Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-19T11:34:46.337Z Has data issue: false hasContentIssue false
  • English
  • Français

Overlapping species boundaries and hybridization within the Montastraea “annularis” reef coral complex in the Pleistocene of the Bahama Islands

Published online by Cambridge University Press:  08 February 2016

Ann F. Budd  and
John M. Pandolfi
Ann F. Budd
Affiliation:
Department of Geoscience, University of Iowa, Iowa City, Iowa 52242. E-mail: ann-budd@uiowa.edu
John M. Pandolfi
Affiliation:
Department of Paleobiology, MRC 121, National Museum of Natural History, Smithsonian Institution, Washington DC. 20560-0121. E-mail: Pandolfi.john@NMNH.SI.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Recent molecular analyses indicate that many reef coral species belong to hybridizing species complexes or “syngameons.” Such complexes consist of numerous genetically distinct species or lineages, which periodically split and/or fuse as they extend through time. During splitting and fusion, morphologic intermediates form and species overlap. Here we focus on processes associated with lineage fusion, specifically introgressive hybridization, and the recognition of such hybridization in the fossil record. Our approach involves comparing patterns of ecologic and morphologic overlap in genetically characterized modern species with fossil representatives of the same or closely related species. We similarly consider the long-term consequences of past hybridization on the structure of modern-day species boundaries.

Our study involves the species complex Montastraea annularis s.l. and is based in the Bahamas, where, unlike other Caribbean locations, two of the three members of the complex today are not genetically distinct. We measured and collected colonies along linear transects across Pleistocene reef terraces of last interglacial age (approximately 125 Ka) on the islands of San Salvador, Andros, and Great Inagua. We performed quantitative ecologic and morphologic analyses of the fossil data, and compared patterns of overlap among species with data from modern localities where species are and are not genetically distinct.

Ecologic and morphologic analyses reveal “moderate” overlap (>10%, but statistically significant differences) and sometimes “high” overlap (no statistically significant differences) among Pleistocene growth forms (= “species”). Ecologic analyses show that three species (massive, column, organ-pipe) co-occurred. Although organ-pipes had higher abundances in patch reef environments, columnar and massive species exhibited broad, completely overlapping distributions and had abundances that were not related to reef environment. For morphometric analyses, we used multivariate discriminant analysis on landmark data and linear measurements. The results show that columnar species overlap “moderately” with organ-pipe and massive species. Comparisons with genetically characterized colonies from Panama show that the Pleistocene Bahamas species have intermediate morphologies, and that the observed “moderate” overlap differs from the morphologic separation among the three modern species. In contrast, massive and columnar species from the Pleistocene of the Dominican Republic comprise distinct morphologic clusters, similar to the modern species; organ-pipe species exhibit “low” overlap (<10%, only at species margins) with columnar and massive species.

Assuming that “moderate” overlap implies hybridization and “high” overlap implies more complete lineage fusion, these results support the hypothesis of hybridization among species within the complex in the Bahamas during the Pleistocene. Hybridization involved introgression of three distinct evolutionary lineages, in association with Pleistocene sea level and temperature fluctuations, and appears to have been limited geographically primarily to the Bahamas and the northern Caribbean. Thus, not only does the structure of species boundaries within the complex vary geographically, but these geographic differences may have persisted since the Pleistocene.

Type
Articles
Information
Paleobiology , Volume 30 , Issue 3 , Summer 2004 , pp. 396 - 425
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Benzie, J. A. H. 1999. Genetic structure of coral reef organisms: ghosts of dispersal past. American Zoologist 39:131–145.CrossRefGoogle Scholar
Bookstein, F. L. 1991. Morphometric tools for landmark data. Cambridge University Press, Cambridge.Google Scholar
Bray, J. R., and Curtis, J. T. 1957. An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 27:325–349.CrossRefGoogle Scholar
Budd, A. F. 1993. Variation within and among morphospecies of Montastraea. Courier Forschungsinstitut Senckenberg 164:241–254.Google Scholar
Budd, A. F., and Johnson, K. G. 1996. Recognizing species of Late Cenozoic Scleractinia and their evolutionary patterns. Paleontological Society Papers 1:59–79.CrossRefGoogle Scholar
Budd, A. F., and Johnson, K. G. 1999. Origination preceding extinction during Late Cenozoic turnover of Caribbean reefs. Paleobiology 25:188–200.CrossRefGoogle Scholar
Budd, A. F., and Klaus, J. S. 2001. The origin and early evolution of the Montastraea “annularis” species complex (Anthozoa: Scleractinia). Journal of Paleontology 75:527–545.2.0.CO;2>CrossRefGoogle Scholar
Chen, J. H., Curran, H. A., White, B., and Wasserburg, G. J. 1991. Precise chronology of the last interglacial period: 234U-230Th data from fossil coral reefs in the Bahamas. Geological Society of America Bulletin 103:82–97.2.3.CO;2>CrossRefGoogle Scholar
Curran, H. A., and White, B. 1984. Field guide to the Cockburn Town fossil coral reef. Pp. 71–96in Teeter, J. W., ed. Proceedings of the second symposium on the geology of the Bahamas. CCFL Bahamian Field Station, San Salvador, Bahamas.Google Scholar
Curran, H. A., and White, B. 1985. The Cockburn Town fossil coral reef. Pp. 95–120in Curran, H. A., ed. Pleistocene and Holocene carbonate environments on San Salvador Island, Bahamas. Guidebook for field trip 2, the Geological Society of America annual meeting, Orlando, Florida. Geological Society of America, Boulder, Colo.Google Scholar
Faith, D. P., Minchin, P. R., and Belbin, L. 1987. Compositional dissimilarity as a robust measure of ecological distance. Vegetatio 69:57–68.CrossRefGoogle Scholar
Field, J. G., Clarke, K. R., and Warwick, D. R. M. 1982. A practical strategy for analyzing multispecies distribution patterns. Marine Ecology Progress Series 8:37–52.CrossRefGoogle Scholar
Foster, A. B. 1979. Phenotypic plasticity in the reef corals Montastraea annularis (Ellis and Solander) and Siderastrea siderea (Ellis and Solander). Journal of Experimental Marine Biology and Ecology 39:25–54.CrossRefGoogle Scholar
Fukami, H., Budd, A. F., Levitan, D. R., Jara, J., Kersanach, R., and Knowlton, N. 2004. Geographical differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution 58:308–323.Google ScholarPubMed
Graus, R. R., and Macintyre, I. G. 1982. Variation in growth forms of the reef coral Montastrea annularis (Ellis and Solander): a quantitative evaluation of growth response to light distribution using computer simulation. In Rützler, K. and Macintyre, I. G., eds. The Atlantic Barrier Reef Ecosystem at Carrie Bow Cay, Belize, Smithsonian Contributions to the Marine Sciences 12:441–464.Google Scholar
Harrison, R. G. 1990. Hybrid zones: windows on evolutionary process. Oxford Surveys in Evolutionary Biology 7:69–128.Google Scholar
Hatta, M., Fukami, H., Wang, W., Omori, M., Shimoike, K., Hayashibara, T., Ina, Y., and Sugiyama, T. 1999. Reproductive and genetic evidence for a reticulate evolutionary history of mass spawning corals. Molecular Biology and Evolution 16:1607–1613.CrossRefGoogle ScholarPubMed
Holcomb, M., Pandolfi, J. M., Macintyre, I. G., and Budd, A. F.In press. Use of X-radiographs to distinguish members of the Montastraea “annularis” reef coral species complex. In Fautin, D. G., Westfall, J. A., Cartwright, P., Daly, M., and Wyttenbach, C. R., eds. Coelenterate biology 2003: trends in research on Cnidaria and Ctenophora. Hydrobiologia.Google Scholar
Jackson, J.B.C., Budd, A. F., and Pandolfi, J. M. 1996. The shifting balance of natural communities? Pp. 89–122. in Jablonski, D., Erwin, D. H., and Lipps, J. H., eds. Evolutionary paleobiology: essays in honor of James W. Valentine. University of Chicago Press, Chicago.Google Scholar
Klaus, J. S., and Budd, A. F. 2003. Comparison of Caribbean coral reef communities before and after Plio-Pleistocene faunal turnover: analyses of two Dominican Republic reef sequences. Palaios 18:3–21.2.0.CO;2>CrossRefGoogle Scholar
Knowlton, N., and Budd, A. F. 2001. Recognizing coral species past and present. Pp.97–119in Jackson, J. B. C., Lidgard, S., and McKinney, F. K., eds. Evolutionary patterns: growth, form, and tempo in the fossil record. University of Chicago Press, Chicago.Google Scholar
Knowlton, N., Weil, E., Weigt, L. A., and Guzman, H. M. 1992. Sibling species in Montastraea annularis, coral bleaching, and the coral climate record. Science 255:330–333.CrossRefGoogle ScholarPubMed
Knowlton, N., Mate, J. L., Guzman, H. M., Rowan, R., and Jara, J. 1997. Direct evidence for reproductive isolation among the three species of the Montastraea annularis complex in Central America (Panama and Honduras). Marine Biology 127:705–711.CrossRefGoogle Scholar
Lopez, J. V., and Knowlton, N. 1997. Discrimination of sibling species in the Montastraea annularis complex using multiple genetic loci. Proceedings of the Eighth International Coral Reef Symposium 2:1613–1618.Google Scholar
Lopez, J. V., Kersanach, R., Rehner, S. A., and Knowlton, N. 1999. Molecular determination of species boundaries in corals: genetic analysis of the Montastraea annularis complex using amplified fragment length polymorphism and a microsatellite marker. Biological Bulletin 196:80–89.CrossRefGoogle Scholar
Marquez, L. M., van Oppen, M. J. H., Willis, B. L., Reyes, A., and Miller, D. J. 2002. The highly cross-fertile coral species, Acropora hyacinthus and Acropora cytherea, constitute statistically distinguishable lineages. Molecular Ecology 11:1339–1349.CrossRefGoogle ScholarPubMed
Miller, K. J., and Benzie, J. A. H. 1997. No clear genetic distinction between morphological species within the coral genus Platygyra. Bulletin of Marine Science 61:907–917.Google Scholar
Neumann, A. C., and Moore, W. S. 1975. Sea level events and Pleistocene coral ages in the northern Bahamas. Quaternary Research 5:215–224.CrossRefGoogle Scholar
Odorico, D. and Miller, D. J. 1997. Variation in the ribosomal internal transcribed spacers and 5.8S rDNA among five species of Acropora (Cnidaria; Scleractinia): patterns of variation consistent with reticulate evolution. Molecular Biology and Evolution 14:465–473.CrossRefGoogle ScholarPubMed
Pandolfi, J. M. 1996. Limited membership in Pleistocene reef coral assemblages from the Huon Peninsula, Papua New Guinea: constancy during global change. Paleobiology 22:152–176.CrossRefGoogle Scholar
Pandolfi, J. M. 2001. Numerical and taxonomic scale of analysis in paleoecological data sets: Examples from Neo-tropical Pleistocene reef coral communities. Journal of Paleontology 75:546–563.2.0.CO;2>CrossRefGoogle Scholar
Pandolfi, J. M., and Jackson, J. B. C. 2001. Community structure of Pleistocene coral reefs of Curaçao, Netherlands Antilles. Ecological Monographs 71:49–67.Google Scholar
Pandolfi, J. M., and Minchin, P. R. 1995. A comparison of taxonomic composition and diversity between reef coral life and dead assemblages in Madang Lagoon, Papua New Guinea: Palaeogeography, Palaeoclimatology, Palaeoecology 119:321–341.CrossRefGoogle Scholar
Pandolfi, J. M., Jackson, J. B. C., and Geister, J. 2001. Geologically sudden extinction of two widespread late Pleistocene Caribbean reef corals. Pp.120–158in Jackson, J. B. C., Lidgard, S., and McKinney, F. K., eds. Evolutionary patterns: growth, form, and tempo in the fossil record. University of Chicago Press, Chicago.Google Scholar
Pandolfi, J. M., Lovelock, C. E., and Budd, A. F. 2002. Character release following extinction in a Caribbean reef coral species complex. Evolution 56:479–501.Google Scholar
Rodriguez-Lanetty, M., and Hoegh-Guldberg, O. 2002. The phylogeography and connectivity of the latitudinally widespread scleractinian coral Plesiastrea versipora in the western Pacific. Molecular Ecology 11:1177–1189.CrossRefGoogle ScholarPubMed
Rowan, R., and Knowlton, N. 1995. Intraspecific diversity and ecological zonation in coral algal symbiosis. Proceedings of the National Academy of Sciences USA 92:2850–2853.CrossRefGoogle ScholarPubMed
Szmant, A. M., Weil, E., Miller, M. W., and Colon, D. E. 1997. Hybridization within the species complex of the scleractinian coral Montastraea annularis. Marine Biology 129:561–572.CrossRefGoogle Scholar
Tomascik, T. 1990. Growth rates of two morphotypes of Montastraea annularis along a eutrophication gradient, Barbados, W.I. Marine Pollution Bulletin 21:376–380.CrossRefGoogle Scholar
Tomb, J. M. 1995. Description and depositional interpretation of a Pleistocene coral reef, Nichollstown, Andros Island, Bahamas. . Wright State University, Dayton, Ohio.Google Scholar
van Oppen, M. J. H., Willis, B. L., Van Vugt, J. A., and Miller, D. J. 2000. Examination of species boundaries in the Acropora cervicornis group (Scleractinia, Cnidaria) using nuclear DNA sequence analyses. Molecular Ecology 9:1363–1373.CrossRefGoogle Scholar
van Oppen, M. J. H., McDonald, B. J., Willis, B. L., and Miller, D. J. 2001. The evolutionary history of the coral genus Acropora (Scleractinia, Cnidaria) based on a mitochondrial and a nuclear marker: reticulation, incomplete lineage sorting, or morphological convergence? Molecular Biology and Evolution 18:1315–1329.CrossRefGoogle ScholarPubMed
van Oppen, M. J. H., Willis, B. L., van Rheede, T., and Miller, D. J. 2002. Spawning times, reproductive compatibilities and genetic structuring in the Acropora aspera group: evidence for natural hybridization and semi-permeable species boundaries in corals. Molecular Ecology 11:1363–1376.CrossRefGoogle ScholarPubMed
van Veghel, M. L. J. 1994. Reproductive characteristics of the polymorphic Caribbean reef building coral, Montastraea annularis: genetic, behavioral, and morphometric aspects. Marine Ecology Progress Series 109:209–219.CrossRefGoogle Scholar
van Veghel, M. L. J., and Bak, R. P. M. 1993. Intraspecific variation of a dominant Caribbean reef building coral, Montastraea annularis: genetic, behavioral and morphometric aspects. Marine Ecology Progress Series 92:255–265.CrossRefGoogle Scholar
Vaughan, T. W. 1919. Fossil corals from Central America, Cuba, and Porto Rico with an account of the American Tertiary, Pleistocene, and Recent coral reefs. U.S. National Museum Bulletin 103:189–524.Google Scholar
Veron, J. E. N. 1995. Corals in space and time. UNSW Press, Sydney.Google Scholar
Vollmer, S. V., and Palumbi, S. R. 2002. Hybridization and the evolution of reef coral diversity. Science 296:2023–2025.CrossRefGoogle ScholarPubMed
Weil, E., and Knowlton, N. 1994. A multi-character analysis of the Caribbean coral Montastraea annularis (Ellis and Solander, 1786), and its two sibling species, M. faveolata (Ellis and Solander, 1786) and M. franksi (Gregory, 1895). Bulletin of Marine Science 55:151–175.Google Scholar
White, B. 1989. Field guide to the Sue Point fossil coral reef, San Salvador Island, Bahamas. Pp. 353–365. in MyIroie, J. E., ed. Proceedings of the fourth symposium on the geology of the Bahamas. CCFL Bahamian Field Station, San Salvador, Bahamas.Google Scholar
White, B., and Curran, H. A. 1987. Coral reef to eolianite transition in the Pleistocene rocks of Great Inagua Island. Pp. 165–179in Curran, H. A., ed. Proceedings of the third symposium on the geology of the Bahamas. CCFL Bahamian Field Station, San Salvador, Bahamas.Google Scholar
White, B., and Curran, H. A. 1995. Entombment and preservation of Sangamonian coral reefs during glacioeustatic sea-level fall, Great Inagua Island, Bahamas. In Curran, H. A. and White, B., eds. Terrestrial and shallow marine geology of the Bahamas and Bermuda. Geological Society of America Special Paper 300:51–61.CrossRefGoogle Scholar
White, B. and Wilson, M. A. 1998. Bahamian coral reefs yield evidence of a brief sea-level lowstand during the last interglacial. Carbonates and Evaporites 13:10–22.CrossRefGoogle Scholar
Wilson, M. A., Curran, H. A., and White, B. 1998. Paleontological evidence of a brief global sea-level event during the last interglacial. Lethaia 31:241–250.CrossRefGoogle Scholar