Ecological and genetic divergence between two lineages of Middle American túngara frogs Physalaemus (= Engystomops) pustulosus

Springer Science and Business Media LLC - Tập 10 - Trang 1-18 - 2010
Heike Pröhl1,2,3, Santiago R Ron4, Michael J Ryan2,3
1Institute of Zoology, University of Veterinary Medicine Hannover, Germany
2Section of Integrative Biology, 1 University Station C09300, The University of Texas, USA
3Smithsonian Tropical Research Institute, Balboa Ancón, Republic of Panamá
4Museo de Zoología, Centro de Biodiversidad y Ambiente, Escuela de Biología, Pontificia Universidad Católica del Ecuador, Aptdo, Quito Ecuador

Tóm tắt

Uncovering how populations of a species differ genetically and ecologically is important for understanding evolutionary processes. Here we combine population genetic methods (microsatellites) with phylogenetic information (mtDNA) to define genetic population clusters of the wide-spread Neotropical túngara frog (Physalaemus pustulosus). We measure gene flow and migration within and between population clusters and compare genetic diversity between population clusters. By applying ecological niche modeling we determine whether the two most divergent genetic groups of the túngara frog (1) inhabit different habitats, and (2) are separated geographically by unsuitable habitat across a gap in the distribution. Most population structure is captured by dividing all sample localities into two allopatric genetic lineages. The Northern genetic lineage (NW Costa Rica) is genetically homogenous while the Southern lineage (SW Costa Rica and Panama) is sub-divided into three population clusters by both microsatellite and mtDNA analyses. Gene flow is higher within the Northern lineage than within the Southern lineage, perhaps due to increased landscape heterogeneity in the South. Niche modeling reveals differences in suitable habitat between the Northern and Southern lineages: the Northern lineage inhabits dry/pine-oak forests, while the Southern lineage is confined to tropical moist forests. Both lineages seem to have had little movement across the distribution gap, which persisted during the last glacial maximum. The lack of movement was more pronounced for the Southern lineage than for the Northern lineage. This study confirms the finding of previous studies that túngara frogs diverged into two allopatric genetic lineages north and south of the gap in the distribution in central Costa Rica several million years ago. The allopatric distribution is attributed to unsuitable habitat and probably other unknown ecological factors present across the distribution gap. Niche conservatism possibly contributes to preventing movements across the gap and gene flow between both groups. Genetic and ecological data indicate that there is the potential for ecological divergence in allopatry between lineages. In this context we discuss whether the Northern and Southern lineages should be recognized as separate species, and we conclude that further studies of pre- and post-zygotic isolation are needed for a final assessment. Identified population clusters should motivate future behavioral and ecological research regarding within-species biodiversity and speciation mechanisms.

Tài liệu tham khảo

Slatkin M: Gene flow in natural populations. Annu Rev Ecol Syst. 1985, 16: 393-430. 10.1146/annurev.ecolsys.16.1.393. Palo JU, Schmeller DS, Laurila A, Primmer CR, Kuzmin SL, Merila J: High degree of population subdivision in a widespread amphibian. Mol Ecol. 2004, 13 (9): 2631-2644. 10.1111/j.1365-294X.2004.02269.x. Funk WC, Blouin MS, Corn PS, Maxell BA, Pilliod DS, Amish S, Allendorf FW: Population structure of Columbia spotted frogs (Rana luteiventris) is strongly affected by the landscape. Mol Ecol. 2005, 14 (2): 483-496. 10.1111/j.1365-294X.2005.02426.x. Kraaijeveld-Smit FJL, Beebee TJC, Griffiths RA, Moore RD, Schley L: Low gene flow but high genetic diversity in the threatened Mallorcan midwife toad Alytes muletensis. Mol Ecol. 2005, 14 (11): 3307-3315. 10.1111/j.1365-294X.2005.02614.x. Wright S: Isolation by distance. Genetics. 1943, 28: 139-156. Hitchings SP, Beebee TJC: Genetic substructuring as a result of barriers to gene flow in urban Rana temporaria (common frog) populations: implications for biodiversity conservation. Heredity. 1997, 79: 117-127. 10.1038/hdy.1997.134. Spear SF, Peterson CR, Matocq MD, Storfer A: Landscape genetics of the blotched tiger salamander (Ambystoma tigrinum melanostictum). Mol Ecol. 2005, 14 (8): 2553-2564. 10.1111/j.1365-294X.2005.02573.x. Monsen KJ, Blouin MS: Extreme isolation by distance in a montane frog Rana cascadae. Conserv Genet. 2004, 5 (6): 827-835. 10.1007/s10592-004-1981-z. Rowe G, Beebee TJC, Burke T: A microsatellite analysis of natterjack toad, Bufo calamita, metapopulations. Oikos. 2000, 88 (3): 641-651. 10.1034/j.1600-0706.2000.880321.x. Waldmann B, McKinnon JS: Inbreeding and outbreeding in fishes, amphibians and reptiles. The natural history of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives. Edited by: Thornhill NW. 1993, Chicago: University of Chicago Press, 251-282. Stebbins RC, Cohen NW: A Natural History of Amphibians. 1995, New Jersey: Princeton University Press Newman RA, Squire T: Microsatellite variation and fine-scale population structure in the wood frog (Rana sylvatica). Mol Ecol. 2001, 10 (5): 1087-1100. 10.1046/j.1365-294X.2001.01255.x. Crawford AJ: Huge populations and old species of Costa Rican and Panamanian dirt frogs inferred from mitochondrial and nuclear gene sequences. Mol Ecol. 2003, 12 (10): 2525-2540. 10.1046/j.1365-294X.2003.01910.x. Leblois R, Rousset F, Tikel D, Moritz C, Estoup A: Absence of evidence for isolation by distance in an expanding cane toad (Bufo marinus) population: an individual-based analysis of microsatellite genotypes. Mol Ecol. 2000, 9 (11): 1905-1909. 10.1046/j.1365-294x.2000.01091.x. Edenhamn P, Hoggren M, Carlson A: Genetic diversity and fitness in peripheral and central populations of the European tree frog Hyla arborea. Hereditas. 2000, 133 (2): 115-122. 10.1111/j.1601-5223.2000.00115.x. Eales J, Thorpe RS, Malhotra A: Weak founder effect signal in a recent introduction of Caribbean Anolis. Mol Ecol. 2008, 17 (6): 1416-1426. 10.1111/j.1365-294X.2007.03684.x. Lougheed SC, Gascon C, Jones DA, Bogart JP, Boag PT: Ridges and rivers: a test of competing hypotheses of Amazonian diversification using a dart-poison frog (Epipedobates femoralis). Proc R Soc B-Biol Sci. 1999, 266 (1431): 1829-1835. 10.1098/rspb.1999.0853. Crawford AJ, Bermingham E, Polania C: The role of tropical dry forest as a long-term barrier to dispersal: a comparative phylogeographical analysis of dry forest tolerant and intolerant frogs. Mol Ecol. 2007, 16 (22): 4789-4807. 10.1111/j.1365-294X.2007.03524.x. deMaynadier PG, Hunter ML: Forest canopy closure and juvenile emigration by pool-breeding amphibians in Maine. J Wildl Manage. 1999, 63 (2): 441-450. 10.2307/3802629. Schluter D: Evidence for Ecological Speciation and Its Alternative. Science. 2009, 323 (5915): 737-741. 10.1126/science.1160006. Graham CH, Ron SR, Santos JC, Schneider CJ, Moritz C: Integrating phylogenetics and environmental niche models to explore speciation mechanisms in dendrobatid frogs. Evolution. 2004, 58 (8): 1781-1793. Gascon C, Lougheed SC, Bogart JP: Patterns of genetic population differentiation in four species of Amazonian frogs: A test of the riverine barrier hypothesis. Biotropica. 1998, 30 (1): 104-119. 10.1111/j.1744-7429.1998.tb00373.x. Robertson JM, Duryea MC, Zamudio KR: Discordant patterns of evolutionary differentiation in two Neotropical treefrogs. Mol Ecol. 2009, 18 (7): 1375-1395. 10.1111/j.1365-294X.2009.04126.x. Elmer KR, Davila JA, Lougheed SC: Cryptic diversity and deep divergence in an upper Amazonian leaflitter frog, Eleutherodactylus ockendeni. Bmc Evolutionary Biology. 2007, 7: 10.1186/1471-2148-7-247. Wang IJ, Crawford AJ, Bermingham E: Phylogeography of the Pygmy Rain Frog (Pristimantis ridens) across the lowland wet forests of isthmian Central America. Molecular Phylogenetics and Evolution. 2008, 47 (3): 992-1004. 10.1016/j.ympev.2008.02.021. Roberts JL, Brown JL, Schulte R, Arizabal W, Summers K: Rapid diversification of colouration among populations of a poison frog isolated on sky peninsulas in the central cordilleras of Peru. Journal of Biogeography. 2007, 34 (3): 417-426. 10.1111/j.1365-2699.2006.01621.x. Noonan BP, Gaucher P: Refugial isolation and secondary contact in the dyeing poison frog Dendrobates tinctorius. Mol Ecol. 2006, 15 (14): 4425-4435. 10.1111/j.1365-294X.2006.03074.x. Noonan BP, Wray KP: Neotropical diversification: the effects of a complex history on diversity within the poison frog genus Dendrobates. Journal of Biogeography. 2006, 33 (6): 1007-1020. 10.1111/j.1365-2699.2006.01483.x. Roberts JL, Brown JL, von May R, Arizabal W, Schulte R, Summers K: Genetic divergence and speciation in lowland and montane peruvian poison frogs. Molecular Phylogenetics and Evolution. 2006, 41 (1): 149-164. 10.1016/j.ympev.2006.05.005. Hagemann S, Pröhl H: Mitochondrial paraphyly in a polymorphic poison frog species (Dendrobatidae; D-pumilio). Molecular Phylogenetics and Evolution. 2007, 45 (2): 740-747. 10.1016/j.ympev.2007.06.010. Wiens JJ, Graham CH, Moen DS, Smith SA, Reeder TW: Evolutionary and ecological causes of the latitudinal diversity gradient in hylid frogs: Treefrog trees unearth the roots of high tropical diversity. American Naturalist. 2006, 168 (5): 579-596. 10.1086/507882. Ryan MJ, Rand AS, Weigt LA: Allozyme and advertisement call variation in the tungara frog, Physalaemus pustulosus. Evolution. 1996, 50 (6): 2435-2453. 10.2307/2410711. Lampert KP, Rand AS, Mueller UG, Ryan MJ: Fine-scale genetic pattern and evidence for sex-biased dispersal in the tungara frog, Physalaemus pustulosus. Mol Ecol. 2003, 12 (12): 3325-3334. 10.1046/j.1365-294X.2003.02016.x. Pröhl H, Koshy RA, Mueller U, Rand AS, Ryan MJ: Geographic variation of genetic and behavioral traits in northern and southern Tungara frogs. Evolution. 2006, 60 (8): 1669-1679. Weigt LA, Crawford AJ, Rand AS, Ryan MJ: Biogeography of the tungara frog, Physalaemus pustulosus: a molecular perspective. Mol Ecol. 2005, 14 (12): 3857-3876. 10.1111/j.1365-294X.2005.02707.x. Ryan MJ: Sexual selection, receiver biases, and the evolution of sex differences. Science. 1998, 281 (5385): 1999-2003. 10.1126/science.281.5385.1999. Ryan MJ, Rand AS: Sexual selection in female perceptual space: How female tungara frogs perceive and respond to complex population variation in acoustic mating signals. Evolution. 2003, 57 (11): 2608-2618. Coates AG, Obando JA: The geologic evolution of the Central American Istmus. Evolution and Environment in Tropical America. Edited by: Jackson JBC, Budd AF, Coates AG. 1996, Chicago, Illinois: University of Chicago Press, 21-56. Ron SR, Santos JC, Cannatella DC: Phylogeny of the tungara frog genus Engystomops (= Physalaemus pustulosus species group; Anura: Leptodactylidae). Mol Phylogenet Evol. 2006, 39 (2): 392-403. 10.1016/j.ympev.2005.11.022. Savage JM: The amphibians and reptiles of Costa Rica - A herpetofauna between two continents between two seas. 2002, Chicago: The University of Chicago Press Lampert KP, Bernal XE, Rand AS, Mueller UG, Ryan MJ: Island populations of Physalaemus pustulosus: History influences genetic diversity and morphology. Herpetologica. 2007, 63 (3): 311-319. 10.1655/0018-0831(2007)63[311:IPOPPH]2.0.CO;2. Marsh DM, Rand AS, Ryan MJ: Effects of inter-pond distance on the breeding ecology of tungara frogs. Oecologia. 2000, 122 (4): 505-513. 10.1007/s004420050973. Marsh DM, Fegraus EH, Harrison S: Effects of breeding pond isolation on the spatial and temporal dynamics of pond use by the tungara frog, Physalaemus pustulosus. J Anim Ecol. 1999, 68 (4): 804-814. 10.1046/j.1365-2656.1999.00332.x. The IUCN Red list of threatended species. [http://www.iucnredlist.org] Wiens JJ, Graham CH: Niche conservatism: Integrating evolution, ecology, and conservation biology. Annu Rev Ecol Evol Syst. 2005, 36: 519-539. 10.1146/annurev.ecolsys.36.102803.095431. Coyne J, Orr H: Speciation. 2004, Sunderland: Sinauer Associates Ryan MJ, Bernal XE, Rand AS: Patterns of mating call preferences in tungara frogs, Physalaemus pustulosus. J Evol Biol. 2007, 20 (6): 2235-2247. 10.1111/j.1420-9101.2007.01420.x. Coyne JA, Orr HA: Speciation. 2004, Sunderland: Sinauer Associates Höbel G, Gerhardt HC: Reproductive character displacement in the acoustic communication system of green tree frogs (Hyla cinerea). Evolution. 2003, 57 (4): 894-904. Wells KD: The ecology and behaviour of amphibians. 2007, Chicago: The University of Chicago Press Tárano Z, Ryan MJ: No pre-existing biases for heterospecific call traits in the frog Physalaemus enesefae. Anim Behav. 2002, 64: 599-607. 10.1006/anbe.2002.3080. Ron SR, Santos JC, Cannatella DC: Phylogeny of the túngara frog genus Engystomops (= Physalaemus pustulosus species group; Anura; Leptodactylidae). Mol Phylogenet Evol. 2006, 39: 392-403. 10.1016/j.ympev.2005.11.022. Pröhl H, Adams RMM, Mueller U, Rand S, Ryan MJ: Polymerase chain reaction primers for polymorphic microsatellite loci from the tungara frog Physalaemus pustulosus. Mol Ecol Notes. 2002, 2 (3): 341-343. 10.1046/j.1471-8286.2002.00240.x. Kalinowski ST: How many alleles per locus should be used to estimate genetic distances?. Heredity. 2002, 88: 62-65. 10.1038/sj.hdy.6800009. Moritz C, Schneider CJ, Wake DB: Evolutionary relationships within the Ensatina-eschscholtzii complex confirn the ring species interpretation. Syst Biol. 1992, 41 (3): 273-291. Goebel AM, Donnelly JM, Atz ME: PCR primers and amplification methods for 125 ribosomal DNA, the control region, cytochrome oxidase I, and cytochrome b in bufonids and other frogs, and an overview of PCR primers which have amplified DNA in amphibians successfully. Mol Phylogenet Evol. 1999, 11 (1): 163-199. 10.1006/mpev.1998.0538. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25 (24): 4876-4882. 10.1093/nar/25.24.4876. Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics. 2000, 155 (2): 945-959. Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005, 14 (8): 2611-2620. 10.1111/j.1365-294X.2005.02553.x. Documentation for STRUCTURE software: Version 2. [http://pritch.bsd.uchicago.edu] Falush D, Stephens M, Pritchard JK: Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics. 2003, 164 (4): 1567-1587. Weir BS, Cockerham CC: Estimating F-Statistics for the analysis of population structure. Evolution. 1984, 38 (6): 1358-1370. 10.2307/2408641. Slatkin M: A measure of population subdivision based on microsatellite allele fequencies. Genetics. 1995, 139 (1): 457-462. Schneider S, Roessli D, Excoffier L: Software for Population Genetic Data Analysis. 2000, Genetics and Biomatry Laboratory, Univ. of Geneva, Geneva Rannala B, Mountain JL: Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA. 1997, 94 (17): 9197-9201. 10.1073/pnas.94.17.9197. Paetkau D, Slade R, Burden M, Estoup A: Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol. 2004, 13 (1): 55-65. 10.1046/j.1365-294X.2004.02008.x. Canestrelli D, Verardi A, Nascetti G: Genetic differentiation and history of populations of the Italian treefrog Hyla intermedia: lack of concordance between mitochondrial and nuclear markers. Genetica. 2007, 130 (3): 241-255. 10.1007/s10709-006-9102-9. Ryan MJ: The túngara frog, a study in sexual selection and communication. 1985, Chicago: University of Chicago Press Petit RJ, ElMousadik A, Pons O: Identifying populations for conservation on the basis of genetic markers. Conserv Biol. 1998, 12 (4): 844-855. 10.1046/j.1523-1739.1998.96489.x. Smouse PE, Long JC, Sokal RR: Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Systematic Zoology. 1986, 35 (4): 627-632. 10.2307/2413122. Rousset F: Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics. 1997, 145 (4): 1219-1228. Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol. 2007, 24 (8): 1596-1599. 10.1093/molbev/msm092. Tamura K, Nei M: Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993, 10 (3): 512-526. Hasegawa M, Kishino H, Yano TA: Dating of the human ape splitting by a molecular clock of mitochondrial. J Mol Evol. 1985, 22 (2): 160-174. 10.1007/BF02101694. Austin JD, Lougheed SC, Moler PE, Boag PT: Phylogenetics, zoogeography, and the role of dispersal and vicariance in the evolution of the Rana catesbeiana (Anura: Ranidae) species group. Biol J Linnean Soc. 2003, 80 (4): 601-624. 10.1111/j.1095-8312.2003.00259.x. Hagemann S, Pröhl H: Mitochondrial paraphyly in a polymorphic poison frog species (Dendrobatidae; D.pumilio). Mol Phylogenet Evol. 2007, 45 (2): 740-747. 10.1016/j.ympev.2007.06.010. Mueller RL: Evolutionary rates, divergence dates, and the performance of mitochondrial genes in Bayesian phylogenetic analysis. Syst Biol. 2006, 55 (2): 289-300. 10.1080/10635150500541672. Macey JR, Schulte JA, Larson A, Fang ZL, Wang YZ, Tuniyev BS, Papenfuss TJ: Phylogenetic relationships of toads in the Bufo bufo species group from the eastern escarpment of the Tibetan Plateau: A case of vicariance and dispersal. Mol Phylogenet Evol. 1998, 9 (1): 80-87. 10.1006/mpev.1997.0440. Macey JR, Strasburg JL, Brisson JA, Vredenburg VT, Jennings M, Larson A: Molecular phylogenetics of western North American frogs of the Rana boylii species group. Mol Phylogenet Evol. 2001, 19 (1): 131-143. 10.1006/mpev.2000.0908. Tan AM, Wake DB: MtDNA phylogeography of the California newt, Taricha torosa (Caudata, salamandridae). Mol Phylogenet Evol. 1995, 4 (4): 383-394. 10.1006/mpev.1995.1036. Veith M, Kosuch J, Vences M: Climatic oscillations triggered post-Messinian speciation of Western Palearctic brown frogs (Amphibia, Ranidae). Mol Phylogenet Evol. 2003, 26 (2): 310-327. 10.1016/S1055-7903(02)00324-X. Elmer KR, Davila JA, Lougheed SC: Cryptic diversity and deep divergence in an upper Amazonian leaflitter frog, Eleutherodactylus ockendeni. BMC Evol Biol. 2007, 7: 14-10.1186/1471-2148-7-247. Clement M, Posada D, Crandall KA: TCS: a computer program to estimate gene genealogies. Mol Ecol. 2000, 9 (10): 1657-1659. 10.1046/j.1365-294x.2000.01020.x. Templeton AR, Crandall KA, Sing CF: Al cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. 3. Cladogram estimation. Genetics. 1992, 132 (2): 619-633. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R: DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 2003, 19 (18): 2496-2497. 10.1093/bioinformatics/btg359. Phillips SJ, Anderson RP, Schapire RE: Maximum entropy modeling of species geographic distributions. Ecol Model. 2006, 190 (3-4): 231-259. 10.1016/j.ecolmodel.2005.03.026. Elith J, Graham CH, Anderson RP, Dudik M, Ferrier S, Guisan A, Hijmans RJ, Huettmann F, Leathwick JR, Lehmann A, et al: Novel methods improve prediction of species' distributions from occurrence data. Ecography. 2006, 29 (2): 129-151. 10.1111/j.2006.0906-7590.04596.x. Hijmans RJ, Graham CH: The ability of climate envelope models to predict the effect of climate change on species distributions. Glob Change Biol. 2006, 12 (12): 2272-2281. 10.1111/j.1365-2486.2006.01256.x. Phillips SJ, Dudik M: Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography. 2008, 31 (2): 161-175. 10.1111/j.0906-7590.2008.5203.x. Maxtent software for species habitat modeling. [http://www.cs.princeton.edu/~schapire/maxent/] HerpNet. [http://www.herpnet.org/] Alexandria Digital Library Project. [http://www.alexandria.ucsb.edu] Ruegg KC, Hijmans RJ, Moritz C: Climate change and the origin of migratory pathways in the Swainson's thrush, Catharus ustulatus. J Biogeogr. 2006, 33 (7): 1172-1182. 10.1111/j.1365-2699.2006.01517.x. Drielsma M, Manion G, Ferrier S: The spatial links tool: Automated mapping of habitat linkages in variegated landscapes. Ecol Model. 2007, 200 (3-4): 403-411. 10.1016/j.ecolmodel.2006.08.017. Lin JP: A metric and GIS tool for measuring connectivity among habitat patches using least-cost distances. 2008, Vicksburg: US Army Engineer Research and Development Center