Printer Friendly

Trans-Pacific range extension by rafting is inferred for the flat oyster Ostrea chilensis.

Stretches of deep ocean are potent barriers to the dispersion of nearshore, benthic marine taxa. Such obstacles can be overcome, however, by species that have either a protracted pelagic larval development or a benthic life-history stage that can be transported by rafting (1, 2). The oyster Ostrea chilensis lacks an extended pelagic larval phase and has discrete populations in New Zealand and Chile that are separated by one of the largest extents ([greater than]7000 km) of open ocean on the planet. We tested competing dispersal hypotheses for this species by using ontogenetically informative, dated fossil and sub-fossil shell material, as well as molecular phylogenetic analyses. Our data show that dispersal by rafting is by far the most likely explanation for trans-Pacific range extension by this oyster, and we reject competing hypotheses of vicariance, anthropogenic introduction, and dispersal by ancestral lineages with extended larval development. The presence of O. chilensis in Chile is important because it clearly demonstrates that transoceanic range extension by rafting is potentially available to a significant fraction of nearshore marine biotas.

A prolonged pelagic larval phase facilitates the crossing of open-ocean barriers by nearshore benthic taxa (3, 4), and an evolutionarily important linkage has been proposed between this mode of development and a suite of species-level traits, including enhanced geographic range (5, 6). However, there are also many nearshore examples of individual species (7), clonal taxa (8, 9), and significant fractions of entire faunas (10) that lack significant pelagic larval development and have biogeographic ranges that span oceanic barriers to dispersal. Spontaneous rafting events, in which sessile life-history stages are passively transported on drifting objects, are common in the marine environment and have probably acted as an alternative long-distance dispersal mechanism for major subsections of shallow-water hard-bottom faunas over ecologically significant timescales (7-11). In the case of individual species, however, claims of long-distance range extension by rafting are usually confounded by the alternative possibilities of undocumented anthropogenic introductions that predate biotic surveys (12), or of transoceanic colonization by ancestral lineages having extended larval development, with the subsequent evolutionary loss of such larvae (13). In this study, we present a specific case of transoceanic range extension by rafting, possibly the first from which the alternative dispersal hypotheses can be excluded with confidence.

Ostrea chilensis is unique among oysters in lacking an obligate feeding pelagic (planktotrophic) larval development; larvae typically metamorphose less than 2 hours after their release from parental brood chambers (14). This greatly abbreviated pelagic phase is associated with a highly distinctive larval shell morphology (15) and is a derived condition among flat oysters (16). O. chilensis occurs in two regional populations separated by 7400 km of uninterrupted south Pacific Ocean [ILLUSTRATION FOR FIGURE 1 OMITTED]. It is found throughout the nearshore waters of New Zealand (including the Chatham Islands) to depths of 550 m (17) and also in the shallow subtidal zone of southern Chile (18). New Zealand and Chile share some relict Gondwanaland taxa (19), but this oyster does not qualify as such because it is unknown from pre-Holocene Chilean fossil strata (20), its appearance in the New Zealand Pliocene fossil record (21) greatly post-dates the separation of New Zealand from Gondwanaland (22), and its New Zealand and Chilean populations are almost indistinguishable allozymically [genetic similarity = 0.991; a value of 1.0 indicates genetic identity (18)].

The fossil record suggests that the New Zealand population is ancestral, and it is speculated that the Chilean population was founded by rafted, post-metamorphic New Zealand oysters transported via the Antarctic circumpolar and Humboldt currents (18). Alternatively, Chilean populations might have been established by the transoceanic dispersal of ancestral New Zealand larvae with extended planktotrophic pelagic development, followed by independent losses of this developmental mode in both source and founder populations. The simplest hypothesis is that the Chilean population resulted from an undocumented human introduction event, a frequent occurrence for commercially important oysters (23, 24).

Samples of sub-fossil O. chilensis were collected for radiocarbon dating from the Raqi-Tubul estuary, a southern Chilean location where this species has been regarded as the sole native oyster (25). Radiocarbon age estimates (95% confidence intervals) of 953-1238 and 2998-3383 years before present (y BP) were obtained for specimens taken respectively from salt marsh sediments and from an oyster midden site (26). Some of the midden specimens had attached juvenile oysters (spat) that retained well-preserved larval shells (prodissoconchs) displaying the diagnostic morphological characteristics of this species of oyster [ILLUSTRATION FOR FIGURE 2A OMITTED]. Unequivocal evidence for human settlement in New Zealand dates from about 850 y BP (27). The presence of significant populations of O. chilensis in South America 2000 years prior to this date precludes anthropogenic introduction as a credible explanation for transoceanic range extension in this species.

Although O. chilensis transversed the South Pacific without human intervention, the Chilean midden data do not reveal whether this occurred via planktotrophic larval dispersal. Previous studies of fossil O. chilensis in New Zealand were based on adult shell morphology (21) and do not provide insights into when planktotrophic larval development was lost in this oyster lineage. We examined museum fossil holdings of O. chilensis and found individuals from North Island strata [late Pliocene, upper Nukumaruan Stage (1.6-2.0 mya)], with a prodissoconch structure identical to that of modern specimens [ILLUSTRATION FOR FIGURE 2B OMITTED]. Earlier Pliocene specimens did not yield interpretable prodissoconchs, but the North Island populations of this species had fully evolved the present day nonplanktotrophic larval development prior to the Pleistocene. This is pertinent because molecular phylogenetic analysis of O. chilensis populations [ILLUSTRATION FOR FIGURE 3 OMITTED] indicates that (1) a pronounced mitochondrial dichotomy exists among North and South Island samples, differing by 19 nucleotide substitutions (3.1% sequence divergence for a 609 nucleotide fragment of cytochrome oxidase I); (2) North Island and Chilean samples form sister lineages, differing by four nucleotide substitutions (0.6% sequence divergence); (3) ancestral North Island lineages were the probable source populations for trans-Pacific colonists.

Joint consideration of the fossil and molecular data allows a comparative evaluation of the two remaining dispersal hypotheses. Rafting is compatible with a single loss of planktotrophic larval development in a common ancestral lineage of O. chilensis and allows for a Pleistocene/Holocene trans-Pacific colonization event. Conversely, dispersal by planktotrophic larvae requires that trans-Pacific colonization be pre-Pleistocene, and that loss of such larvae (a condition unique to O. chilensis among the Ostreacea) occurred on three independent occasions after the respective branching of South Island, North Island, and (pre-Pleistocene and post-trans-Pacific colonization) Chilean lineages. This mechanism of dispersal also requires the assumption that putative ancestral larval cohorts were sufficiently long-lived and numerous to overcome mortality and (enormous) diffusion effects over a [greater than]7000-km linear dispersive pathway, and to recruit in viable breeding densities in Chile. Extant flat oyster species with planktotrophic larvae have pelagic periods ranging from 6 to 33 days (29). The effective dispersal distances [10 s-100 s of km (30)] calculated from these periods are insufficient for trans-Pacific colonization, even if calculated for the most favorable oceanic currents: transoceanic, non-meandering flow rates of 125 cm [multiplied by] [s.sup.-1] [[less than]3600 km (31)]. On grounds of phylogenetic parsimony [ILLUSTRATION FOR FIGURE 3 OMITTED], apparent absence of Pliocene/Pleistocene fossil specimens in Chile (20), and absence of exceptionally long-lived/teleplanic (2) larvae in flat oysters (29), the ancestral planktotrophic larval dispersal hypothesis is rejected as a plausible explanation for trans-Pacific range extension in O. chilensis.

We conclude that dispersal by rafting is by far the most likely explanation for the trans-Pacific range extension of O. chilensis. Pumice, an effective long-distance rafting vector for hard-bottom, shallow-water, suspension-feeding epibenthos (11), may have served as the transport platform, because very significant quantities of this buoyant material have been released by repeated eruptions of the North Island Taupo Volcanic Zone since the Pliocene (32). Further genetic characterization of the North Island and Chilean populations may uncover haplotypes common to both populations, a finding that would be necessary to entertain the possibility of continued trans-Pacific gene flow.

In principle, there may be no maximum dispersal distance for rafting organisms (7, 11), and the presence of O. chilensis in Chile highlights the existence of an alternative dispersal mechanism, of truly transoceanic scope, which is potentially available to many members of nearshore faunas (7-11). A broad cross-section of the North Island hard-bottom epibenthos was probably also rafted across the Pacific, including indirect developing species with an obligate planktotrophic larval stage. Rafted innocula of such taxa are less likely to have become established in Chile because an obligate extended pelagic larval phase would dilute population densities below the concentrations needed for reproductive success in the crucial initial generations of the new colonies (7-9, 11). However, careful analysis of Chilean taxa with reduced or absent pelagic larval development - including sponge, ascidian, cheilostome bryozoan and hydroid faunas (8) - may reveal additional cryptic rafted immigrants from New Zealand. Such taxa would have New Zealand sister lineages and might be identified by morphological or molecular characterization of epifaunal residues from Chilean midden shells that predate human settlement of New Zealand.

Our molecular results are in striking contrast to those from another oyster, Crassostrea virginica; this species undergoes a planktotrophic larval development, but it exhibits greater intraspecific genetic divergence values over a few hundred kilometers of contiguous southeastern Floridian coastline (33) than do North Island and Chilean populations of O. chilensis. The contrasting phylogeographic patterns of these developmentally heterogeneous oyster taxa indicate that assumptions of marine invertebrate genetic structuring based solely on extrapolations from pelagic larval periods may lead to spectacular error.

Acknowledgments

We are indebted to our colleagues who graciously provided ethanol-fixed oyster tissue samples: A. Jeffs, M. Barker, A. Frazer, O. Chaparro, J. Toro, R. Ward, and J. Nell. Manuscript drafts were improved by the comments of G.

Paulay, T. Baumiller, W. Brown, S. Palumbi, and two anonymous reviewers. This study was supported by NSF award 9617689 to D. O Foighil.

Literature Cited

1. Vermeij, G. J. 1987. The dispersal barrier in the tropical Pacific: implications for molluscan speciation and extinction. Evolution 41: 1046-1058.

2. Scheltema, R. S. 1988. Initial evidence for the transport of teleplanic larvae of benthic invertebrates across the east Pacific barrier. Biol. Bull. 174: 145-156.

3. Kohn, A. J., and F. E. Perron. 1994. Life history and biogeography patterns in Conus. Oxford Biogeography Series. 9. Clarendon Press, Oxford. 110 pp.

4. Lessios, H. A., B. D. Kessing, and D. R. Robertson. 1998. Massive gene flow across the world's most potent marine biogeographic barrier. Proc. R. Soc. Lond. B 265: 583-588.

5. Jablonski, D. 1986. Larval ecology and macroevolution in marine invertebrates. Bull. Mar. Sci. 39: 565-587.

6. Jablonski, D. 1987. Heritability at the species level: analysis of geographic ranges of Cretaceous mollusks. Science 238: 360-363.

7. Johannesson, K. 1988. The paradox of Rockall: why is a brooding gastropod (Littorina saxatilis) more widespread than one having a planktonic larval stage (L. littorea)? Mar. Biol. 99: 507-513.

8. Jackson, J. B. C. 1986. Modes of dispersal of clonal benthic invertebrates: consequences for species' distributions and genetic structure of local populations. Bull. Mar. Sci. 39: 588-606.

9. O Foighil, D. 1989. Planktotrophic larval development is associated with a restricted geographic range in Lasaea, a genus of brooding, hermaphroditic bivalves. Mar. Biol. 103: 349-358.

10. Davenport, J., and H. Macalister. 1996. Environmental conditions and physiological tolerances of intertidal fauna in relation to shore zonation at Husvik, South Georgia. J. Mar. Biol. Assoc. UK 76: 985-1002.

11. Jokiel, P. L. 1990. Transport of reef corals into the Great-Barrier Reef. Nature 347: 665-667.

12. Carlton, J. T., and J. Hodder. 1995. Biogeography and dispersal of coastal marine organisms: experimental studies on a replica of a 16th-century sailing vessel. Mar. Biol. 121: 721-730.

13. Jablonski, D., and R. A. Lutz. 1983. Larval ecology of marine benthic invertebrates: paleobiological implications. Biol. Rev. Camb. Philos. Soc. 58: 21-89.

14. Millar, R. H., and P. J. Hollis. 1963. Abbreviated pelagic life of Chilean and New Zealand oysters. Nature 197: 512-513.

15. Chanley, P., and P. Dinamani. 1980. Comparative descriptions of some oyster larvae from New Zealand and Chile, and a description of a new genus of oyster, Tiostrea. N. Z. J. Mar. Freshwater Res. 14: 103-120.

16. Jozefowitz, C. J., and D. O Foighil. 1998. Molecular phylogenetic analysis of Southern Hemisphere flat oysters based on partial mitochondrial 16S rDNA gene sequences. Mol. Phylogenet. Evol. 10:426-435.

17. Jeffs, A. G., and R. G. Creese. 1996. Overview and bibliography of research on the Chilean oyster Tiostrea chilensis (Phillippi, 1845) from New Zealand waters. J. Shellfish Res. 15:305-311.

18. Buroker, N. E., P. Chanley, and P. Dinamani. 1983. Systematic status of two oyster populations of the genus Tiostrea from New Zealand and Chile. Mar. Biol. 77: 191-200.

19. Cooper, R. A., and P. R. Millener. 1993. The New Zealand biota: historical background and new research. TREE 8: 429-433.

20. Herm, D. 1969. Marines Pliozan und Pleistozan in Nord und Mittel-Chile unter besonderer Berucksichtigung der Entwicklung der Mollusken-faunen. Zitteliana 2:159 pp.

21. Beu, A. G., and P. A. Maxwell. 1990. Cenozoic Mollusca of New Zealand. N. Z. Geol. Surv. Paleontol. Bull. 58: 336-341.

22. Weissel, J. K., and D. E. Hayes. 1977. Evolution of the Tasman Sea reappraised. Earth Planet. Sci. Lett. 36: 77-84.

23. Carlton, J. T., and R. Mann. 1996. Transfers and world-wide introductions. Pp. 691-706 in The Eastern Oyster Crassostrea virginica, V. S. Kennedy, R. I. E. Newell, and A. F. Eble, eds. Maryland Sea Grant, College Park, Maryland.

24. O Foighil, D., P. M. Gaffney, A. E. Wilbur, and T. J. Hilbish. 1998. Mitochondrial cytochrome oxidase I gene sequences support an Asian origin for the Portuguese oyster, Crassostrea angulata. Mar. Biol. 131: 497-503.

25. Solis, I. F. 1967. Observaciones biologicas en Ostras (Ostrea chilensis Philippi) de Pullinque. Biol. Pesq. (Chile) 2:51-82.

26. Bustos, V, N. Vergara, and Z. Seguel. 1997. Los conchales antropicos de ostras en la micro-area de Raqui-Tubul del golfo de Arauco, Vii Region. Abstract, XIV Congreso Nacional de Arqueologia Chilena, Copiapo, p. 41.

27. McGlone, M. S., A. J. Anderson, and R. N. Holdaway. 1994. An ecological approach to the Polynesian settlement of New Zealand. Pp. 136-163 in The Origins of the First New Zealanders, D. G. Sutton, ed. Auckland University Press, Auckland, NZ.

28. Boore, J. L., and W. M. Brown. 1994. Complete DNA sequence of the mitochondrial genome of the black chiton, Katharina tunicata. Genetics 138: 423-443.

29. Buroker, N. E. 1985. Evolutionary patterns in the family Ostreidae: larviparous vs. oviparous. J. Exp. Mar. Biol. Ecol. 90: 233-247.

30. Okubo, A. 1971. Oceanic diffusion diagrams. Deep-Sea Res. 18: 789-802.

31. Scheltema, R. S. 1992. Passive dispersal of planktonic larvae and the biogeography of tropical sublittoral invertebrate species. Pp. 195-202 in Marine Eutrophication and Population Dynamics. Proceedings of the 25th EMBS, G. Colombo et al., eds. Olsen and Olsen, Fredensborg, Denmark.

32. Wilson, C. J. N., B. F. Houghton, and E. F. Lloyd. 1986. Volcanic history and evolution of the Maroa-Taupo area, central North Island. Pp. 194-223 in Late Cenozoic Volcanism in New Zealand, I. E. M. Smith, ed. The Royal Society of New Zealand, Bulletin 23.

33. Reeb, C. A., and J. C. Avise. 1990. A genetic discontinuity in a continuously distributed species: mitochondrial DNA in the American oyster, Crassostrea virginica. Genetics 124: 397-4.
COPYRIGHT 1999 University of Chicago Press
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 1999 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Foighil, Diarmaid O.; Marshall, Bruce A.; Hilbish, Thomas J.; Pino, Mario A.
Publication:The Biological Bulletin
Date:Apr 1, 1999
Words:2549
Previous Article:Mechanisms of specification in ascidian embryos.
Next Article:Comparative analysis of neurogenesis in the central olfactory pathway of adult decapod crustaceans by in vivo BrdU labeling.
Topics:

Terms of use | Privacy policy | Copyright © 2021 Farlex, Inc. | Feedback | For webmasters |