenomic divergence from type-locality S. intermedia. Analyses of two scnDNA loci revealed that S. lacertina is monophyletic but nested with low positional support in a clade including the three S. intermedia mtDNA lineages. Further study is needed to determine whether S. intermedia lineages A, B, and C represent distinct species or incompletely sorted lineages. We restrict the range of S. intermedia to the region from the Escambia and Perdido river drainages of Florida and Alabama eastward through Virginia (the combined ranges of lineages A, B, and C). We also elevate S. i. nettingi (lineage E) to species status and include the larger S. i. texana form in that taxon, generating a species that occurs from the Mobile Bay drainages westward through the Mississippi Basin and southwest into northeastern Mexico. Lastly, we describe a new miniature species, S. sphagnicola, that ranges from the Florida Parishes of Louisiana eastward to the westernmost tributary creeks of Choctawhatchee Bay in the western Florida panhandle.

 

References

  1. Bandelt, H., Forster, P. & Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16 (1), 37–48.https://doi.org/10.1093/oxfordjournals.molbev.a026036
    Barnes, D.H. (1826) An arrangement of the genera of batracian [sic] animals, with a description of the more remarkable species; including a monograph of the doubtful reptils [sic]. American Journal of Science and Arts, 11 (2), 268–297.
    Benjamani, Y. & Hochberg, Y. (1995) Controlling the False Discovery Rate: a Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society. Series B (Methodological), 57 (1), pp. 289–300.https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
    Bingham, R.E., Papenfuss, T.J., Lindstrand, L. & Wake, D.B. (2018) Phylogeography and species boundaries in the Hydromantes shastae complex, with description of two new species (Amphibia; Caudata; Plethodontidae). Bulletin of the Museum of Comparative Zoology, 161 (10), 403‒427.https://doi.org/10.3099/MCZ42.1
    Bonett, R.M., Trujano-Alvarez, A.L., Williams, M.J. & Timpe, E.K. (2013) Biogeography and body size shuffling of aquatic salamander communities on a shifting refuge. Proceedings of the Royal Society B: Biological Sciences, 280 (1758), 20130200.https://doi.org/10.1098/rspb.2013.0200
    Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C.-H., Xie, D., Suchard, M.A., Rambaut, A. & Drummond, A.J. (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 10 (4), e1003537. https://doi.org/10.1371/journal.pcbi.1003537
    Boyd, C. & Vickers, D.H. (1963) Distribution of some Mississippi amphibians and reptiles. Herpetologica, 19 (3), 202‒205.
    Caldwell, R.D. & Howell, W.M. (1966) Siren intermedia nettingi from Alabama. Herpetologica 22 (4), 310‒311.
    Cope, E.D. (1889) The Batrachia of North American. Bulletin of the United States National Museum, 1889, 1–525.https://doi.org/10.5962/bhl.title.38254
    Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) JModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9 (8), 772.https://doi.org/10.1038/nmeth.2109
    Drummond, A.J., Ho, S.Y.W., Phillips, M.J. & Rambaut, A. (2006) Relaxed phylogenetics and dating with confidence. PLoS Biology, 4 (5), e88.https://doi.org/10.1371/journal.pbio.0040088
    Dunn, E.R. (1923) The salamanders of the family Hynobiidae. Proceedings of the American Academy of Arts and Sciences, 58 (13), 445‒523.https://doi.org/10.2307/20026019
    Enge, K.M. (2005) Herpetofaunal drift-fence surveys of steephead ravines in the Florida panhandle. Southeastern Naturalist, 4 (4), 657–678.https://doi.org/10.1656/1528-7092(2005)004[0657:HDSOSR]2.0.CO;2
    ESRI (2015) ArcGIS Desktop: Release 10.3.1. Environmental Systems Research Institute, Redlands, California.
    Flores-Villela, O. & Brandon, R.A. (1992) Siren lacertina (Amphibia: Caudata) in northeastern Mexico and southern Texas. Annals of the Carnegie Museum, 61, 289–291.https://doi.org/10.5962/p.226656
    Gehlbach, F.R. & Kennedy, S.E. (1978) Population ecology of a highly productive aquatic salamander (Siren intermedia). Southwestern Naturalist, 23 (3), 423‒429.https://doi.org/10.2307/3670250
    Godley, J.S. (1980) Foraging ecology of the striped swamp snake, Regina alleni, in southern Florida. Ecological Monographs, 50 (4), 411–436.https://doi.org/10.2307/1942651
    Goin, C.J. (1942) Description of a new race of Siren intermedia Le Conte. Annals of the Carnegie Museum, 29, 211–217.https://doi.org/10.5962/p.215158
    Goin, C.J. (1957) Description of a new salamander of the genus Siren from the Rio Grande. Herpetologica, 13 (1), 37–42.https://doi.org/10.2307/1439392
    Graham, S.P., Kline, R., Steen, D.A. & Kelehear, C. (2018) Description of an extant salamander from the Gulf Coastal Plain of North America: the Reticulated Siren, Siren reticulata. PLoS One, 13 (12), e0207460. https://doi.org/10.1371/journal.pone.0207460.
    Gray, J.E. (1831) A synopsis of the species of the Class Reptilia. In: Griffith, E. & Pidgeon, E. (Ed.), The Animal Kingdom arranged in conformity with its organization, by the Baron Cuvier, member of the Institute of France, with additional descriptions of all the species hitherto named, and of many not before noticed. Volume the Ninth. The Class Reptilia arranged by the Baron Cuvier, with specific descriptions. Appendix. Whittaker Treacher, and Co. London, pp. 1–86 + 1–110 (Appendix), pls. 1–55.
    Guindon, S. & Gascuel, O. (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Systematic Biology, 52 (5), 696–704.https://doi.org/10.1080/10635150390235520
    Harlan, R. (1827) Genera of North American Reptilia, and a synopsis of the species. Journal of the Academy of Natural Sciences of Philadelphia, 5, 317–372.
    Harper, F. (1935) Records of amphibians in the southeastern states. The American Midland Naturalist, 16 (3), 275–310.https://doi.org/10.2307/2420030
    Hartig, F. (2021) DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models. R Package version 0.4.1. Available from: https://CRAN.R-project.org/package=DHARMa (accessed 14 March 2023)
    Heled, J. & Drummond, A.J. (2010) Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution, 27 (3), 570–580.https://doi.org/10.1093/molbev/msp274
    Highton, R. (1957) Correlating costal grooves with trunk vertebrae in salamanders. Copeia, 1957 (2), 107–109. https://doi.org/10.2307/1439396
    Highton, R., Bonett, R.M. & Jockusch, E.L. (2017) Caudata salamanders. In: Crother, B.I. (Ed.), Scientific and Standard English Names of Amphibians and Reptiles of North America North of Mexico, with Comments Regarding Confidence in our Understanding. Society for the Study of Amphibians and Reptiles Herpetological Circular No. 43. 8th Edition. Society for the Study of Amphibians and Reptiles, s.n., pp. 18‒30.
    Huang A. (2017) Mean-parametrized Conway-Maxwell-Poisson regression models for dispersed counts. Statistical Modelling, 17, 1‒22.https://doi.org/10.1177/1471082X17697749
    Irisarri, I., Baurain, D., Brinkmann, H., Delsuc, F., Sire, J.Y., Kupfer, A., Petersen, J., Jarek, M., Meyer, A., Vences, M. & Philippe, H. (2017) Phylotranscriptomic consolidation of the jawed vertebrate timetree. Nature Ecology and Evolution, 1 (9), 1370–1378. https://doi.org/10.1038/s41559-017-0240-5
    Kessing, B., Croom, H., Martin, A., McIntosh, C., McMillan, W.O. & Palumbi, S. (1989) The simple fool’s guide to PCR. Version 1.0. University of Hawaii, Honolulu, Hawaii, 43 pp.
    LaFortune, T.C. (2015) Species Identification and Habitat Assessment of the South Texas Siren. M.S. Thesis, University of Texas at Brownsville, Brownsville, Texas, 91 pp.
    Le Conte, J.E. (1828) Description of a new species of Siren. Annals of the Lyceum of Natural History of New York, 2 (1), 133‒134.https://doi.org/10.1111/j.1749-6632.1826.tb00242.x
    Leigh, J.W. & Bryant, D. (2015) PopART: full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6 (9), 1110–1116.https://doi.org/10.1111/2041-210X.12410
    Length, R. (2021) emmeans: Estimated Marginal Means, aka Lease-Squares Means. R package Version 1.6.1. Available from: https://CRAN.R-project.org/package=emmeans (accessed 14 March 2023)
    León, P. & Kezer, J. (1974) The chromosomes of Siren intermedia nettingi (Goin) and their significance to comparative salamander karyology. Herpetologica, 30 (1), 1–11. [http://www.jstor.org/stable/3891403]
    Licht, L.E. & Lowcock, L.A. (1991) Genome size and metabolic rate in salamanders. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 100 (1), 83‒92.https://doi.org/10.1016/0305-0491(91)90089-V
    Litvinchuk, S.N. & Borkin, L.J. (2003) Variation in number of trunk vertebrae and in count of costal grooves in salamanders of the family Hynobiidae. Contributions to Zoology, 72 (4), 195‒209.https://doi.org/10.1163/18759866-07204001
    Martof, B.S. (1973a) Siren intermedia Le Conte. Lesser Siren. Catalogue of American Amphibians and Reptiles, 127, 1–3.
    Martof, B.S. (1973b) Siren lacertina Linnaeus. Greater Siren. Catalogue of American Amphibians and Reptiles, 128, 1–2.
    Martof, B.S. (1974) Sirenidae. Sirens. Catalogue of American Amphibians and Reptiles, 151, 1–2.
    McDaniel, V.R. (1969) A Morphological Investigation of Sirens from Southern Texas. M.S. Thesis, Texas A & M University, College Station, Texas, 58 pp.
    Means, D.B. (1981) Steepheads: Florida’s little-known canyon lands. ENFO (Florida Conservation Foundation), 81 (6), 1–4.
    Means, D.B. (2000) Southeastern U.S. Coastal Plain habitats of the Plethodontidae: the importance of relief, ravines, and seepage. In: Bruce, R.C., Jaeger, R.J. & Houck, L.D. (Eds.), The Biology of Plethodontid Salamanders. Plenum, New York, New York, pp. 287–302.https://doi.org/10.1007/978-1-4615-4255-1_14
    Misawa, Y. (1989) The method of counting costal grooves. In: Matsui, M., Hikada, T. & Goris, R.C. (Eds.), Current Herpetology in East Asia. Proceedings of the Second Japan-China Herpetological Symposium, Kyoto, Japan, July 1988, pp. 129‒134.
    Moler, P.E. (1985) A new species of frog (Ranidae: Rana) from northwestern Florida. Copeia, 1985 (2), 379–383.https://doi.org/10.2307/1444847
    Moler, P.E. (2019a) Siren intermedia complex Barnes 1826, Lesser Siren. In: Krysko, K.L., Enge, K.M. & Moler, P.E. (Eds.), Amphibians and Reptiles of Florida. University of Florida Press, Gainesville, Florida, pp. 128‒130.
    Moler, P.E. (2019b) Pseudobranchus axanthus Nettingi and Goin 1942, Southern Dwarf Siren. In: Krysko, K.L., Enge, K.M. & Moler, P.E. (Eds.), Amphibians and Reptiles of Florida. University of Florida Press, Gainesville, Florida, pp. 124‒126.
    Moler, P.E. (2019c) Pseudobranchus striatus Barnes 1826, Northern Dwarf Siren. In: Krysko, K.L., Enge, K.M. & Moler, P.E. (Eds.), Amphibians and Reptiles of Florida. University of Florida Press, Gainesville, Florida, pp. 126‒128.
    Mosimann, J.E. & James, F.C. (1979) New statistical methods for allometry with application to Florida Red-winged Blackbirds. Evolution, 33 (1), 444‒459.https://doi.org/10.1111/j.1558-5646.1979.tb04697.x
    Noble, G.K. (1924) The “retrograde metamorphosis” of the Sirenidae: experiments on the functional activity of the thyroid of the perennibranchs. The Anatomical Record, 29, 100.
    Noble, G.K. & Marshall, B.C. (1932) The validity of Siren intermedia Le Conte, with observations on its life history. American Museum Novitates, 532, 1–17.
    Parmley, D. & Gaddis, G. (1999) Occurrence of Siren intermedia Le Conte (Amphibia: Caudata) in Central Georgia. Georgia Journal of Science, 57 (3), 192–198.
    Petranka, J.W. (1998) Salamanders of the United States and Canada. Smithsonian Institution Press, Washington, D.C., 597 pp.
    Powell, R., Conant, R. & Collins, J.T. (2016) Peterson Field Guide to Reptiles and Amphibians of Eastern and Central North America. Fourth edition. Houghton Mifflin Harcourt, Boston, Massachusetts, 512 pp.
    Powell, R., Collins, J.T. & Hooper, E.D. (2019) Key to the Herpetofauna of the Continental United States and Canada. 3rd Edition. University Press of Kansas, Lawrence, Kansas, 184 pp.
    Puillandre, N, Brouillet, S. & Achaz, G. (2021) ASAP: assemble species by automatic partitioning. Molecular Ecology Resources, 21 (2), 609–620. https://doi.org/10.1111/1755-0998.13281
    R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna. Available from: https://www.R-project.org/ (accessed 14 March 2023)
    Reinhard, S., Voitel, S. and Kupfer, A. (2013) External fertilisation and paternal care in the paedomorphic salamander Siren intermedia Barnes, 1826 (Urodela: Sirenidae). Zoologischer Anzeiger-A Journal of Comparative Zoology, 253 (1), 1–5.https://doi.org/10.1016/j.jcz.2013.06.002
    Roelants, K., Gower, D.J., Wilkinson, M., Loader, S.P., Biju, S.D., Guillaume, K., Moriau, L. & Bossuyt, F. (2007) Global patterns of diversification in the history of modern amphibians. Proceedings of the National Academy of Sciences of the United States of America, 104 (3), 887–892. https://doi.org/10.1073/pnas.0608378104
    Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J.C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S.E. & Sánchez-Gracia, A. (2017) DnaSP 6: DNA sequence polymorphism analysis of large datasets. Molecular Biology and Evolution, 34 (12), 3299–3302. https://doi.org/10.1093/molbev/msx248
    Schmidt, K.P. (1953) A Check List of North American Amphibians and Reptiles. 6th Edition. American Society of Ichthyologists and Herpetologists and University of Chicago Press Chicago, Illinois, 280 pp.
    Smith, H.M., Smith, R.B. & Sawin, H.L. (1975) The authorship and date of publication of Siren intermedia (Amphibia: Caudata). Great Basin Naturalist, 35 (1), 100–102.
    Sorensen, K. (2004) Population characteristics of Siren lacertina and Amphiuma means in North Florida. Southeastern Naturalist, 3 (2), 249–258.https://doi.org/10.1656/1528-7092(2004)003[0249:PCOSLA]2.0.CO;2
    Steinke, D., Salzburger, W., Vences, M. & Meyer, A. (2005) TaxI—a software tool for DNA barcoding using distance methods. Philosophical Transactions of the Royal Society B, 360, 1975–1980.https://doi.org/10.1098/rstb.2005.1729
    Strahler, A.N. (1964) Section 4-II. Geology. Part II. Quantitative geomorphology of drainage basins and channel networks. In: Te Chow, V. (Ed.), Handbook of Applied Hydrology. McGraw-Hill, New York, New York, pp. 39–76.
    Vences, M., Miralles, A., Brouillet, S., Ducasse, J., Fedosov, A., Kharchev, V., Kumari, S, Patmanidis, S., Puillandre, N., Scherz, M.D., Kostadinov, I. & Renner, S.S. (2021) iTaxoTools 0.1: kickstarting a specimen-based software toolkit for taxonomists. Megataxa, 6, 77‒92.https://doi.org/10.11646/megataxa.6.2.1
    Wahlgren, R. (2011) Carl Linnaeus and the Amphibia. Bibliotheca Herpetologica, 9 (1–2), 5–38
    Wray, K.P., Means, D.B. & Steppan, S.J. (2017) Revision of the Eurycea quadridigitata (Holbrook 1842) complex of dwarf salamanders (Caudata: Plethodontidae: Hemidactyliinae) with a description of two new species. Herpetological Monographs, 31 (1), 18‒46.https://doi.org/10.1655/HERPMONOGRAPHS-D-16-00011
    Zhang, P. & Wake, D.B. (2009) Higher-level salamander relationships and divergence dates inferred from complete mitochondrial genomes. Molecular Phylogenetics and Evolution, 53 (2), 492‒508.https://doi.org/10.1016/j.ympev.2009.07.010

  2.