Skip to main content
SpringerLink
Log in

Integrating fossils and molecules to study cupuladriid evolution in an emerging Isthmus

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Fossils and genes represent two principal sources of data for studying evolutionary biology, but they are rarely unified. The aim of this paper is to integrate the fossil and molecular records of Tropical American cupuladriid bryozoans to elucidate their evolutionary history. Molecules and fossils broadly concur in determining the timing of species divergences, and point to seaway constriction associated with the emergence of the Isthmus of Panama as a driver of speciation. We discover that although cross-Isthmian isolation of taxa was important, strong isolating mechanisms also existed within the southwestern Caribbean (SWC), caused by increasing physical and environmental heterogeneity as inter-oceanic straits constricted in the Late Pliocene. During this time of rapid environmental change and instability, recently diverged species pairs existed in locally separated habitats for around 2 million years, only to co-exist after final closure of the seaway. This pattern is consistent with a model of allopatric speciation caused by local isolating mechanisms followed by secondary contact. Fossils also reveal the trajectories of reproductive life history and morphology during and after species divergences. In the SWC, all extant species started to shift from clonal to aclonal reproduction immediately in response to changing oceanographic conditions. However, it took another million years for colonies to gain skeletal strength, a trait that reduces cloning by fragmentation, suggesting that the appearance of advantageous traits was delayed by 1–2 million years and only arose after the process of allopatric speciation had run its course. Changes in colony shape, height and size also appear to lag 2 million years, but may reflect exploitation of the diverse sedimentary environments created as reefs proliferated at this time.

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

Notes

  1. C. sp. 14 is synonymous with C. sp. nov. ‘gigante’ in O’Dea et al. (2008) and O’Dea (2009).

References

  • Allmon WD (1992) Role of temperature and nutrients in extinction of Turritenlline gastropods-Cenozoic of the Northwestern Atlantic and Northeaster Pacific. Palaeogeogr Palaeoclimatol Palaeoecol 92:41–54

    Article  Google Scholar 

  • Allmon WD (2001) Nutrients, temperature, disturbance, and evolution: a model for the late Cenozoic marine record of the western Atlantic. Palaeogeogr Palaeoclimatol Palaeoecol 166:9–26

    Article  Google Scholar 

  • Arnaud S, Bonhomme F, Borsa P (1999) Mitochondrial DNA analysis of the genetic relationships among populations of scad mackerel (Decapterus macarellus, D. macrosoma, and D. russelli) in South-East Asia. Mar Biol 135:699–707

    Article  CAS  Google Scholar 

  • Barber P, Palumbi S, Erdmann M, Moosa M (2002) Sharp genetic breaks among populations of Haptosquilla pulchella (Stomatopoda) indicate limits to larval transport: patterns, causes, and consequences. Mol Ecol 11:659–674

    Article  PubMed  CAS  Google Scholar 

  • Bartoli G, Sarnthein M, Weinelt M, Erlenkeuser H, Garbe-Schˆnberg D, Lea D (2005) Final closure of Panama and the onset of northern hemisphere glaciation. Earth Planet Sci Lett 237:33–44

    Article  CAS  Google Scholar 

  • Benton MJ, Donoghue PC (2007) Paleontological evidence to date the tree of life. Mol Biol Evol 24:26–53

    Article  PubMed  CAS  Google Scholar 

  • Benton MJ, Pearson PN (2001) Speciation in the fossil record. Trends Ecol Evol 16:405–411

    Article  PubMed  Google Scholar 

  • Budd AF, Johnson KG (1999) Origination preceding extinction during late Cenozoic turnover of Caribbean reefs. Paleobiology 25:188–200

    Google Scholar 

  • Budd AF, Johnson KG, Stemann TA (1996) Plio-Pleistocene turnover and extinctions in the Caribbean reef coral fauna. In: Jackson JBC, Budd AF, Coates AG (eds) Evolution and environment in tropical America. The University of Chicago Press, Chicago, pp 168–204

    Google Scholar 

  • Cheetham AH, Jackson JBC (1996) Speciation, extinction, and the decline of arborescent growth in Neogene and Quaternary cheilostome Bryozoa of tropical America (In Jackson et al. 1996), pp 205–233

  • Cheetham A, Jackson J, Sanner J, Ventocilla Y (1999) Neogene cheilostome Bryozoa of tropical America: comparison and contrast between the Central American isthmus (Panama, Costa Rica) and North-Central Caribbean (Dominican Republic). Bull Am Paleontol 113:159–192

    Google Scholar 

  • Coates AG, Obando JA (1996) The geologic evolution of the Central American Isthmus. In: Jackson JBC, Budd AF, Coates AG (eds) Evolution and environment in tropical America. The University of Chicago Press, Chicago, pp 21–56

    Google Scholar 

  • Coates AG, Jackson JBC, Collins LS, Cronin TM, Dowsett HJ, Bybell LM, Jung P, Obando JA (1992) Closure of the Isthmus of Panama—the near-shore marine record of Costa Rica and western Panama. Geol Soc Am Bull 104:814–828

    Article  Google Scholar 

  • Coates AG, Aubry MP, Berggren WA, Collins LS, Kunk M (2003) Early neogene history of the Central American arc from Bocas del Toro, western Panama. Geol Soc Am Bull 115:271–287

    Article  Google Scholar 

  • Coates AG, Collins LS, Aubry MP, Berggren WA (2004) The geology of the Darien, Panama, and the late Miocene-Pliocene collision of the Panama arc with northwestern South America. Geol Soc Am Bull 116:1327–1344

    Article  Google Scholar 

  • Coates AG, McNeill DF, Aubry MP, Berggren WA, Collins LS (2005) An introduction to the geology of the Bocas del Toro archipelago, Panama. Caribb J Sci 41:374–391

    Google Scholar 

  • Collins LS (1996) Environmental changes in Caribbean shallow waters relative to the closing tropical American Seaway. In: Jackson JBC, Budd AF, Coates AG (eds) Evolution and environment in tropical America. The University of Chicago Press, Chicago, pp 130–167

    Google Scholar 

  • Collins LS, Coates AG, Jackson JBC, Obando JA (1995) Timing and rates of emergence of the Limon and Bocas del Toro Basins: Caribbean effects of Cocos Ridge subduction? Geol Soc Am Special Paper 295:263–289

    Google Scholar 

  • Collins LS, Budd AF, Coates AG (1996a) Earliest evolution associated with closure of the Tropical American Seaway. Proc Natl Acad Sci USA 93:6069–6072

    Article  PubMed  CAS  Google Scholar 

  • Collins LS, Coates AG, Berggren WA, Aubry MP, Zhang JJ (1996b) The late Miocene Panama Isthmian strait. Geology 24:687–690

    Article  Google Scholar 

  • Collins LS, Coates AG (eds) (1999) A paleobiotic survey of caribbean faunas from the neogene of the isthmus of panama. Bull Am Paleontol 357:351

    Google Scholar 

  • Cook PL (1963) Observations on live lunulitiform zoaria of Polyzoa. Cahiers de Biol Mar 4:407–413

    Google Scholar 

  • Cook PL, Chimonides PJ (1983) A short history of the Lunulite Bryozoa. B Mar Sci 33:566–581

    Google Scholar 

  • Cook PL, Chimonides PJ (1994) Notes on the family Cupuladriidae (Bryozoa), and on Cupuladria remota Sp-N from the Marquesas Islands. Zoologica Scripta 23:251–268

    Article  Google Scholar 

  • Dick MH (2008) Unexpectedly high diversity of Monoporella (Bryozoa; Cheilostomata) in the Aleutian Islands, Alaska: taxonomy and distribution of six new species. Zool Sci 1:36–52

    Article  Google Scholar 

  • Dick MH, Herrera-Cubilla A, Jackson JBC (2003) Molecular phylogeny and phylogeography of free-living Bryozoa (Cupuladriidae) from both sides of the Isthmus of Panama. Mol Phylogenet Evol 27:355–371

    Article  PubMed  CAS  Google Scholar 

  • Dick MH, Matawari SF, Sanner J, Grischenko AV (2011) Cribrimorph and other Cauloramphus species (Bryozoa; Cheilostomata) from the northwestern pacific. Zool Sci 2:134–147

    Article  Google Scholar 

  • Driscoll EG, Gibson JW, Mitchell WS (1971) Larval selection of substrate by Bryozoa Discoporella and Cupuladria. Hydrobiologia 37:347

    Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: bayesian evolutionary analysis by sampling trees. Bmc Evol Biol 7:214

    Article  PubMed  Google Scholar 

  • Duquecaro H (1990) Neogene stratigraphy, paleoceanography and paleobiogeography in Nothwest South-America and the evolution of the Panama seaway. Palaeogeogr Palaeoclimatol Palaeoecol 77:203–234

    Article  Google Scholar 

  • Fukami H, Budd AF, Paulay G, SolÈ-Cava A, Chen CA, Iwao K, Knowlton N (2004) Conventional taxonomy obscures deep divergence between Pacific and Atlantic corals. Nature 427:832–835

    Article  PubMed  CAS  Google Scholar 

  • Gavrilets S (2003) Perspective: models of speciation: what have we learned in 40 years? Evolution 57:2197–2215

    PubMed  Google Scholar 

  • Håkansson E, Thomsen E (2001) Asexual propagation in cheilostome Bryozoa: evolutionary trends in a major group of colonial animals. In: Jackson JBC, Lidgard S, McKinney FK (eds) Evolutionary patterns: growth, form and tempoin the fossil record. University of Chicago Press, Chicago, pp 326–347

    Google Scholar 

  • Haug GH, Tiedemann R (1998) Effect of the formation of the Isthmus of Panama on Atlantic Ocean thermohaline circulation. Nature 393:673–676

    Article  CAS  Google Scholar 

  • Herrera-Cubilla A, Dick MH, Sanner J, Jackson JBC (2006) Neogene Cupuladriidae of tropical America. I: Taxonomy of recent Cupuladria from opposite sides of the Isthmus of Panama. J Paleontol 80:245–263

    Article  Google Scholar 

  • Herrera-Cubilla A, Dick MH, Sanner J, Jackson JBC (2008) Neogene Cupuladriidae of tropical America. II: Taxonomy of recent Discoporella from opposite sides of the Isthmus of Panama. J Paleontol 82:279–298

    Article  Google Scholar 

  • Jackson JBC, Cheetham AH (1999) Tempo and mode of speciation in the sea. Trends Ecol Evol 14:72–77

    Article  PubMed  Google Scholar 

  • Jackson JBC, D’croz L (1999) The Ocean divided. In Central America. In: Coates AG (ed) A natural and cultural history. Yale University Press, New Haven, pp 38–71

    Google Scholar 

  • Jackson JBC, Erwin DH (2006) What can we learn about ecology and evolution from the fossil record? Trends Ecol Evol 21:322–328

    Article  PubMed  Google Scholar 

  • Jackson JBC, Johnson KG (2000) Life in the last few million years. Paleobiology 26:221–235

    Article  Google Scholar 

  • Jackson JBC, Johnson KG (2001) Paleoecology—measuring past biodiversity. Science 293:2403–2404

    Google Scholar 

  • Jackson JBC, Jung P, Coates AG, Collins LS (1993) Diversity and extinction of Tropical American molluscks and emergence of the Isthmus of Panama. Science 260:1624–1626

    Article  PubMed  CAS  Google Scholar 

  • Jackson JBC, Budd AF, Coates AG (1996) Evolution & environment in tropical America. University of Chicago Press, Chicago

  • Johnson KG, Todd JA, Jackson JBC (2007) Coral reef development drives molluscan diversity increase at local and regional scales in the late Neogene and Quaternary of the southwestern Caribbean. Paleobiology 33:24–52

    Article  Google Scholar 

  • Johnson KG, Jackson JBC, Budd AF (2008) Caribbean reef development was independent of coral diversity over 28 million years. Science 319:1521–1523

    Article  PubMed  CAS  Google Scholar 

  • Kidwell SM (2001) Preservation of species abundance in marine death assemblages. Science 294:1091

    Article  PubMed  CAS  Google Scholar 

  • Kidwell SM (2005) Shell composition has no net impact on large-scale evolutionary patterns in mollusks. Science 307:914

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Lasker HR (1984) Asexual reproduction, fragmentation, and skeletal morphology of a plexaurid gorgonian. Marine ecology progress series. Oldendorf 19:261–268

    Google Scholar 

  • Lessios H (1981) Divergence in allopatry: molecular and morphological differentiation between sea urchins separated by the Isthmus of Panama. Evolution 35:618–634

    Article  Google Scholar 

  • Lessios HA (2008) The great American Schism: divergence of marine organisms after the rise of the Central American Isthmus. Annu Rev Ecol Evol Syst 39:63–91

    Article  Google Scholar 

  • Maddison DR, Maddison WP (2000) MacClade 4. Sinauer Associates

  • Marcus E, Marcus E (1962) On some lunulitiform Bryozoa. Universidade de São Paulo Boletins da Faculdade de Philosophia, Sciéncias e Letras, Zoologia 3:111–353

    Google Scholar 

  • Marko PB (2000) Fossil calibration of molecular clocks and the divergence times of the geminate species pairs separated by the Isthmus of Panama. Mol Biol Evol 19:2005–2021

    Article  Google Scholar 

  • Mayr E (1954) Geographic speciation in tropical echinoids. Evolution 8:1–18

    Article  Google Scholar 

  • Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge

    Google Scholar 

  • McKinney FK, Jackson JBC (1989) Bryozoan evolution. Unwin Hyman, Boston

    Google Scholar 

  • Mendelson TC, Shaw KL (2005) Sexual behaviour: rapid speciation in an arthropod. Nature 433:375–376

    Article  PubMed  CAS  Google Scholar 

  • Miura O, Torchin ME, Bermingham E (2010) Molecular phylogenetics reveals differential divergence of coastal snails separated by the Isthmus of Panama. Mol Phylogenet Evol 56:40–48

    Article  PubMed  Google Scholar 

  • Nehm RH, Geary DH (1994) A gradual morphologic transition during a rapid speciation event in marginellid gastropods (neogene—dominican-republic). J Paleontol 68:787–795

    Google Scholar 

  • Nuryanto A, Kochzius M (2009) Highly restricted gene flow and deep evolutionary lineages in the giant clam Tridacna maxima. Coral Reefs 28:607–619

    Article  Google Scholar 

  • Nylander JAA (2004) MrModeltest Version 2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University: Uppsala, Sweden

  • O’Dea A (2006) Asexual propagation in the marine bryozoan Cupuladria exfragminis. J Exp Mar Biol Ecol 335:312–322

    Article  Google Scholar 

  • O’Dea A (2009) Relation of form to life habit in free-living cupuladriid bryozoans. Aquat Biol 7:1–18

    Article  Google Scholar 

  • O’Dea A, Jackson J (2009) Environmental change drove macroevolution in cupuladriid bryozoans. Proc R Soc B Biol Sci 276:3629–3634

    Article  Google Scholar 

  • O’Dea A, Herrera-Cubilla A, Fortunato H, Jackson JBC (2004) Life history variation in cupuladriid bryozoans from either side of the Isthmus of Panama. Mar Ecol Prog Ser 280:145–161

    Article  Google Scholar 

  • O’Dea A, Jackson JBC, Fortunato H, Smith JT, D’Croz L, Johnson KG, Todd JA (2007) Environmental change preceded Caribbean extinction by 2 million years. Proc Natl Acad Sci USA 104:5501–5506

    Article  PubMed  Google Scholar 

  • O’Dea A, Jackson JBC, Taylor PD, Rodriguez F (2008) Modes of reproduction in recent and fossil cupuladriid bryozoans. Palaeontology 51:847–864

    Article  Google Scholar 

  • Passamaneck Y, Halanych KM (2006) Lophotrochozoan phylogeny assessed with LSU and SSU data: evidence of lophophorate polyphyly. Mol Phylogenet Evol 40:20–28

    Article  PubMed  CAS  Google Scholar 

  • Quenouille R, Hubert N, Bermingam E, Planes S (2010) Speciation in tropical seas; Allopatry followed by range change. Mol Phylogenet Evol 58:546–552

    Google Scholar 

  • Quental TB, Marshall CR (2010) Diversity dynamics: molecular phylogenies need the fossil record. Trends Ecol Evol 25:434–441

    Google Scholar 

  • Renema W, Bellwood DR, Braga JC, Bromfield K, Hall R, Johnson KG, Lunt P, Meyer CP, McMonagle LB, Morley RJ, O’Dea A, Todd JA, Wesselingh FP, Wilson MEJ, Pandolfi JM (2008) Hopping hotspots: global shifts in marine biodiversity. Science 321:654–657

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Schluter D (2001) Ecology and the origin of species. Trends Ecol Evol 16:372–380

    Article  PubMed  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 

  • Smith JT, Jackson JBC (2009) Ecology of extreme faunal turnover of tropical American scallops. Paleobiology 35:77–93

    Article  Google Scholar 

  • Smith PL, Tipper HW (1986) Plate tectonics and paleobiogeography, Early Jurassic Pleinsbachian endemism and diversity. Palaios 1:399–412

    Article  Google Scholar 

  • Todd JA, Jackson JBC, Johnson KG, Fortunato HM, Heitz A, Alvarez M, Jung P (2002) The ecology of extinction: molluscan feeding and faunal turnover in the Caribbean Neogene. Proc R Soc Lond Ser B Biol Sci 269:571–577

    Article  CAS  Google Scholar 

  • Vermeij G, Petuch E (1986) Differential extinction in tropical American molluscs: endemism, architecture, and the Panama land bridge. Malacologia 27:29–41

    Google Scholar 

  • Williams DM (2007) Diatom phylogeny: fossils, molecules and the extinction of evidence. Comptes Rendus Palevol 6:505–514

    Article  Google Scholar 

  • Winston JE (1988) Life histories of free-living bryozoans. Natl Geogr Res 4:528–539

    Google Scholar 

  • Woodring WP (1966) The Panama land bridge as a sea barrier. Proc Am Phil Soc 110:425–433

    Google Scholar 

Download references

Acknowledgments

We are indebted to Felix Rodriguez, Brigida Degracia, and Yadixa del Valle who worked tirelessly collecting morphological data. Anthony Coates, Carlos De Gracia, Javier Jara, Amalia Herrera and the crew of the R/V Urraca helped in the field. Ligia Calderon helped with sequencing. Paul Taylor produced the scanning electron micrographs. Adriana Bilgray, Harilaos Lessios and Eldredge Bermigham provided logistical support. We thank Simon Coppard, Osamu Miura, Scott Lidgard and Matthew Dick for stimulating discussion. The manuscript benefited from constructive criticism and suggestions from Matthew Dick and an anonymous reviewer. Recursos Minerales kindly gave permission to collect fossil material in Panama. This work was funded by the NSF (EAR03-45471), the Smithsonian Marine Science Network, the Smithsonian Tropical Research Institute’s Tupper Fellowship and Scholarly Studies Programs, SENACYT and the National Geographic Society’s Exploration Grants. This work is dedicated to Jeremy B.C. Jackson for his vision, guidance and support.

Author information

Authors and Affiliations

  1. Smithsonian Tropical Research Institute, Apartado, 0843-03092, Panama, Republic of Panama

    Santosh Jagadeeshan & Aaron O’Dea

Authors
  1. Santosh Jagadeeshan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aaron O’Dea
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aaron O’Dea.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jagadeeshan, S., O’Dea, A. Integrating fossils and molecules to study cupuladriid evolution in an emerging Isthmus. Evol Ecol 26, 337–355 (2012). https://doi.org/10.1007/s10682-011-9522-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-011-9522-6

Keywords

Search

Navigation