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The riverine thruway hypothesis: rivers as a key mediator of gene flow for the aquatic paradoxical frog Pseudis tocantins (Anura, Hylidae)

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Abstract

Context

Rivers, landscape, and climate can alter patterns of gene flow and consequently, shape intraspecific genetic variation. While rivers are predicted to halt gene flow in terrestrial species, they may facilitate migration for aquatic species. Amphibians are usually seen as water-dependent, yet multiple studies have indicated that rivers exert a barrier effect on these organisms.

Objectives

In this study, we investigated the effects of rivers and other abiotic factors, such as climate and geography on genetic variation of a highly aquatic frog (Pseudis tocantins) inhabiting central Brazil.

Methods

We sequenced fragments of one mitochondrial and two nuclear genes of 179 individuals of P. tocantins from 19 localities along the Tocantins-Araguaia Basin in Brazil and used Generalized Dissimilarity Modeling (GDM) to test the role of rivers, landscape, and climate features on its genetic differentiation. Next, we tested three scenarios of migration along the Tocantins-Araguaia Basin using approximate Bayesian computation (ABC).

Results

We found that genetic differentiation among localities is mostly explained by the influence of river connectivity. Conversely, elevation, slope, and past and current climate have little or no impact on genetic differentiation. Furthermore, our results show that patterns of migration took place directionally, from upstream to downstream sites.

Conclusions

Rivers have shaped patterns of intraspecific diversity in P. tocantins by acting as the most important facilitator of gene flow. Therefore, we suggest that future research should include the role of rivers as a facilitator of gene flow, especially for those species that are associated with aquatic environments.

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References

  • Anantharaman, R, Hall, K, Shah, V, Edelman, A (2019) Circuitscape in Julia: high performance connectivity modelling to support conservation decisions. ArXiv Preprint. http://arxiv.org/abs/1906.03542

  • Bartáková V, Richards M, Blazek R, Polacik M, Bryja J (2015) Terrestrial fishes: rivers are barriers to gene flow in annual fishes from the African savanna. J Biogeogr 18:1832–1844

    Article  Google Scholar 

  • Bruford MW, Hanotte O, Brookfield JFY, Burke T (1992) Single- locus and multilocus DNA fingerprint. In: Hoelzel AR (ed) Molecular genetic analysis of populations: a practical approach. IRL Press, Oxford, pp 225–270

  • Choueri EL, Gubili C, Borges SH, Thom G, Sawakuchi AO, Soares EAA, Ribas CC (2017) Phylogeography and population dynamics of Antbirds (Thamnophilidae) from Amazonian fluvial islands. J Biogeogr 44:2284–2294

    Article  Google Scholar 

  • Csilléry K, François O, Blum MGB (2012) abc: an R package for approximate Bayesian computation (ABC). Methods Ecol Evol 3:475–479

    Article  Google Scholar 

  • Downie JR, Sams K, Walsh PT (2009a) The paradoxical frog Pseudis paradoxa: larval anatomical characteristics, including gonadal maturation. Herpetol J 19:1–10

    Google Scholar 

  • Downie JR, Ramnarine I, Sams K, Walsh PT (2009b) The paradoxical frog Pseudis paradoxa: larval habitat, growth and metamorphosis. Herpetol J 19:11–19

    Google Scholar 

  • Duellman WE, Trueb L (1986) Biology of Amphibians. The Johns Hopkins University Press, Baltimore and London

    Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Emerson SB (1988) The giant tadpole of Pseudis paradoxa. Biol J Linnean Soc 34:93–104

    Article  Google Scholar 

  • Fabrezi M, Goldberg J (2009) Heterochrony during skeletal development of Pseudis platensis (Anura, Hylidae) and the early offset of skeleton development and growth. J Morphol 270:205–220

    Article  PubMed  Google Scholar 

  • Faivovich J, Haddad CFB, Garcia PCA, Frost DR, Campbell JA, Wheeler WC (2005) Systematic review of the frog family Hylidae, with special reference to Hylinae: phylogenetic analysis and taxonomic revision. Bull Am Mus Nat Hist 294:1–240

    Article  Google Scholar 

  • Ferrier S, Manion G, Elith J, Richardson K (2007) Using generalized dissimilarity modelling to analyse and predict patterns of beta diversity in regional biodiversity assessment. Divers Distrib 13:252–264

    Article  Google Scholar 

  • Fitzpatrick MC, Sanders NJ, Ferrier S, Longino JT, Weiser MD, Dunn R (2011) Forecasting the future of biodiversity: a test of single- and multi-species models for ants in North America. Ecography 34:836–847

    Article  Google Scholar 

  • Fouquet A, Courtois EA, Baudain D, Lima JD, Souza SM, Noonan BP, Rodrigues MT (2015) The trans-riverine genetic structure of 28 Amazonian frog species is dependent on life history. J Trop Ecol 31:361–373

    Article  Google Scholar 

  • Frost DR (2020) Amphibian Species of the World: an Online Reference Version 6.1 https://amphibiansoftheworld.amnh.org/index.php. Accessed 24 March 2020.

  • Funk WC, Caldwell JP, Peden CE, Padial JM, De la Riva I, Cannatella DC (2007) Tests of biogeographic hypotheses for diversification in the Amazonian forest frog, Physalaemus petersi. Mol Phylogenet Evol 44:825–837

    Article  PubMed  CAS  Google Scholar 

  • Garda AA, Cannatella DC (2007) Phylogeny and biogeography of paradoxical frogs (Anura, Hylidae, Pseudae) inferred from 12S and 16S mitochondrial DNA. Mol Phylogenet Evol 44:104–114

    Article  PubMed  CAS  Google Scholar 

  • Garda AA, Santana DJ, São-Pedro VA (2010) Taxonomic characterization of Paradoxical frogs (Anura, Hylidae, Pseudae): geographic distribution, external morphology, and morphometry. Zootaxa 2666:1–28

    Article  Google Scholar 

  • Gascon C, Lougheed SC, Bogart JP (1996) Genetic and morphological variation in Vanzolinius discodactylus: a direct test of the riverine barrier hypothesis. Biotropica 29:376–387

    Article  Google Scholar 

  • Gascon C, Lougheed SC, Bogart JP (1998) Patterns of genetic population differentiation in four species of Amazonian frogs: a test of the riverine barrier hypothesis. Biotropica 30:104–119

    Article  Google Scholar 

  • Gascon C, Malcolm JR, Patton JL, da Silva MNF, Bogart JP, Lougheed SC, Peres CA, Neckel S, Boag PT (2000) Riverine barriers and the geographic distributions of Amazonian species. Proc Natl Acad Sci USA 97:13672–13677

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gehara M, Mazzochinni GG, Burbrink F (2020) PipeMaster: inferring population divergence and demographic history with approximate Bayesian computation and supervised machine-learning in R. bioRxiv. https://doi.org/10.1101/2020.12.04.410670

    Article  Google Scholar 

  • Gehring PS, Pabijan M, Randrianirina JE, Glaw F, Vences M (2012) The influence of riverine barriers on phylogeographic patterns of Malagasy reed frogs (Heterixalus). Mol Phylogenet Evol 64:618–632

    Article  PubMed  Google Scholar 

  • Godinho MBC, da Silva FR (2018) The influence of riverine barriers, climate, and topography on the biogeographic regionalization of Amazonian anurans. Sci Rep 8:3427

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hayakawa EH, Rossetti DF (2015) Late quaternary dynamics in the Madeira river basin, southern Amazonia (Brazil), as revealed by paleomorphological analysis. An Acad Bras Ciênc 87:29–49

    Article  PubMed  Google Scholar 

  • Hijmans RJ, Elith J (2013) Species distribution modeling with R

  • Hijmans, RJ, van Etten J (2014) Raster: geographic analysis and modelling with raster data

  • Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Article  Google Scholar 

  • Hudson RR, Slatkin M, Maddison WP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132:583–589

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lanna FM, Gehara M, Werneck FP, Fonseca EM, Colli GR, Sites J Jr, Rodrigues MT, Garda AA (2020) Dwarf geckos and giant rivers: the role of the São Francisco River in the evolution of Lygodactylus klugei (Squamata: Gekkonidae) in the semi-arid Caatinga of north-eastern Brazil. Biol J Linnean Soc 129:88–98

    Article  Google Scholar 

  • Latrubesse EM, Stevaux JC (2002) Geomorphology and environmental aspects of the Araguaia fluvial basin, Brazil. Z Geomorphol 129:109–127

    Google Scholar 

  • Lawson LP (2013) Diversification in a biodiversity hot spot: landscape correlates of phylogeographic patterns in the African spotted reed frog. Mol Ecol 22:1947–1960

    Article  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  PubMed  CAS  Google Scholar 

  • Lima SMQ, Berbel-Filho WM, Araújo TFP, Lazzarotto H, Tatarenkov A, Avise JC (2017) Headwater capture evidenced by paleo-rivers reconstruction and population genetic structure of the armored catfish (Pareiorhaphis garbei) in the Serra do Mar Mountains of Southeastern Brazil. Front Genet 8:199

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lougheed SC, Gascon C, Jones DA, Bogart JP, Boag PT (1999) Ridges and rivers: a test of competing hypotheses of Amazonian diversification using a dart-poison frog (Epipedobates femoralis). Proc R Soc Lond B 1431:1829–1835

    Article  Google Scholar 

  • Lowe WH, Allendorf FW (2010) What can genetics tell us about population connectivity? Mol Ecol 19:3038–3051

    Article  PubMed  Google Scholar 

  • Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197

    Article  Google Scholar 

  • MMA (2006) Caderno da região hidrográfica do Tocantins-Araguaia. https://www.mma.gov.br/estruturas/161/_publicacao/161_publicacao02032011035943.pdf. Accessed 21 Sept 2020

  • Nazareno AG, Dick CW, Lohmann LG (2017) Wide but not impermeable: testing the riverine barrier hypothesis for an Amazonian plant species. Mol Ecol 26:3636–3648

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Neves MO, Morais CJS, Garda AA (2014) Sexual dimorphism and diet of Pseudis tocantins (Anura, Hylidae, Pseudae). South Am J Herpetol 9:177–182

    Article  Google Scholar 

  • Oliveira EF, Gehara M, São-Pedro VA, Chen X, Myers EA, Burbrink FT, Mesquita DO, Garda AA, Colli GR, Rodrigues MT, Arias FJ, Zaher H, Santos RML, Costa GC (2015) Speciation with gene flow in whiptail lizards from a Neotropical xeric biome. Mol Ecol 24:5957–5975

    Article  PubMed  Google Scholar 

  • Oliveira EF, Martinez PA, São-Pedro VA, Gehara M, Burbrink FT, Mesquita DO, Garda AA, Colli GR, Costa GC (2018) Climatic suitability, isolation by distance and river resistance explain genetic variation in a Brazilian whiptail lizard. Heredity 120:251–265

    Article  PubMed  Google Scholar 

  • Oliveira JA, Farias IP, Costa GC, Werneck FP (2019) Model-based riverscape genetics: disentangling the roles of local and connectivity factors in shaping spatial genetic patterns of two Amazonian turtles with different dispersal abilities. Evol Ecol 33:273–298

    Article  Google Scholar 

  • Pelletier TA, Carstens BC (2018) Geographical range size and latitude predict population genetic structure in a global survey. Biol Lett 14:20170566

    Article  PubMed  PubMed Central  Google Scholar 

  • Perron JT, Richardson PW, Ferrier KL, Lapôtre M (2012) The root of branching river networks. Nature 492:100–103

    Article  PubMed  CAS  Google Scholar 

  • Pfeifer B, Wittelsbürger U, Ramos-Onsins SE, Lercher MJ (2014) PopGenome: an efficient swiss army knife for population genomic analyses in R. Mol Biol Evol 31:1929–1936

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259

    Article  Google Scholar 

  • Pirani RM, Werneck FP, Thomaz AT, Kenney M, Sturaro MJ, Avila-Pires TCS, Rodrigues MT, Knowles LL (2019) Testing main Amazonian rivers as barriers across time and space within widespread taxa. J Biogeogr 46:2444–2456

    Article  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  PubMed  CAS  Google Scholar 

  • Richards-Zawacki CL (2009) Effects of slope and riparian habitat connectivity on gene flow in an endangered Panamanian frog, Atelopus varius. Divers Distrib 15:796–806

    Article  Google Scholar 

  • Roček Z, Böttcher R, Wassersug R (2006) Gigantism in tadpoles of the Neogene frog Palaeobatrachus. Paleobiology 32:666–675

    Article  Google Scholar 

  • Salzburger W, Ewing GB, Von Haeseler A (2011) The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Mol Ecol 20:1952–1963

    Article  PubMed  Google Scholar 

  • Satler JD, Carstens B (2016) Do ecological communities disperse across biogeographic barriers as a unit? Mol Ecol 26:3533–3545

    Article  Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thom G, Xue AT, Sawakuchi AO, Ribas CC, Hickerson MJ, Aleixo A, Miyaki C (2020) Quaternary climate changes as speciation drivers in the Amazon floodplains. Sci Adv 6:eaax4718

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thomaz AT, Christie MR, Knowles LL (2016) The architecture of river networks can drive the evolutionary dynamics of aquatic populations. Evolution 70:731–739

    Article  PubMed  Google Scholar 

  • Vasconcellos MM, Colli GR, Ortiz EM, Weber JN, Cannatella DC, Rodrigues MT (2019) Isolation by instability: historical climate change shapes population structure and genomic divergence of treefrogs in the Neotropical Cerrado savanna. Mol Ecol 28:1748–1764

    Article  PubMed  Google Scholar 

  • Wang IJ, Bradburd GS (2014) Isolation by environment. Mol Ecol 23:5649–5662

    Article  PubMed  Google Scholar 

  • Wallace AR (1852) On the monkeys of the Amazon. Proc Zool Soc Lond 20:107–110

    Google Scholar 

  • Wilkinson MJ, Marshall LG, Lundberg JG (2006) River behavior on megafans and potential influences on diversification and distribution of aquatic organisms. J S Am Earth Sci 21:151–172

    Article  Google Scholar 

  • Wollenberg VKC (2015) Evidence for an intrinsic factor promoting landscape genetic divergence in Madagascan leaf-litter frogs. Front Genet 6:155

    Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

We thank the two anonymous reviewers whose comments and suggestions helped improve and clarify this manuscript. EMF and RM (process #88881.170016/2018-1 and 1489596, respectively) thank Coordenação de Apoio à Formação de Pessoal de Nível Superior (CAPES) for their doctoral fellowships. AAG thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and CAPES for financial support.

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Authors and Affiliations

  1. Department of Evolution, Ecology, & Organismal Biology, The Ohio State University, Columbus, OH, USA

    Emanuel M. Fonseca & Flávia M. Lanna

  2. Museum of Biological Diversity, The Ohio State University, 1315 Kinnear Rd., Columbus, OH, 43212, USA

    Emanuel M. Fonseca & Flávia M. Lanna

  3. Departamento de Botânica e Zoologia, Centro de Biociências, Universidade Federal do Rio Grande do Norte, Lagoa Nova, Natal, RN, Brazil

    Adrian A. Garda

  4. Centro de Ciências Biológicas e da Saúde, Laboratório de Zoologia, Cidade Universitária, Universidade Federal de Mato Grosso Do Sul, Campo Grande, MS, Brazil

    Eliana F. Oliveira & Felipe Camurugi

  5. Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Centro de Ciências Exatas e da Natureza, Universidade Federal da Paraíba, João Pessoa, PB, Brazil

    Felipe Camurugi, Felipe de M. Magalhães & Ricardo Marques

  6. Instituto de Biología Subtropical (IBS), Universidad Nacional de Misiones (UNaM) - CONICET, Bertoni 85, Puerto Iguazú, Misiones, Argentina

    Juan Pablo Zurano

  7. Zoological Institute, Braunschweig University of Technology, Mendelssohnstr. 4, 38106, Braunschweig, Germany

    Miguel Vences

  8. Department of Earth and Environmental Sciences, Rutgers University-Newark, 195 University Ave, Newark, NJ, USA

    Marcelo Gehara

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  1. Emanuel M. Fonseca
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  2. Adrian A. Garda
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  3. Eliana F. Oliveira
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  4. Felipe Camurugi
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  5. Felipe de M. Magalhães
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  6. Flávia M. Lanna
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  9. Miguel Vences
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Correspondence to Adrian A. Garda.

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Fonseca, E.M., Garda, A.A., Oliveira, E.F. et al. The riverine thruway hypothesis: rivers as a key mediator of gene flow for the aquatic paradoxical frog Pseudis tocantins (Anura, Hylidae). Landscape Ecol 36, 3049–3060 (2021). https://doi.org/10.1007/s10980-021-01257-z

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