Biogeography, phylogeny, and morphological evolution of central Texas cave and spring salamanders

BMC Evolutionary Biology

Paul T Chippindale⁴  Corey E Roelke⁴  Andrew G Gluesenkamp³  Jesse M Meik²  Nathan F Bendik¹ 

[1] City of Austin, Watershed Protection Department, Austin, Texas 78704, USA;Department of Biological Sciences, Tarleton State University, Stephenville, Texas 76402, USA;Texas Parks and Wildlife Department, Austin, Texas 78744, USA;Department of Biology, University of Texas at Arlington, Arlington, Texas 76019, USA

关键词: Troglomorphism;    Morphological evolution;    Cave adaptation;    Troglobites;    Salamanders;    Blepsimolge;    Eurycea;   

Others  :  1086083
DOI  :  10.1186/1471-2148-13-201

 received in 2013-04-03, accepted in 2013-09-12,  发布年份 2013

【 摘 要 】

Background

Subterranean faunal radiations can result in complex patterns of morphological divergence involving both convergent or parallel phenotypic evolution and cryptic species diversity. Salamanders of the genus Eurycea in central Texas provide a particularly challenging example with respect to phylogeny reconstruction, biogeography and taxonomy. These predominantly aquatic species inhabit karst limestone aquifers and spring outflows, and exhibit a wide range of morphological and genetic variation. We extensively sampled spring and cave populations of six Eurycea species within this group (eastern Blepsimolge clade), to reconstruct their phylogenetic and biogeographic history using mtDNA and examine patterns and origins of cave- and surface-associated morphological variation.

Results

Genetic divergence is generally low, and many populations share ancestral haplotypes and/or show evidence of introgression. This pattern likely indicates a recent radiation coupled with a complex history of intermittent connections within the aquatic karst system. Cave populations that exhibit the most extreme troglobitic morphologies show no or very low divergence from surface populations and are geographically interspersed among them, suggesting multiple instances of rapid, parallel phenotypic evolution. Morphological variation is diffuse among cave populations; this is in contrast to surface populations, which form a tight cluster in morphospace. Unexpectedly, our analyses reveal two distinct and previously unrecognized morphological groups encompassing multiple species that are not correlated with spring or cave habitat, phylogeny or geography, and may be due to developmental plasticity.

Conclusions

The evolutionary history of this group of spring- and cave-dwelling salamanders reflects patterns of intermittent isolation and gene flow influenced by complex hydrogeologic dynamics that are characteristic of karst regions. Shallow genetic divergences among several species, evidence of genetic exchange, and nested relationships across morphologically disparate cave and spring forms suggests that cave invasion was recent and many troglobitic morphologies arose independently. These patterns are consistent with an adaptive-shift hypothesis of divergence, which has been proposed to explain diversification in other karst fauna. While cave and surface forms often do not appear to be genetically isolated, morphological diversity within and among populations may be maintained by developmental plasticity, selection, or a combination thereof.

【 授权许可】

   
2013 Bendik et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 6.

Figure 4.

Figure 5.

Figure 6.

【 参考文献 】

• [1]Wilkens H, Strecker U: Convergent evolution of the cavefish Astyanax (Characidae, Teleostei): genetic evidence from reduced eye‒size and pigmentation. Biol J Linn Soc Lond 2003, 80:545-554.
• [2]Xiao H, Chen S, Liu Z, Zhang R, Li W, Zan R, Zhang Y: Molecular phylogeny of Sinocyclocheilus (Cypriniformes: Cyprinidae) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 2005, 36:67-77.
• [3]Derkarabetian S, Steinmann DB, Hedin M: Repeated and time-correlated morphological convergence in cave-dwelling harvestmen (Opiliones, Laniatores) from montane western North America. PLoS ONE 2010, 5:e10388.
• [4]Culver DC, Kane TC, Fong DW: Adaptation and Natural Selection in Caves: The Evolution of Gammarus minus. Cambridge: Harvard University Press; 1995.
• [5]Strecker U, Bernatchez L, Wilkens H: Genetic divergence between cave and surface populations of Astyanax in Mexico (Characidae, Teleostei). Mol Ecol 2003, 12:699-710.
• [6]Bradic M, Beerli P, León FJG, Esquivel-Bobadilla S, Borowsky RL: Gene flow and population structure in the Mexican blind cavefish complex (Astyanax mexicanus). BMC Evol Biol 2012, 12:9. BioMed Central Full Text
• [7]Paquin P, Hedin M: The power and perils of “molecular taxonomy”: a case study of eyeless and endangered Cicurina (Araneae: Dictynidae) from Texas caves. Mol Ecol 2004, 13:3239-3255.
• [8]Juan C, Guzik MT, Jaume D, Cooper SJB: Evolution in caves: Darwin’s “wrecks of ancient life” in the molecular era. Mol Ecol 2010, 19:3865-3880.
• [9]Reddell JR: The cave fauna of Texas with special reference to the western Edwards Plateau. Huntsville: National Speleological Society; 1994:31-50. [The Caves and Karst of Texas. A Guidebook for the 1994 Convention of the National Speleological Society with Emphasis on the Southwestern Edwards Plateau]
• [10]Chippindale PT, Price AH, Wiens JJ, Hillis DM: Phylogenetic relationships and systematic revision of central Texas hemidactyliine plethodontid salamanders. Herpetol Monogr 2000, 14:1-80.
• [11]Potter FE, Sweet SS: Generic boundaries in Texas cave salamanders, and a redescription of Typhlomolge robusta (Amphibia: Plethodontidae). Copeia 1981, 1981:64-75.
• [12]Sweet SS: Natural metamorphosis in Eurycea neotenes, and the generic allocation of the Texas Eurycea (Amphibia: Plethodontidae). Herpetologica 1977, 33:364-375.
• [13]Sweet SS: A distributional analysis of epigean populations of Eurycea neotenes in central Texas, with comments on the origin of troglobitic populations. Herpetologica 1982, 38:430-444.
• [14]Mitchell RW, Reddell JR: Eurycea tridentifera, a new species of troglobitic salamander from Texas and a reclassification of Typhlomolge rathbuni. Tex J Sci 1965, 17:12-27.
• [15]Bowles BD, Sanders MS, Hansen RS: Ecology of the Jollyville Plateau salamander (Eurycea tonkawae: Plethodontidae) with an assessment of the potential effects of urbanization. Hydrobiologia 2006, 553:111-120.
• [16]Chippindale PT, Price AH: Conservation of Texas spring and cave salamanders (Eurycea). In Amphibian Declines: The Conservation Status of United States Species. Edited by Berkeley LM. Los Angeles: University of California Press; 2005:193-197.
• [17]Wiens JJ, Chippindale PT, Hillis DM: When are phylogenetic analyses misled by convergence? A case study in Texas cave salamanders. Syst Biol 2003, 52:501-514.
• [18]Mitchell RW, Smith RE: Some aspects of the osteology and evolution of the neotenic spring and cave salamanders (Eurycea, Plethodontidae) of central Texas. Tex J Sci 1972, 23:343-362.
• [19]Sweet SS: On the status of Eurycea pterophila (Amphibia: Plethodontidae). Herpetologica 1978, 34:101-108.
• [20]Chippindale PT: Species boundaries and species diversity in the central Texas hemidactyliine plethodontid salamanders, genus Eurycea. In The Biology of Plethodontid Salamanders. Edited by Bruce RC, Jaeger R, Houck LD. New York: Kluwer Academic/Plenum Publishers; 2000:149-165.
• [21]Hillis DM, Chamberlain DA, Wilcox TP, Chippindale PT: A new species of subterranean blind salamander (Plethodontidae: Hemidactyliini: Eurycea: Typhlomolge) from Austin, Texas, and a systematic revision of central Texas paedomorphic salamanders. Herpetologica 2001, 57:266-280.
• [22]Sweet SS: Secondary contact and hybridization in the Texas cave salamanders Eurycea neotenes and E. tridentifera. Copeia 1984, 1984:428-441.
• [23]Cantino PD, de Queiroz K: Phylocode. http://www.ohio.edu/phylocode webcite
• [24]Wiens JJ, Engstrom TN, Chippindale PT: Rapid diversification, incomplete isolation, and the “speciation clock” in North American salamanders (genus Plethodon): testing the hybrid swarm hypothesis of rapid radiation. Evolution 2006, 60:2585-2603.
• [25]Hillis DM, Mable BK, Larson A, Davis SK, Zimmer EA: Nucleic acids IV: sequencing and cloning. In Molecular Systematics. 2nd edition. Edited by Hillis DM, Moritz C, Mable BK. Sunderland: Sinauer Associates; 1996:321-381.
• [26]Walsh PS, Metzger DA, Higuchi R: Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 1991, 10:506-513.
• [27]Moritz C, Schneider CJ, Wake DB: Evolutionary relationships within the Ensatina eschscholtzii complex confirm the ring species interpretation. Syst Biol 1992, 41:273-291.
• [28]Vences M, Thomas M, Bonett RM, Vieites DR: Deciphering amphibian diversity through DNA barcoding: chances and challenges. Philos Trans R Soc Lond B Biol Sci 2005, 360:1859-1868.
• [29]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
• [30]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797.
• [31]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
• [32]Miller MA, Pfeiffer W, Schwartz T: Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Washington DC, USA: IEEE; 2010:1-8. [2010 Gateway Computing Environments Workshop: 14 November 2010; New Orleans]
• [33]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
• [34]Posada D: jModelTest: phylogenetic model averaging. Mol Biol Evol 2008, 25:1253-1256.
• [35]Marshall DC: Cryptic failure of partitioned Bayesian phylogenetic analyses: lost in the land of long trees. Syst Biol 2010, 59:108-117.
• [36]Rambaut A, Drummond AJ: Tracer v1.5. 2009. http://tree.bio.ed.ac.uk/software/tracer/ webcite [Accessed March 12 2013]
• [37]Marroig G: When size makes a difference: allometry, life-history and morphological evolution of capuchins (Cebus) and squirrels (Saimiri) monkeys (Cebinae, Platyrrhini). BMC Evol Biol 2007, 7:20. BioMed Central Full Text
• [38]McCoy MW, Bolker BM, Osenberg CW, Miner BG, Vonesh JR: Size correction: comparing morphological traits among populations and environments. Oecologia 2006, 148:547-554.
• [39]Adams DC, Rohlf FJ, Slice DE: Geometric morphometrics: ten years of progress following the “revolution. Italian Journal of Zoology 2004, 71:5-16.
• [40]Bishop SC, Wright M: A new neotenic salamander from Texas. Proc Biol Soc Wash 1937, 50:141-144.
• [41]Chippindale PT: Status of newly discovered cave and spring salamanders (Eurycea) in southern Travis and northern Hays Counties. Austin, Texas: Texas Parks and Wildlife Department; 2012:31.
• [42]Johnson S, Schindel G, Veni G, Hauwert N, Hunt B, Smith B, Gary M: Tracing groundwater flowpaths in the vicinity of San Marcos Springs, Texas. San Antonio, Texas: Edwards Aquifer Authority; 2012:139.
• [43]Lucas L, Gompert Z, Ott J, Nice C: Geographic and genetic isolation in spring-associated Eurycea salamanders endemic to the Edwards Plateau region of Texas. Conserv Genet 2009, 10:1309-1319.
• [44]Chippindale PT, Price AH, Hillis DM: Systematic status of the San Marcos salamander, Eurycea nana (Caudata: Plethodontidae). Copeia 1998, 1998:1046-1049.
• [45]Chippindale PT, Price AH, Hillis DM: A new species of perennibranchiate salamander (Eurycea: Plethodontidae) from Austin, Texas. Herpetologica 1993, 49:248-259.
• [46]Andrews F, Schertz T, Slade RJ, Rawson J: Effects of storm-water runoff on water quality of the Edwards Aquifer near Austin, Texas. Water-Resources Investigations Report. Austin, Texa: United States Geological Survey; 1984:50.
• [47]Hauwert NM: Groundwater flow and recharge within the Barton Springs Segment of the Edwards Aquifer, southern Travis and northern Hays Counties, Texas. The University of Texas at Austin: Department of Geological Sciences; 2009. [PhD thesis]
• [48]Veni G: Geomorphology, hydrology, geochemistry, and evolution of the karstic lower Glen Rose aquifer, south-central Texas. The Pennsylvania State University: Department of Geosciences; 1994. [PhD thesis]
• [49]Bendik NF, Gluesenkamp AG: Body length shrinkage in an endangered amphibian is associated with drought. J Zool 2013, 290:35-41.
• [50]Protas M, Conrad M, Gross JB, Tabin C, Borowsky R: Regressive evolution in the Mexican cave tetra, Astyanax mexicanus. Curr Biol 2007, 17:452-454.
• [51]Yamamoto Y, Byerly MS, Jackman WR, Jeffery WR: Pleiotropic functions of embryonic sonic hedgehog expression link jaw and taste bud amplification with eye loss during cavefish evolution. Dev Biol 2009, 330:200-211.
• [52]Niemiller ML, Poulson TL: Subterranean fishes of North America: Amblyopsidae. In Biology of Subterranean Fishes. Edited by Trajano E, Bichuette ME, Kapoor BG. Enfield: Science Publishers; 2010:169-280.
• [53]Badyaev AV: Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends Ecol Evol 2002, 17:369-378.
• [54]Gluesenkamp AG, Acosta N: Sexual dimorphism in Osornophryne guacamayo with notes on natural history and reproduction in the species. J Herpetol 2001, 35:148-151.
• [55]West-Eberhard MJ: Developmental Plasticity and Evolution. 1st edition. New York: Oxford University Press; 2003.
• [56]Cooke J, Zeeman EC: A clock and wavefront model for control of the number of repeated structures during animal morphogenesis. J Theor Biol 1976, 58:455-476.
• [57]Gomez C, Özbudak EM, Wunderlich J, Baumann D, Lewis J, Pourquié O: Control of segment number in vertebrate embryos. Nature 2008, 454:335-339.
• [58]Müller J, Scheyer TM, Head JJ, Barrett PM, Werneburg I, Ericson PGP, Pol D, Sánchez-Villagra MR: Homeotic effects, somitogenesis and the evolution of vertebral numbers in recent and fossil amniotes. Proc Natl Acad Sci USA 2010, 107:2118-2123.
• [59]Adams DC: Quantitative genetics and evolution of head shape in Plethodon salamanders. Evol Biol 2011, 38:278-286.
• [60]Wake DB: Comparative osteology and evolution of the lungless salamanders, family Plethodontidae. Memoirs of the Southern California Academy of Sciences 1966, 4:1-111.
• [61]Sweet SS: Eurycea tridentifera. Catalogue of American Amphibians and Reptiles 1977, 199:1-199.
• [62]Smith HM, Potter FE Jr: A third neotenic salamander of the genus Eurycea from Texas. Herpetologica 1946, 3:105-109.
• [63]Burger W, Smith HM, Floyd E: Potter: Another neotenic Eurycea from the Edwards Plateau . Proceedings of the Biological Society of Washington, D.C. 1950, 63:51-57.
• [64]Shaw KL: Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation: what mtDNA reveals and conceals about modes of speciation in Hawaiian crickets. Proc Natl Acad Sci USA 2002, 99:16122-16127.
• [65]Fisher-Reid MC, Wiens JJ: What are the consequences of combining nuclear and mitochondrial data for phylogenetic analysis? Lessons from Plethodon salamanders and 13 other vertebrate clades. BMC Evol Biol 2011, 11:300. BioMed Central Full Text
• [66]Leaché AD: Species trees for spiny lizards (genus Sceloporus): identifying points of concordance and conflict between nuclear and mitochondrial data. Mol Phylogenet Evol 2010, 54:162-171.
• [67]Desutter-Grandcolas L, Grandcolas P: The evolution toward troglobitic life: a phylogenetic reappraisal of climatic relict and local habitat shift hypotheses. Mémoires de Biospléologie 1996, 23:57-63.
• [68]Howarth FG: The evolution of non-relictual tropical troglobites. Int J Speleol 1987, 16:1-16.
• [69]Rivera MAJ, Howarth FG, Taiti S, Roderick GK: Evolution in Hawaiian cave-adapted isopods (Oniscidea: Philosciidae): vicariant speciation or adaptive shifts? Mol Phylogenet Evol 2002, 25:1-9.
• [70]Peck, Finston TL: Galapagos Islands troglobites: the questions of tropical troglobites, parapatric distributions with eyed-sister-species, and their origin by parapatric speciation. Mémoires de Biospléologie 1993, 20:19-37.
• [71]Howarth F: High-stress subterranean habitats and evolutionary change in cave-inhabiting arthropods. Am Nat 1993, 142:S65-S77.
• [72]Niemiller ML, Fitzpatrick BM, Miller BT: Recent divergence with gene flow in Tennessee cave salamanders (Plethodontidae: Gyrinophilus) inferred from gene genealogies. Mol Ecol 2008, 17:2258-2275.
• [73]Wiens JJ, Penkrot TA: Delimiting species using DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Syst Biol 2002, 51:69-91.
• [74]City of Austin: Biological Assessment Barton Springs Flood Debris Removal and Bypass Repairs, Austin, Texas. Austin, Texas: U.S. Army Corps of Engineers, Ft. Worth District Office; 2010.