Skip to main content

Advertisement

SpringerLink
Log in

A panmictic fiddler crab from the coast of Brazil? Impact of divergent ocean currents and larval dispersal potential on genetic and morphological variation in Uca maracoani

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Marine species tend to exhibit relatively less population structuring than terrestrial species owing to fewer barriers to gene flow and increased connectivity resulting from greater dispersal abilities. Thus, in many cases, life history plays a more important role in phylogeography of marine taxa than do oceanographic features. Littoral species are of particular phylogeographic interest because they possess life histories that have both marine and terrestrial characteristics. This study evaluates the synergistic impact of divergent ocean currents and a high larval dispersal potential on the phylogeography of the fiddler crab, Uca maracoani, distributed along the coast of Brazil. Patterns of genetic variation were assessed with sequence data for a portion of the mitochondrial COI gene and AFLPs. Geometric morphometric techniques were used to evaluate morphological variation. Results revealed a lack of discernible genetic subdivision. However, geometric morphometrics showed statistically significant morphological differentiation. The absence of a clear phylogeographic pattern appears to be determined primarily by life history characteristics permitting a high level of connectivity. One, or a combination of several factors, may explain the incongruity between genetic and morphologic signatures, including phenotypic plasticity, incomplete lineage sorting, or recent and ongoing genetic divergence.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Avise JC (2009) Phylogeography: retrospect and prospect. J Biogeogr 36:3–15

    Article  Google Scholar 

  • Barber PH, Palumbi SR, Erdmann MV, Moosa MK (2000) Biogeography—a marine Wallace’s line? Nature 406:692–693

    Article  CAS  Google Scholar 

  • Beerli P (2006) Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 22:341–345

    Article  CAS  Google Scholar 

  • Beerli P (2009) How to use migrate or why are Markov chain Monte Carlo programs difficult to use? In: Bertorelle G, Bruford MW, Hauffe HC, Rizzoli A, Vernesi C (eds) Population genetics for animal conservation, vol 17., Conservation BiologyCambridge University Press, Cambridge, pp 42–79

    Google Scholar 

  • Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568

    Article  CAS  Google Scholar 

  • Bookstein FL (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, Cambridge

    Google Scholar 

  • Bowen BW, Bass AL, Muss A, Carlin J, Robertson DR (2006) Phylogeography of two Atlantic squirrel fishes (Family Holocentridae): exploring links between pelagic larval duration and population connectivity. Mar Biol 149:899–913

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) tcs: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  Google Scholar 

  • Cowen RK, Lwiza KMM, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: open or closed? Science 287:857–859

    Article  CAS  Google Scholar 

  • Crane J (1975) Fiddler crabs of the world: Ocypodidae: Genus Uca. Princeton University Press, Princeton

    Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Epifanio CE, Little KT, Rowe PM (1988) Dispersal and recruitment of fiddler crab larvae in the Delaware River estuary. Mar Ecol Prog Ser 43:181–188

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  • François O, Durand E (2010) Spatially explicit Bayesian clustering models in population genetics. Mol Ecol Resour 10:773–784

    Article  Google Scholar 

  • Fu Y-X, Li W-H (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    CAS  Google Scholar 

  • Galligan TH, Donnellan SC, Sulloway FJ, Fitch AJ, Bertozzi T, Kleindorfer S (2012) Panmixia supports divergence with gene flow in Darwin’s small ground finch. Geospiza fuligonosa, on Santa Cruz, Galápagos Islands 21:2106–2115

    Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  Google Scholar 

  • Hellberg ME, Burton RS, Neigel JE, Palumbi SR (2002) Genetic assessment of connectivity among marine populations. Bull Mar Sci 70:273–290

    Google Scholar 

  • Hopkins MJ, Thurman CL (2010) The geographic structure of morphological variation in eight species of fiddler crabs (Ocypodidae: genus Uca) from the eastern United States and Mexico. Biol J Linn Soc 100:248–270

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MrBayes: bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  CAS  Google Scholar 

  • Ituarte RB, D’Anatro A, Luppi TA, Ribeiro PD, Spivak ED, Iribarne OO, Lessa EP (2012) Population structure of the SW Atlantic estuarine crab Neohelice granulata throughout its range: a genetic and morphometric study. Estuaries and Oceans 35:1249–1260

    Article  CAS  Google Scholar 

  • Jensen JL, Bohonak AJ, Kelley ST (2005). Isolation by distance, web service. BMC Genetics 6: 13. v.3.23 http://ibdws.sdsu.edu/ Johnson WS, Allen DM (2005) Zooplankton of the Atlantic and Gulf coasts. Johns Hopkins University Press, Baltimore, Maryland

  • Kelly RP, Palumbi SR (2010) Genetic structure among 50 species of the Northeastern Pacific rocky intertidal community. PLoS ONE 5:e8594. doi:10.1371/journal.pone.0008594

    Article  Google Scholar 

  • Knowlton N, Weigt LA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proc R Soc B 265:2257–2263

    Article  Google Scholar 

  • Koch V, Wolff M, Diele K (2005) Comparative population dynamics of four fiddler crabs (Ocypodidae, genus Uca) from a North Brazilian mangrove ecosystem. Mar Ecol Prog Ser 291:177–188

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Melo GAS (1996) Manual de identificação dos Brachyura (caranguejos e siris) do litoral Brasileiro. Plêiade, São Paulo

    Google Scholar 

  • Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends Ecol Evol 20:685–692

    Article  Google Scholar 

  • Neethling M, Matthee CA, Bowie RCK, von der Heyden S (2008) Evidence for panmixia despite barriers to gene flow in the southern African endemic, Caffrogobius caffer (Teleostei: Gobiidae). BMC Evol Biol 8:325–333

    Article  Google Scholar 

  • Palumbi SR (1994) Genetic divergence, reproductive isolation and marine speciation. Annu Rev Ecol Syst 25:547–572

    Article  Google Scholar 

  • Peterson RG, Stramma L (1991) Upper-level circulation in the South Atlantic Ocean. Prog Oceanogr 26:1–73

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Rambaut A, Drummond AJ (2009) Tracer, version 1.5. Available from http://beast.bio.ed.ac.uk/Tracer

  • Rohlf FJ (1990) Rotational fit (Procrustes) methods. In: Rohlf FJ, Bookstein FL (eds) Proceedings of the Michigan morphometrics workshop, vol 2., University of Michigan Museum of Zoology Special PublicationAnn Arbor, MI, pp 227–236

    Google Scholar 

  • Rohlf FJ (2010) tpsDig2.16. Available from http://life.bio.sunysb.edu/morph/

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  Google Scholar 

  • Rosenberg MS (2001) The systematics and taxonomy of fiddler crabs: a phylogeny of the genus Uca. J Crust Biol 21:839–869

    Google Scholar 

  • Schneider B, Schmittner A (2006) Simulating the impact of the Panamanian seaway closure on ocean circulation, marine productivity and nutrient cycling. Earth Planet Sci Lett 246:367–380

    Article  CAS  Google Scholar 

  • Schubart CD, Diesel R, Hedges SB (1998) Rapid evolution to terrestrial life in Jamaican crabs. Nature 393:363–365

    Article  CAS  Google Scholar 

  • Shanks AL (2009) Pelagic larval duration and dispersal distance revisited. Biol Bull 216:373–385

    Google Scholar 

  • Sheets HD (2001–2007) Integrated morphometrics package. Canisius College, Buffalo, NY. Available from http://www2.canisius.edu/~sheets/morphsoft.html

  • Shulman MJ, Bermingham E (1995) Early life histories, ocean currents, and the population genetics of Caribbean reef fishes. Evolution 49:897–910

    Article  Google Scholar 

  • Silva IC, Mesquita N, Paula J (2010) Lack of population structure in the fiddler crab Uca annulipes along an East African latitudinal gradient: genetic and morphometric evidence. Mar Biol 157:1113–1126

    Article  Google Scholar 

  • Sotka EE (2012) Natural selection, larval dispersal, and the geography of phenotype in the sea. Integr Comp Biol 52:538–545

    Article  Google Scholar 

  • Spivak ED, Cuesta JA (2009) The effect of salinity on larval development of Uca tangeri (Eydoux, 1835) (Brachyura: Ocypodidae) and new findings of the zoeal morphology. Sci Mar 73:297–305

    Article  CAS  Google Scholar 

  • Swofford DL (2003) paup*: Phylogenetic analysis using parsimony (*and other methods), Version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  Google Scholar 

  • Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109

    Article  CAS  Google Scholar 

  • Teske PR, McQuaid CD, Froneman PW, Barker NP (2006) Impacts of marine biogeographic boundaries on phylogeographic patterns of three South African estuarine crustaceans. Mar Ecol Prog Ser 314:283–293

    Article  Google Scholar 

  • Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev 25:1–45

    Article  Google Scholar 

  • Thurman CL, Faria SC, McNamara JC (2013) The distribution of fiddler crabs (Uca) along the coast of Brazil: implications for biogeography of the western Atlantic Ocean. Mar Biodiversity Rec. doi:10.1017/S1755267212000942

    Google Scholar 

  • Vogt G, Huber M, Thiemann M, van den Boogaart G, Schmitz OJ, Schubart CD (2008) Production of different phenotypes from the same genotype in the same environment by developmental variation. J Exp Biol 211:510–523

    Article  CAS  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, Vandelee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP—a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    Article  CAS  Google Scholar 

  • Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55:2455–2469

    CAS  Google Scholar 

  • Weese DA, McLain DK, Pratt AE, Fang QQ (2009) Population structure of the Atlantic sand fiddler crab Uca pugilator along the eastern coast of US revealed by molecular data. Curr Zool 55:150–157

    Google Scholar 

  • Wilgenbusch JC, Warren DL, Swofford DL (2004) awty: A system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference. Available from http://ceb.csit.fsu.edu/awty

  • Young CM, Chia FS (1987) Abundance and distribution of pelagic larvae as Influenced by predation, behavior and hydrographic factors. In: Giese C, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates. Blackwell Scientific and the Boxwood Press, Palo Alto and Pacific Grove, pp 385–463

    Google Scholar 

  • Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2004) Geometric morphometrics for biologists. Elsevier Academic Press, New York

    Google Scholar 

  • Zeller KA, Jurgenson JE, El-Assiuty EM, Leslie JF (2000) Isozyme and amplified fragment length polymorphisms (AFLPs) from cephalosporium maydis in Egypt. Phytoparasitica 28:121–130

    Article  CAS  Google Scholar 

  • Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17:2107–2121

    Article  CAS  Google Scholar 

  • Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD Thesis, University of Texas, Austin

Download references

Acknowledgments

We graciously acknowledge the agencies and institutions that supported this research financially, logistically, and by providing permits: the University of Northern Iowa (UNI) Department of Biology Undergraduate Research Program; UNI Summer Undergraduate Research Program; the UNI College of Natural Sciences; the UNI Graduate College; the US Fish and Wildlife Service; the Fulbright Foundation; the University of Iowa Center for Global Regional Environmental Research; the Conselho Nacional de Desenvolvimento Científico e Tecnológico (Grants 300662/2009-2 to JCM, and 450320/2010-3 to JCM and CLT); the Fundação de Amparo à Pesquisa do Estado de São Paulo (Grant 2009/50799-0 to JCM and CLT); the Coordenadoria de Aperfeiçoamento de Pessoal de Ensino Superior; and the Centro de Biologia Marinha/USP at São Sebastião, SP. Specimen collection and export of tissues and extracted DNA were authorized by the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA, permits #2009/18559-1 and #2010/23976-1 to JCM). We also thank Dr. Gary and Myrna Floyd who kindly provided undergraduate financial support for A. C. Wieman; K. H. Fehlauer-Ale, L. C. Branco, and Samuel C. Faria (USP, Brazil) for assistance with initial DNA extractions and field work; K. Berge, S. Holmes and J. Woodin (UNI) for laboratory assistance; and A.R. Warwick (Florida State University) for comments on the manuscript.

Author information

Authors and Affiliations

  1. Department of Biology, University of Northern Iowa, McCollum Science Hall #144, Cedar Falls, IA, 50614-0421, USA

    A. C. Wieman, P. B. Berendzen, K. R. Hampton, J. Jang, J. Jurgenson & C. L. Thurman

  2. Departamento de Biologia, FFCLRP, Universidade de São Paulo, Ribeirão Prêto, SP, 14040-901, Brazil

    J. C. McNamara

  3. GeoZentrum Nordbayern, Universität Erlangen-Nürnberg, Loewenichstraße 28, 91054, Erlangen, Germany

    M. J. Hopkins

Authors
  1. A. C. Wieman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. B. Berendzen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. R. Hampton
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Jang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. J. Hopkins
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. Jurgenson
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. C. McNamara
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. C. L. Thurman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to A. C. Wieman or P. B. Berendzen.

Additional information

Communicated by C. Riginos.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wieman, A.C., Berendzen, P.B., Hampton, K.R. et al. A panmictic fiddler crab from the coast of Brazil? Impact of divergent ocean currents and larval dispersal potential on genetic and morphological variation in Uca maracoani . Mar Biol 161, 173–185 (2014). https://doi.org/10.1007/s00227-013-2327-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-013-2327-0

Keywords

Search

Navigation