Abstract
Studies on the morphology, reproductive compatibility, life cycle and molecular phylogeny of the euryhaline red alga Caloglossa provide insights into the speciation events and biogeographic patterns. The C. leprieurii complex is separated into three morphotypes based on the number of cell rows at nodes and the blade width. The three morphotypes are reproductively incompatible with each other, and furthermore many mating groups are recognized within the morphotypes. Incomplete reproductive isolation is occasionally seen between geographically distant mating groups, whereas no sexual compatibility occurs between sympatrically or parapatrically distributed mating groups. In the molecular phylogenetic analyses, the C. leprieurii complex is resolved as two clusters that phenotypically correspond to the single and multiple cell row types, respectively. The strains belonging to the same mating group are closely related to each other, without exception, while the mating groups showing incomplete reproductive reactions do not always make a clade. The genetic distance is generally not correlative to the geographic distance, and this is also suggested by the morphological data and crossability. These results indicate that allopatric speciation has frequently occurred in this species complex, although there is some evidence of long-distance dispersal.
Similar content being viewed by others
References
Briggs JC (1994) Species diversity: land and sea compared. Syst Biol 43:130–135
Chapman VJ (1984) Mangrove biogeography. In: Por FD, Dor I (eds) Hydrobiology of the mangal. Junk, The Hague, pp 15–24
Chiang TY, Chiang YC, Chen YJ, Chou CH, Havanond S, Hong TN, Huang S (2001) Phylogeography of Kandelia candel in East Asiatic mangroves based on nucleotide variation of chloroplast and mitochondrial DNAs. Mol Ecol 10:2697–2710
Coates AG, Obando JA (1996) The geological evolution of the Central American Isthmus. In: Jackson JBC, Budd AF, Coates AG (eds) Evolution and environment in tropical America. University of Chicago Press, Chicago, pp 21–56
Destombe C, Douglas SE (1991) Rubisco spacer sequence divergence in the rhodohyte alga Gracilaria verrucosa and closely related species. Curr Genet 19:395–398
Duke NC (1995) Genetic diversity, distributional barriers and rafting continents—more thoughts on the evolution of mangroves. Hydrobiologia 295:167–181
Ellison AM, Farnsworth EJ, Merkt RE (1999) Origins of mangrove ecosystems and the mangrove biodiversity anomaly. Global Ecol Biogeogr 8:95–115
Guiry MD, Tripodi G, Lüning K (1987) Biosystematics, genetics and upper temperature tolerance of Gigartina teedii (Rhodophyta) from the Atlantic and Mediterranean. Helgol Meeresunters 41:283–295
Iwamoto K, Kawanobe H, Shiraiwa Y, Ikawa T (2001) Purification and characterization of mannitol-1-phosphatase in the red alga Caloglossa continua (Ceramiales, Rhodophyta). Mar Biotechnol 3:493–500
Iwamoto K, Kawanobe H, Ikawa T, Shiraiwa, Y (2003) Characterization of salt-regulated mannitol-1-phosphate dehydrogenase in the red alga Caloglossa continua. Plant Physiol 133:893–900
Kamiya M, Tanaka J, Hara Y (1995) A morphological study and hybridization analysis of Caloglossa leprieurii (Ceramiales, Rhodophyta) from Japan, Singapore and Australia. Phycol Res 43:81–91
Kamiya M, Tanaka J, Hara Y (1997) Comparative morphology, crossability, and taxonomy within the Caloglossa continua (Delesseriaceae, Rhodophyta) complex from the Western Pacific. J Phycol 33:97–105
Kamiya M, West JA, King RJ, Zuccarello GC, Tanaka J, Hara Y (1998) Evolutionary divergence in the red algae Caloglossa leprieurii and C. apomeiotica. J Phycol 34:361–370
Kamiya M, Tanaka J, King RJ, West JA, Zuccarello GC, Kawai H (1999) Reproductive and genetic distinction between broad and narrow entities of Caloglossa continua (Delesseriaceae, Rhodophyta). Phycologia 38:356–367
Kamiya M, West JA, Zuccarello GC, Kawai H (2000) Caloglossa intermedia sp. nov. (Rhodophyta) from the western Atlantic coast: molecular and morphological analyses with special reference to C. leprieurii and C. monosticha. J Phycol 36:411–420
Kamiya M, Zuccarello GC, West JA (2003) Evolutionary relationships of the genus Caloglossa (Delesseriaceae, Rhodophyta) inferred from large-subunit ribosomal RNA gene sequences, morphological evidence and reproductive compatibility, with description of a new species from Guatemala. Phycologia 42:478–497
Kamiya M, Zuccarello GC, West JA (2004) Phylogeography of Caloglossa leprieurii and related species (Delesseriaceae, Rhodophyta) based on the rbcL gene sequences. Jpn J Phycol 52:147–151 (supplement)
Karsten U, West JA (1993) Ecophysiological studies on six species of the mangrove red algal genus Caloglossa. Aust J Plant Physiol 20:729–739
Karsten U, Barrow KD, Nixdorf O, West JA, King RJ (1997) Characterization of mannitol metabolism in the mangrove red alga Caloglossa leprieurii (Montagne) J Agardh Planta 201:173–178
Karsten U, West JA, Zuccarello GC, Engbrodt R, Yokoyama A, Hara Y, Brodie J (2003) Low molecular weight carbohydrates of the Bangiophycidae (Rhodophyta). J Phycol 39:584–589
Knowlton N, Weigt LA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proc R Soc Lond B 265:2257–2263
McCoy ED, Heck KL Jr (1976) Biogeography of corals, seagrasses, and mangroves: an alternative to the center of origin concept. Syst Zool 25:201–210
McLachlan J, van der Meer JP, Bird NL (1977) Chromosome numbers of Gracilaria foliifera and Gracilaria sp. (Rhodophyta) and attempted hybridizations. J Mar Biol Assoc UK 57:1137–1141
Mepham RH (1983) Mangrove floras of the southern continents. Part 1. The geographical origin of Indo-Pacific mangrove genera and the development and present status of the Australian mangroves. S Afr J Bot 2:1–8
Palumbi SR (1994) Genetic divergence, reproductive isolation and marine speciation. Annu Rev Ecol Syst 25:547–572
Plastino EM, Oliveira EC de (1988) Sterility barriers among species of Gracilaria (Rhodophyta, Gigartinales) from the São Paulo littoral, Brazil. Br Phycol J 23:267–271
Rögl F, Steininger FF (1984) Neogene Paratethys, Mediterranean and Indo-Pacific seaways. Implications for the paleobiogeography of marine and terrestrial biotas. In: Brenchley PJ (ed) Fossils and climate. Wiley, Chichester, pp 171–200
Saenger P (1998) Mangrove vegetation: an evolutionary perspective. Mar Freshwater Res 49:277–286
Valentin K, Zetsche K (1990) Structure of the Rubisco operon from the unicellular red alga Cyanidium caldarium: evidence for a polyphyletic origin of the plastids. Mol Gen Genet 222:425–430
van den Hoek C (1987) The possible significance of long-range dispersal for the biogeography of seaweeds. Helgol Meeresunters 41:261–272
West JA, Zuccarello GC, Pedroche FF, Karsten U (1994) Caloglossa apomeiotica sp. nov. (Ceramiales, Rhodophyta) from Pacific México. Bot Mar 37:381–90
West JA, Zuccarello GC, Kamiya M (2001) Reproductive patterns of Caloglossa species (Delesseriaceae, Rhodophyta) from Australia and New Zealand: multiple origins of asexuality in C. leprieurii. Literature review on apomixis, mixed-phase, bisexuality and sexual compatibility. Phycol Res 49:183–200
Yoshizaki M, Fujita T, Hatogai T, Iura K (1985) Phenology on the three species of estuarine red algae from the Kidogawa river mouth area, Kujûkurihama, central Japan. Chiba Seibutsushi 35:64–70
Zuccarello GC, West JA (1995) Hybridization studies in Bostrychia. 1: B. radicans (Rhodomelaceae, Rhodophyta) from Pacific and Atlantic North America. Phycol Res 43:233–240
Zuccarello GC, West JA (1997) Hybridization studies in Bostrychia: 2. Correlation of crossing data and plastid DNA sequence data within B. radicans and B. moritziana (Ceramiales, Rhodophyta). Phycologia 36:293–304
Zuccarello GC, West JA (2002) Phylogeography of the Bostrychia calliptera–B. pinnata complex (Rhodomelaceae, Rhodophyta) and divergence rates based on nuclear, mitochondrial and plastid DNA markers. Phycologia 41:49–60
Zuccarello GC, West JA, King RJ (1999) Evolutionary divergence in the Bostrychia moritziana/B. radicans complex (Rhodomelaceae, Rhodophyta): molecular and hybridization data. Phycologia 38:234–244
Acknowledgments
I am grateful to Dr. J.A. West for critically reading and improving this manuscript. I sincerely thank Drs. J.A. West, G.C. Zuccarello, R.J. King, Y. Hara, J. Tanaka, and H. Kawai for their collaboration and helpful discussion. I am also indebted to many researchers for their suggestions, collections, and cultures of Caloglossa materials and loan of herbarium specimens. This work is financially supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Science and Culture, Japan, the Syowa Seitoku Memorial Foundation and the Fujiwara Natural History Foundation.
Author information
Authors and Affiliations
Corresponding author
Additional information
M. Kamiya is the recipient of the Botanical Society Award for Young Scientist, 2002.
Rights and permissions
About this article
Cite this article
Kamiya, M. Speciation and biogeography of the Caloglossa leprieurii complex (Delesseriaceae, Rhodophyta). J Plant Res 117, 421–428 (2004). https://doi.org/10.1007/s10265-004-0166-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-004-0166-2