Testing dispersal limits in the sea: range-wide phylogeography of the pronghorn spiny lobster Panulirus penicillatus
Corresponding Author
Matthew Iacchei
Hawai‘i Institute of Marine Biology, Kāne‘ohe, HI, 96744 USA
Department of Oceanography, School of Ocean and Earth Science and Technology, University of Hawai‘i at Mānoa, Honolulu, HI, 96822 USA
Correspondence: Matthew Iacchei, Department of Oceanography, School of Ocean and Earth Science and Technology, University of Hawai'i at Mānoa, 1000 Pope Rd., Honolulu, HI 96822, USA.
E-mail: [email protected]
Search for more papers by this authorMichelle R. Gaither
School of Biological and Biomedical Sciences, Durham University, Durham, DH1 3LE UK
Search for more papers by this authorBrian W. Bowen
Hawai‘i Institute of Marine Biology, Kāne‘ohe, HI, 96744 USA
Search for more papers by this authorRobert J. Toonen
Hawai‘i Institute of Marine Biology, Kāne‘ohe, HI, 96744 USA
Search for more papers by this authorCorresponding Author
Matthew Iacchei
Hawai‘i Institute of Marine Biology, Kāne‘ohe, HI, 96744 USA
Department of Oceanography, School of Ocean and Earth Science and Technology, University of Hawai‘i at Mānoa, Honolulu, HI, 96822 USA
Correspondence: Matthew Iacchei, Department of Oceanography, School of Ocean and Earth Science and Technology, University of Hawai'i at Mānoa, 1000 Pope Rd., Honolulu, HI 96822, USA.
E-mail: [email protected]
Search for more papers by this authorMichelle R. Gaither
School of Biological and Biomedical Sciences, Durham University, Durham, DH1 3LE UK
Search for more papers by this authorBrian W. Bowen
Hawai‘i Institute of Marine Biology, Kāne‘ohe, HI, 96744 USA
Search for more papers by this authorRobert J. Toonen
Hawai‘i Institute of Marine Biology, Kāne‘ohe, HI, 96744 USA
Search for more papers by this authorAbstract
Aim
To resolve phylogeographical partitions in the pronghorn spiny lobster, Panulirus penicillatus, which has a nine-month pelagic larval phase and the broadest distribution among spiny lobsters. With samples from the Red Sea to the East Pacific, we test genetic partitions across two-thirds of the planet, in a species with one of the longest pelagic phases.
Location
Red Sea, Indian and Pacific Oceans.
Methods
A fragment of the mtDNA cytochrome c oxidase subunit I gene (COI) was resolved in 774 individuals from 28 locations, plus 55 sequences (10 locations) from public databases. Portions of COI, 12S and 16S mtDNA regions were resolved for phylogenetic analyses on a subset of individuals. Phylogenetic and population-level analyses were used to detect evolutionary partitions and dispersal barriers.
Results
Significant population structuring was detected (overall ΦST = 0.310, P < 0.001). Samples from the Red Sea and East Pacific Provinces (western and eastern range edges) comprise distinct phylogenetic lineages, divergent at d = 1.1% and 1.8%, respectively, from the Indo-Pacific. Coalescent analyses indicate a Pleistocene isolation for the Red Sea (0.71 Ma) and East Pacific (1.52 Ma). Excluding the Red Sea and East Pacific, structure across the rest of the range was comparatively low, but significant (ΦST = 0.018, P < 0.001).
Main conclusions
The Red Sea and East Pacific populations are phylogenetically distinct from populations elsewhere in the range. The East Pacific population diverged earliest, and may represent a distinct subspecies. Phylogeographical divisions align with the major Indo-Pacific biogeographical barriers, and with subsets of provincial designations from two frameworks: one based on levels of endemism and one on species composition. Tropical and temperate regions in the Pacific are significantly differentiated, potentially indicating an ecological partition. Isolation at eastern and western peripheral provinces may serve as a starting point for evolutionary diversification within this group.
Supporting Information
Filename | Description |
---|---|
jbi12689-sup-0001-AppendixS1-S3.docxWord document, 3.8 MB | Appendix S1 Photographs depicting regional variation in P. penicillatus specimens. Appendix S2 Sample list, detailed methods, additional analyses. Appendix S3 Acknowledgements. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Abdullah, M.F., Muththalib, M., Salama, A.J. & Imai, H. (2014) Genetic isolation among the Northwestern, Southwestern and Central-Eastern Indian Ocean populations of the pronghorn spiny lobster Panulirus penicillatus. International Journal of Molecular Sciences, 15, 9242–9254.
- Allen, G.R. & Robertson, D.R. (1994) Fishes of the Tropical Eastern Pacific. University of Hawaii Press, Honolulu, HI.
- Bandelt, H.J., Forster, P. & Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48.
- Barber, P.H., Cheng, S., Erdmann, M. & Tenggardjaja, K. (2011) Evolution and conservation of marine biodiversity in the Coral Triangle: insights from stomatopod Crustacea. Crustacean Issues, 19, 129–156.
- Baums, I.B., Boulay, J.N., Polato, N.R. & Hellberg, M.E. (2012) No gene flow across the East Pacific Barrier in the reef-building coral Porites lobata. Molecular Ecology, 21, 5418–5433.
- Benzie, J.A.H. (1999) Major genetic differences between crown-of-thorns starfish (Acanthaster planci) populations in the Indian and Pacific Oceans. Evolution, 53, 1782–1795.
- Bernardi, G., Holbrook, S.J., Schmitt, R.J., Crane, N.L. & DeMartini, E. (2002) Species boundaries, populations and colour morphs in the coral reef three-spot damselfish (Dascyllus trimaculatus) species complex. Proceedings of the Royal Society B: Biological Sciences, 269, 599–605.
- Briggs, J.C. (1961) The East Pacific Barrier and the distribution of marine shore fishes. Evolution, 15, 545–554.
- Briggs, J.C. (1974) Marine zoogeography. McGraw-Hill, New York, NY.
- Briggs, J.C. & Bowen, B.W. (2012) A realignment of marine biogeographic provinces with particular reference to fish distributions. Journal of Biogeography, 39, 12–30.
- Butler, M.J., Paris, C.B., Goldstein, J.S., Matsuda, H. & Cowen, R.K. (2011) Behavior constrains the dispersal of long-lived spiny lobster larvae. Marine Ecology Progress Series, 422, 223–237.
- Castelin, M., Feutry, P., Hautecoeur, M., Marquet, G., Wowor, D., Zimmermann, G. & Keith, P. (2013) New insight on population genetic connectivity of widespread amphidromous prawn Macrobrachium lar (Fabricius, 1798) (Crustacea: Decapoda: Palaemonidae). Marine Biology, 160, 1395–1406.
- Chow, S., Jeffs, A., Miyake, Y. et al. (2011) Genetic isolation between the Western and Eastern Pacific populations of pronghorn spiny lobster Panulirus penicillatus. PLoS ONE, 6, e29280.
- Coates, A.G. & Obando, J.A. (1996) The geologic evolution of the Central American isthmus. Evolution and environment in tropical America (ed. by J. Jackson, A.F. Budd and A.G. Coates), pp. 21–56. University of Chicago Press, Chicago.
- Collins, L.S., Coates, A.G., Berggren, W.A., Aubry, M.P. & Zhang, J. (1996) The late Miocene Panama isthmian strait. Geology, 24, 687–690.
- Cortes, J. (1997) Biology and geology of eastern Pacific coral reefs. Coral Reefs, 16, S39–S46.
- Cowman, P.F. & Bellwood, D.R. (2013) The historical biogeography of coral reef fishes: global patterns of origination and dispersal. Journal of Biogeography, 40, 209–224.
- Craig, M.T., Eble, J.A., Bowen, B.W. & Robertson, D.R. (2007) High genetic connectivity across the Indian and Pacific Oceans in the reef fish Myripristis berndti (Holocentridae). Marine Ecology Progress Series, 334, 245–254.
- Crandall, E.D., Frey, M.A., Grosberg, R.K. & Barber, P.H. (2008) Contrasting demographic history and phylogeographical patterns in two Indo-Pacific gastropods. Molecular Ecology, 17, 611–626.
- Crandall, E.D., Treml, E.A. & Barber, P.H. (2012) Coalescent and biophysical models of stepping-stone gene flow in neritid snails. Molecular Ecology, 21, 5579–5598.
- Darwin, C. (1872) The origin of species by means of natural selection, 6th edn. Doubleday & Co., Garden City, NY.
- DiBattista, J.D., Berumen, M.L., Gaither, M.R., Rocha, L.A., Eble, J.A., Choat, J.H., Craig, M.T., Skillings, D.J. & Bowen, B.W. (2013) After continents divide: comparative phylogeography of reef fishes from the Red Sea and Indian Ocean. Journal of Biogeography, 40, 1170–1181.
- DiBattista, J.D., Waldrop, E., Rocha, L.A., Craig, M.T., Berumen, M.L. & Bowen, B.W. (2015a) Blinded by the bright: a lack of congruence between colour morphs, phylogeography and taxonomy for a cosmopolitan Indo-Pacific butterflyfish, Chaetodon auriga. Journal of Biogeography, 42, 1919–1929.
- DiBattista, J.D., Roberts, M., Baird, A.H. et al. (2015b) A review of contemporary patterns of endemism for shallow water reef fauna in the Red Sea. Journal of Biogeography. doi:10.1111/jbi.12689.
- Drew, J.A., Allen, G.R., Kaufman, L. & Barber, P.H. (2008) Regional color and genetic differences demonstrate endemism in five putatively cosmopolitan reef fishes. Conservation Biology, 22, 965–975.
- Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214–221.
- Eble, J.A., Toonen, R.J., Sorensen, L.L., Papastamatiou, Y. & Bowen, B.W. (2011) Escaping paradise: larval export from Hawaii in an Indo-Pacific reef fish, the yellow tang (Zebrasoma flavescens). Marine Ecology Progress Series, 428, 245–258.
- Ekman, S. (1953) Zoogeography of the sea. Sidgwick and Jackson, London, UK.
- Excoffier, L., Laval, G. & Schneider, S. (2010) arlequin version 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564–567.
- Fernandez-Silva, I., Randall, J.E., Coleman, R.R., DiBattista, J.D., Rocha, L.A., Reimer, J.D., Meyer, C.G. & Bowen, B.W. (2015) Yellow tails in a Red Sea: phylogeography of the Indo-Pacific goatfish Mulloidichthys flavolineatus reveals isolation in peripheral provinces and cryptic evolutionary lineages. Journal of Biogeography, 42, 2402–2413.
- Forsman, Z., Wellington, G.M., Fox, G.E. & Toonen, R.J. (2015) Clues to unraveling the coral species problem: distinguishing species from geographic variation in Porites across the Pacific with molecular markers and microskeletal traits. PeerJ, 3, e751.
- Fratini, S. & Vannini, M. (2002) Genetic differentiation in the mud crab Scylla serrata (Decapoda: Portunidae) within the Indian Ocean. Journal of Experimental Marine Biology and Ecology, 272, 103–116.
- Gaither, M.R. & Rocha, L.A. (2013) Origins of species richness in the Indo-Malay-Philippine biodiversity hotspot: evidence for the centre of overlap hypothesis. Journal of Biogeography, 40, 1638–1648.
- Gaither, M.R., Toonen, R.J., Robertson, R.R., Planes, S. & Bowen, B.W. (2010) Genetic evaluation of marine biogeographic barriers: perspectives from two widespread Indo-Pacific snappers (Lutjanus kasmira and Lutjanus fulvus). Journal of Biogeography, 37, 133–147.
- Gaither, M.R., Bowen, B.W., Bordenave, T.R., Newman, S.J., Gomez, J.A., van Herwerden, L. & Craig, M.T. (2011a) Phylogeography of the reef fish Cephalopholis argus (Epinephelidae) indicates Pleistocene isolation across the Indo-Pacific Barrier with contemporary overlap in the Coral Triangle. BMC Evolutionary Biology, 11, 189.
- Gaither, M.R., Jones, S.A., Kelley, C., Newman, S.J., Sorenson, L. & Bowen, B.W. (2011b) High connectivity in the deepwater snapper Pristipomoides filamentosus (Lutjanidae) across the Indo-Pacific with isolation in the Hawaiian Archipelago. PLoS ONE, 6, e28913.
- Gaither, M.R., Bernal, M.A., Coleman, R.R., Bowen, B.W., Jones, S.A., Simison, W.B. & Rocha, L.A. (2015) Genomic signatures of geographic isolation and natural selection in coral reef fishes. Molecular Ecology, 24, 1543–1557.
- George, R.W. (1974) Coral reefs and rock lobster ecology in the Indo-West Pacific region. Proceedings of the 2nd International Coral Reef Symposium, 1, 321–325.
- George, R.W. (2005) Tethys sea fragmentation and speciation of Panulirus spiny lobsters. Crustaceana, 78, 1281–1309.
- George, R.W. & Main, A.R. (1967) The evolution of spiny lobsters (Palinuridae): a study of evolution in the marine environment. Evolution, 21, 803–820.
- Gopal, K., Tolley, K.A., Groeneveld, J.C. & Matthee, C.A. (2006) Mitochondrial DNA variation in spiny lobster Palinurus delagoae suggests genetically structured populations in the southwestern Indian Ocean. Marine Ecology Progress Series, 319, 191–198.
- Hoareau, T.B., Boissin, E., Paulay, G. & Bruggemann, J.H. (2013) The Southwestern Indian Ocean as a potential marine evolutionary hotspot: perspectives from comparative phylogeography of reef brittle-stars. Journal of Biogeography, 40, 2167–2179.
- Holthuis, L.B. (1968) The Palinuridae and Scyllaridae of the Red Sea. Zoologische Mededelingen (Leiden), 42, 281–310.
- Holthuis, L.B. (1991) Marine lobsters of the world: an annotated and illustrated catalogue of species of interest to fisheries known to date. FAO Fisheries Synopsis, 13, 1–292 (FAO Species Catalogue, Rome).
- Holthuis, L.B. & Loesch, H. (1967) The lobsters of the Galápagos Islands (Decapoda, Palinuridae). Crustaceana, 12, 214–222.
10.1163/156854067X00620 Google Scholar
- Iacchei, M., Ben-Horin, T., Selkoe, K.A., Bird, C.E., García-Rodríguez, F.J. & Toonen, R.J. (2013) Combined analyses of kinship and FST suggest potential drivers of chaotic genetic patchiness in high gene flow populations. Molecular Ecology, 22, 3476–3494.
- Iacchei, M., O'Malley, J.M. & Toonen, R.J. (2014) After the gold rush: population structure of spiny lobsters in Hawai‘i following a fishery closure and the implications for contemporary spatial management. Bulletin of Marine Science, 90, 331–357.
- Jeffs, A.G., Montgomery, J.C. & Tindle, C.T. (2005) How do spiny lobster post-larvae find the coast? New Zealand Journal of Marine and Freshwater Research, 39, 605–617.
- Jensen, J.L., Bohonak, A.J. & Kelley, S.T. (2005) Isolation by distance, web service. BMC Genetics, 6, 13. v.3.23 http://ibdws.sdsu.edu/
- Johnson, M.W. (1968) Palinurid phyllosoma from the Hawaiian archipelago (Palinuridae). Crustaceana, S2, 59–79.
- Johnson, M.W. (1974) On the dispersal of lobster larvae into the East Pacific Barrier (Decapoda, Palinuridea). Fisheries Bulletin, 72, 639–647.
- Keyse, J., Crandall, E.D., Toonen, R.J., Treml, E.A. & Riginos, C. (2013) The scope of published population genetic data for Indo-Pacific marine fauna and future research opportunities. Bulletin of Marine Science, 90, 47–78.
- Klausewitz, W. (1989) Evolutionary history and zoogeography of the Red Sea ichthyofauna. Fauna of Saudi Arabia, 10, 310–337.
- Kulbicki, M., Parravicini, V., Bellwood, D.R., Arias-Gonzàlez, E., Chabanet, P., Floeter, S.R., Friedlander, A., McPherson, J., Myers, R.E., Vigliola, L. & Mouillot, D. (2013) Global biogeography of reef fishes: a hierarchical quantitative delineation of regions. PLoS ONE, 8, e81847.
- Lanfear, R., Calcott, B., Ho, S.Y. & Guindon, S. (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701.
- Lavery, S.D., Farhadi, A., Farahmand, H., Chan, T.Y., Azhdehakoshpour, A., Thakur, V. & Jeffs, A.G. (2014) Evolutionary divergence of geographic subspecies within the scalloped spiny lobster Panulirus homarus (Linnaeus 1758). PLoS ONE, 9, e97247.
- Lessios, H.A. & Robertson, D.R. (2006) Crossing the impassible: genetic connections in 20 reef fishes across the eastern Pacific barrier. Proceedings of the Royal Society B: Biological Sciences, 273, 2201–2208.
- Lessios, H.A., Kessing, B.D. & Robertson, D.R. (1998) Massive gene flow across the world's most potent marine biogeographic barrier. Proceedings of the Royal Society B: Biological Sciences, 265, 583–588.
- Malay, M.C.M.D. & Paulay, G. (2010) Peripatric speciation drives diversification and distributional pattern of reef hermit crabs (Decapoda: Diogenidae: Calcinus). Evolution, 64, 634–662.
- Matsuda, H., Takenouchi, T. & Goldstein, J.S. (2006) The complete larval development of the pronghorn spiny lobster Panulirus penicillatus (Decapoda: Palinuridae) in culture. Journal of Crustacean Biology, 26, 579–600.
- Mayr, E. (1954) Geographic speciation in tropical echinoids. Evolution, 8, 1–18.
- McCoy, E.D. & Heck, K.L. (1983) Centers of origin revisited. Paleobiology, 9, 17–19.
- McWilliam, P.S. (1995) Evolution in the phyllosoma and puerulus phases of the spiny lobster genus Panulirus White. Journal of Crustacean Biology, 15, 542–557.
- Mora, C., Treml, E.A., Roberts, J., Crosby, K., Roy, D. & Tittensor, D.P. (2012) High connectivity among habitats precludes the relationship between dispersal and range size in tropical reef fishes. Ecography, 35, 89–96.
- Naish, T., Powell, R., Levy, R. et al. (2009) Obliquity-paced Pliocene West Atlantic ice sheet oscillations. Nature, 458, 322–328.
- O'Malley, J.M., Drazen, J.C., Popp, B.N., Gier, E. & Toonen, R.J. (2012) Spatial variability in growth and prey availability of lobsters in the northwestern Hawaiian Islands. Marine Ecology Progress Series, 449, 211–220.
- Pitcher, C.R. (1993) Spiny Lobster. Nearshore marine resources of the South Pacific: information for fisheries development and management (ed. by A. Wright and L. Hill), pp. 539–607. Suva, Institute of Pacific Studies.
- Planes, S. & Fauvelot, C. (2002) Isolation by distance and vicariance drive genetic structure of a coral reef fish in the Pacific Ocean. Evolution, 56, 378–399.
- Plaut, I. & Fishelson, L. (1991) Population structure and growth in captivity of the spiny lobster Panulirus penicillatus from Dahab, Gulf of Aqaba, Red Sea. Marine Biology, 111, 467–472.
- Ptacek, M.B., Sarver, S.K., Childress, M.J. & Herrnkind, W.F. (2001) Molecular phylogeny of the spiny lobster genus Panulirus (Decapoda: Palinuridae). Marine and Freshwater Research, 52, 1037–1047.
- Randall, J.E. (1994) Twenty-two new records of fishes from the Red Sea. Fauna of Saudi Arabia, 14, 259–275.
- Reid, D.G., Lal, K., Mackenzie-Dodds, J., Kaligis, F., Littlewood, D.T.J. & Williams, S.T. (2006) Comparative phylogeography and species boundaries in Echinolittorina snails in the central Indo-West Pacific. Journal of Biogeography, 33, 990–1006.
- Robertson, D.R., Grove, J.S. & McCosker, J.E. (2004) Tropical transpacific shore fishes. Pacific Science, 58, 507–565.
10.1353/psc.2004.0041 Google Scholar
- Schultz, J.K., Feldheim, K.A., Gruber, S.H., Ashley, M.V., McGovern, T.M. & Bowen, B.W. (2008) Global phylogeography and seascape genetics of the lemon sharks (genus Negaprion). Molecular Ecology, 17, 5336–5348.
- Selkoe, K.A., Gaggiotti, O.E., Laboratory, ToBo, Bowen, B.W. & Toonen, R.J. (2014) Emergent patterns of population genetic structure for a coral reef community. Molecular Ecology, 23, 3064–3079.
- Shao, K.T., Chen, J.P. & Wang, S.C. (1999) Biogeography and database of marine fishes in Taiwan waters. Proceedings of the 5th Indo-Pacific Fish Conference, Noumea, 1997 (ed. by B. Seret and J.Y. Sire), pp. 673–680. Societe Francaise Ichthyologique, Paris.
- Siddall, M., Smeed, D.A., Hemleben, C., Rohling, E.J., Schmelzer, I. & Peltier, W.R. (2004) Understanding the Red Sea response to sea level. Earth and Planetary Science Letters, 225, 421–434.
- Skillings, D.J., Bird, C.E. & Toonen, R.J. (2011) Gateways to Hawai‘i: genetic population structure of the tropical sea cucumber Holothuria atra. Journal of Marine Biology, 2011, 783030.
10.1155/2011/783030 Google Scholar
- Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.
- Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725–2729.
- Toonen, R.J., Andrews, K.R., Baums, I.B. et al. (2011) Defining boundaries for ecosystem-based management: a multispecies case study of marine connectivity across the Hawaiian Archipelago. Journal of Marine Biology, 2011, 460173.
- Tourinho, J.L., Solé-Cava, A.M. & Lazoski, C. (2012) Cryptic species within the commercially most important lobster in the tropical Atlantic, the spiny lobster Panulirus argus. Marine Biology, 159, 1897–1906.
- Treml, E.A., Halpin, P.N., Urban, D.L. & Pratson, L.F. (2008) Modeling population connectivity by ocean currents, a graph-theoretic approach for marine conservation. Landscape Ecology, 23, 19–36.
- Truett, G.E., Mynatt, R.L., Truett, A.A., Walker, J.A. & Warman, M.L. (2000) Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and Tris (HotSHOT). BioTechniques, 29, 52–54.
- Ujiie, Y., Ujiie, H., Taira, A., Nakamura, T. & Oguri, K. (2003) Spatial and temporal variability of surface water in the Kuroshio source region, Pacific Ocean, over the past 21,000 years: evidence from planktonic foraminifera. Marine Micropaleontology, 49, 335–364.
- Voris, H.K. (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. Journal of Biogeography, 27, 1153–1167.
- Wyrtki, K., Firing, E., Halpern, D., Knox, R., McNally, G.H., Patzert, W.C., Stroup, E.D., Taft, B.A. & Williams, R. (1981) The Hawaii to Tahiti shuttle experiment. Science, 211, 22–28.