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7 - Evolution of anisogamy and related phenomena in marine green algae

Published online by Cambridge University Press:  19 May 2011

By
Tatsuya Togashi  and
John L. Bartelt
Edited by
Tatsuya Togashi  and
Paul Alan Cox
Tatsuya Togashi
Affiliation:
Chiba University, Kamogawa, Japan
John L. Bartelt
Affiliation:
Evolutionary Programming, San Clemente, California
Tatsuya Togashi
Affiliation:
Chiba University, Japan
Paul Alan Cox
Affiliation:
Institute for Ethnomedicine
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Summary

INTRODUCTION

External fertilization is a reproductive strategy, common to invertebrates and algae in aquatic environments. In this chapter, we focus mainly on marine green algae, and as well as other algae if they are useful for understanding the evolution of anisogamy. In contrast to the consistency of oogamous animals, various types of mating systems from isogamy to pronounced anisogamy are observed in marine green algae; this facilitates comparisons of different reproductive strategies. This biological group, therefore, represents a superb opportunity to examine patterns of sexual allocation and gamete size versus a suite of ecologically relevant factors (e.g. dioecious versus monoecious life history, size of gametophytes, density of gametophytes in nature, and type of habitats). This study makes remarkable progress in the study of the evolution of anisogamy beyond theoretical speculation. If we know how the evolution of anisogamy happened, we might begin to see why it happened.

In green algae, the freshwater green algal order Volvocales has played an important role as the traditional testing ground for Parker, Baker, and Smith's model (hereafter the PBS model) (Parker et al., 1972, see also Parker's chapter, Chapter 1) (Knowlton, 1974; Madsen and Waller, 1983; Bell, 1985; Randerson and Hurst, 2001a). Although it is useful for study since this group has various types of mating systems from isogamy to strong anisogamy, it violates an important assumption of the PBS model. The PBS model assumes broadcast fertilization without any parental care.

Type
Chapter
Information
The Evolution of Anisogamy
A Fundamental Phenomenon Underlying Sexual Selection
 , pp. 194 - 242
Publisher: Cambridge University Press
Print publication year: 2011

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References

Bell, G. (1978). The evolution of anisogamy. Journal of Theoretical Biology, 73, 247–270.CrossRefGoogle ScholarPubMed
Bell, G. (1985). The origin and early evolution of germ cells as illustrated by the Volvocales. In Halvorson, H. O. and Monroy, A. (editors), The Origin and Evolution of Sex. New York: Alan R. Liss, pp. 221–256.Google Scholar
Bennoun, P., Delosme, M., and Kuck, U. (1991). Mitochondrial genetics of Chlamydomonas reinhardtii: resistance mutations marking the cytochrome b gene. Genetics, 127, 335–343.Google ScholarPubMed
Bonsall, M. B. (2006). The evolution of anisogamy: the adaptive significance of damage, repair and mortality. Journal of Theoretical Biology, 238, 198–210.CrossRefGoogle ScholarPubMed
Brawley, S. H. (1992). Fertilization in natural populations of the dioecious brown alga Fucus ceranoides and the importance of the polyspermy block. Marine Biology, 113, 145–157.CrossRefGoogle Scholar
Bray, D. (1992). Cell swimming. In Bray, D. (editor), Cell Movements. New York: Garland, pp. 3–16.Google Scholar
Bulmer, M. (1994). Theoretical Evolutionary Ecology. Sunderland, MA: Sinauer Associates.Google Scholar
Bulmer, M. G. and Parker, G. A. (2002). The evolution of anisogamy: a game-theoretic approach. Proceedings of the Royal Society of London B, 269, 2381–2388.CrossRefGoogle ScholarPubMed
Burr, F. A. and West, J. A. (1970). Light and electron microscope observations on the vegetative and reproductive structures ofBryopsis hypnoides. Phycologia, 9, 17–37.CrossRefGoogle Scholar
Chapman, V. J., Edmonds, A. S., and Drogmoole, F. I. (1964). Halicystis in New Zealand. Nature, 202, 414.CrossRefGoogle Scholar
Charlesworth, B. (1978). The population genetics of anisogamy. Journal of Theoretical Biology, 73, 347–357.CrossRefGoogle ScholarPubMed
Charnov, E. L. (1982). The Theory of Sex Allocation. Princeton, NJ: Princeton University Press.Google ScholarPubMed
Chihara, M. (1969). Culture study of Chlorochytrium inclusum from the northeast Pacific. Phycologia, 8, 127–133.CrossRefGoogle Scholar
Clifton, K. E. (1997). Mass spawning by green algae on coral reefs. Science, 275, 1116–1118.CrossRefGoogle ScholarPubMed
Clifton, K. E. and Clifton, L. M. (1999). The phenology f sexual reproduction by green algae (Bryopsidales) on Caribbean coral reefs. Journal of Phycology, 35, 24–34.CrossRefGoogle Scholar
Coleman, A. W. (1999). Phylogenetic analysis of “Volvocacae” for comparative genetic studies. Proceedings of the National Academy of Sciences of the United States of America, 96, 13892–13897.CrossRefGoogle ScholarPubMed
Cosmides, L. M. and Tooby, J. (1981). Cytoplasmic inheritance and intragenomic conflict. Journal of Theoretical Biology, 89, 83–129.CrossRefGoogle ScholarPubMed
Cox, P. A. (1981). Niche partitioning between sexes of dioecious plants. American Naturalist, 117, 295–307.CrossRefGoogle Scholar
Cox, P. A. (1983). Search theory, random motion, and the convergent evolution of pollen and spore morphology in aquatic plants. American Naturalist, 121, 9–31.CrossRefGoogle Scholar
Cox, P. A. and Sethian, J. A. (1985). Gamete motion, search, and the evolution of anisogamy, oogamy, and chemotaxis. American Naturalist, 125, 74–101.CrossRefGoogle Scholar
Darwin, C. R. (1871). The Descent of Man, and Selection in Relation to Sex. London: J. Murray.Google Scholar
Denny, M. W., Dairiki, J., and Distefano, S. (1992). Biological consequences of topography on wave-swept rocky shores: I. Enhancement of external fertilization. Biological Bulletin, 183, 220–232.CrossRefGoogle ScholarPubMed
Denny, M. W. and Shibata, M. F. (1989). Consequences of surf-zone turbulence for settlement and external fertilization. American Naturalist, 134, 859–889.CrossRefGoogle Scholar
Wreede, R. E. and Klinger, T. (1988). Reproductive strategies in algae. In Doust, J. L. and Doust, L. L. (editors), Plant Reproductive Ecology. Oxford: Oxford University Press, pp. 267–284.Google Scholar
Dusenbery, D. B. (2000). Selection for high gamete encounter rates explains the success of male and female mating types. Journal of Theoretical Biology, 202, 1–10.CrossRefGoogle ScholarPubMed
Fisher, R. A. (1930). The Genetical Theory of Natural Selection. Oxford: Clarendon Press.CrossRefGoogle Scholar
Fletcher, R. L. (1980). Studies of the recently introduced brown alga Sargassum muticum (Yendo) Fensholt: III. Periodicity in gamete release and “incubation” of early germling stages. Botanica Marina, 23, 425–432.Google Scholar
Geider, R. J. and Osborne, B. A. (1992). Algal Photosynthesis. New York: Chapman and Hall.CrossRefGoogle Scholar
Goldberger, M. L. and Watson, K. M. (2004). Collision Theory. Mineola, NY: Dover Publications.Google Scholar
Hamilton, W. D. (1967). Extraordinary sex ratios. Science, 156, 477–488.CrossRefGoogle ScholarPubMed
Hanyuda, T., Arai, S., and Ueda, K. (2000). Variability in the rbcL lntrons of Caulerpalean algae (Chlorophyta, Ulvophyceae). Journal of Plant Research, 113, 403–413.CrossRefGoogle Scholar
Harvey, P. H. and Purvis, A. (1991). Comparative methods for explaining adaptations. Nature, 351, 619–624.CrossRefGoogle ScholarPubMed
Hastings, I. M. (1999). The cost of sex due to deleterious intracellular parasites. Journal of Evolutionary Biology, 12, 177–183.CrossRefGoogle Scholar
Hiraoka, M. and Enomoto, S. (1998). The induction of reproductive cell formation of Ulva pertusa Kjellman (Ulvales, Ulvophyceae). Phycological Research, 46, 199–203.CrossRefGoogle Scholar
Hoek, C., Mann, D. G., and Jahns, H. M. (1996). Algae: An Introduction to Phycology, Cambridge: Cambridge University Press.Google Scholar
Hoekstra, R. F. (1980). Why do organisms produce gametes of only two different sizes? Some theoretical aspects of the evolution of anisogamy. Journal of Theoretical Biology, 87, 785–793.CrossRefGoogle ScholarPubMed
Hoekstra, R. F. (1984). Evolution of gamete motility differences II. Interaction with the evolution of anisogamy. Journal of Theoretical Biology, 107, 71–83.CrossRefGoogle Scholar
Hoekstra, R. F., Janz, R. F., and Schilstra, A. J. (1984). Evolution of gamete motility differences I. Relation between swimming speed and pheromonal attraction. Journal of Theoretical Biology, 107, 57–70.CrossRefGoogle Scholar
Hommersand, M. H. and Fredericq, S. (1990). Sexual reproduction and cytocarp development. In Cole, K. M. and Sheath, R. G. (editors), Biology of the Red Algae. Cambridge: Cambridge University Press, pp. 305–346.Google Scholar
Hurst, L. D. and Hamilton, W. D. (1992). Cytoplasmic fusion and the nature of sexes. Proceedings of the Royal Society of London. B, 247, 189–194.CrossRefGoogle Scholar
Jones, E. W. and Babb, S. M. (1968). The motile period of swarmers of Enteromorpha intestinalis (L.). Link. European Journal of Phycology, 3, 525–528.Google Scholar
Kagami, Y., Mogi, Y., Arai, T., et al. (2008). Sexuality and uniparental inheritance of chloroplast DNA in the isogamous green alga Ulva compressa (Ulvophyceae). Journal of Phycology, 44, 691–702.CrossRefGoogle Scholar
Kapraun, D. F. (1994). Cytophotometric estimation of nuclear DNA contents in thirteen species of the Caulerpales (Chlorophyta). Cryptogamic Botany, 4, 410–418.Google Scholar
Karlin, S. and Lessard, S. (1986). Theoretical Studies on Sex Ratio Evolution. Princeton, NJ: Princeton University Press.Google ScholarPubMed
Knowlton, N. (1974). A note on the evolution of gamete dimorphism. Journal of Theoretical Biology, 46, 283–285.CrossRefGoogle ScholarPubMed
Lam, D. W. and Zechman, F. W. (2006). Phylogenetic analyses of the Bryopsidales (Ulvophyceae, Chlorophyta) based on rubisco large subunit gene sequences. Journal of Phycology, 42, 669–678.CrossRefGoogle Scholar
Levitan, D. R. (1991). Influence of body size and population density on fertilization success and reproductive output in a free spawning invertebrate. Biological Bulletin, 181, 261–268.CrossRefGoogle Scholar
Levitan, D. R. (1993). The importance of sperm limitation to the evolution of egg size in marine invertebrates. American Naturalist, 141, 517–536.CrossRefGoogle ScholarPubMed
Levitan, D. R. (1996). Effects of gamete traits on fertilization in the sea and the evolution of sexual dimorphism. Nature, 382, 153–155.CrossRefGoogle Scholar
Levitan, D. R. (1998). Sperm limitation, gamete competition, and sexual selection in external fertilizers. In Birkhead, T. R. and Møller, A. P. (editors), Sperm Competition and Sexual Selection. San Diego, CA: Academic Press, pp. 173–215.Google Scholar
Levitan, D. R. (2000). Optimal egg size in marine invertebrates: theory and phylogenetic analysis of the critical relationship between egg size and development time in Echinoids. American Naturalist, 156, 175–192.CrossRefGoogle ScholarPubMed
Lloyd, D. G. (1982). Selection of combined versus separate sexes in seed plants. American Naturalist, 120, 571–585.CrossRefGoogle Scholar
Løvlie, A. and Bryhni, E. (1976). Signal for cell fusion. Nature, 263, 779–781.CrossRefGoogle ScholarPubMed
Madsen, J. D. and Waller, D. M. (1983). A note on the evolution of gamete dimorphism in algae. American Naturalist, 121, 443–447.CrossRefGoogle Scholar
Maier, I. (1993). Gamete orientation and induction of gametogenesis by pheromones in algae and plants. Plant, Cell and Environment, 16, 891–907.CrossRefGoogle Scholar
Maier, I. and Müller, D. G. (1986). Sexual pheromones in algae. Biological Bulletin, 170, 145–175.CrossRefGoogle Scholar
Matsuda, H. and Abrams, P. A. (1999). Why are equally sized gametes so rare? The instability of isogamy and the cost of anisogamy. Evolutionary Ecology Research, 1, 769–784.Google Scholar
Maynard Smith, J. (1978). The Evolution of Sex. Cambridge: Cambridge University Press.Google Scholar
Maynard Smith, J. (1982). Evolution and the Theory of Games. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Meinesz, A. (1980). Connaisances actuelles et contribution a l'etude de la reproduction et du cyle des Udoteacees (Caulerpales, Chlorophytes). Phycologia, 19, 110–138.CrossRefGoogle Scholar
Melkonian, M. (1980). Flagellar roots, mating structure and gametic fusion in the green alga Ulva lactuca (Ulvales). Journal of Cell Science, 46, 149–169.Google Scholar
Melkonian, M. (1982). Structural and evolutionary aspects of the flagellar apparatus in green algae and land plants. Taxon, 31, 255–265.CrossRefGoogle Scholar
Melkonian, M. and Robenek, H. (1984). The eyespot apparatus of flagellated green algae: a critical review. In Round, F. E. and Chapman, D. J. (editors), Progress in Phycological Research, Vol. 3. Bristol: Biopress, pp. 193–268.Google Scholar
Mine, I., Okuda, K., and Tatewaki, M. (1996). Gamete discharge by Bryopsis plumosa (Codiales, Chlorophyta) induced by blue and UV-A light. Phycological Research, 44, 185–191.CrossRefGoogle Scholar
Miyaji, K. (1985). Taxonomic Studies on the Genus Spongomorpha in Japan. Unpublished Ph.D. thesis, Hokkaido University.Google Scholar
Neumann, D. (1989). Circadian components of semilunar and lunar timing mechanisms. Journal of Biological Rhythms, 4, 285–294.CrossRefGoogle ScholarPubMed
Norton, T. A. (1981). Gamete expulsion and release in Sargassum muticum. Botanica Marina, 24, 465–470.CrossRefGoogle Scholar
Nozaki, H. (1988). Morphology, sexual reproduction and taxonomy of Volvox carteri f. kawasakiensis f. nov. (Chlorophyta) from Japan. Phycologia, 27, 209–220.CrossRefGoogle Scholar
Nozaki, H., Misawa, K., Kajita, T., et al. (2000). Origin and evolution of the colonial Volvocales (Chlorophyceae) as inferred from multiple, chloroplast gene sequences. Molecular Phylogenetics and Evolution, 17, 256–268.CrossRefGoogle ScholarPubMed
Okubo, A. and Levin, S. A. (2001). The basics of diffusion. In Okubo, A. and Levin, S. A. (editors), Diffusion and Ecological Problems, 2nd edn. New York: Springer, pp. 10–30.CrossRefGoogle Scholar
Okuda, K., Enomoto, S., and Tatewaki, M. (1979). Life history of Pseudobryopsis sp. (Codiales, Chlorophyta). Japanese Journal of Phycology, 27, 7–16.Google Scholar
Parker, G. A. (1978). Selection on non-random fusion of gametes during the evolution of anisogamy. Journal of Theoretical Biology, 73, 1–28.CrossRefGoogle ScholarPubMed
Parker, G. A., Baker, R. R., and Smith, V. G. F. (1972). The origin and evolution of gamete dimorphism and the male–female phenomenon. Journal of Theoretical Biology, 36, 529–553.CrossRefGoogle ScholarPubMed
Podolsky, R. D. and Strathmann, R. R. (1996). Evolution of egg size in free-spawners: consequences of the fertilization-fecundity trade-off. American Naturalist, 148, 160–173.CrossRefGoogle Scholar
Purcell, E. M. (1977). Life at low Reynolds number. American Journal of Physics, 45, 3–11.CrossRefGoogle Scholar
Randerson, J. P. and Hurst, L. D. (2001a). A comparative test of a theory for the evolution of anisogamy. Proceedings of the Royal Society of London B, 268, 879–884.CrossRefGoogle ScholarPubMed
Randerson, J. P. and Hurst, L. D. (2001b). The uncertain evolution of the sexes. Trends in Ecology and Evolution, 16, 571–579.CrossRefGoogle Scholar
Reboud, X. and Zeyl, C. (1994). Organelle inheritance in plants. Heredity, 72, 132–140.CrossRefGoogle Scholar
Reed, D. C., Laur, D. R., and Ebeling, A. W. (1988). Variation in algal dispersal and recruitment: the importance of episodic events. Ecological Monographs, 58, 321–335.CrossRefGoogle Scholar
Rietema, H. (1971). Life-history studies in the genus Bryopsis (Chlorophyceae) IV. Life-histories in Bryopsis hypnoides Lamx, from different points along the European coasts. Acta Botanica Neerlandica, 20, 291–298.CrossRefGoogle Scholar
Roth, W. C. and Friedmann, E. I. (1977). Development of the siphonous green alga Penicillus and the espera state. Botanical Journal of the Linnean Society, 74, 189–214.Google Scholar
Schmeisser, E. T., Baumgartel, D. M., and Howell, S. H. (1973). Gametic differentiation in Chlamydomonas reinhardtii: cell cycle dependency and rates in attainment of mating competency. Developmental Biology, 31, 31–37.CrossRefGoogle Scholar
Schuster, P. and Sigmund, K. (1982). A note on the evolution of sexual dimorphism. Journal of Theoretical Biology, 94, 107–110.CrossRefGoogle ScholarPubMed
Seger, J. and Stubblefield, J. M. (2002). Models of sex ratio evolution. In Hardy, I. C. W. (editor), Sex Ratios: Concepts and Research Methods. Cambridge: Cambridge University Press, pp. 2–25.CrossRefGoogle Scholar
Serrão, E. A., Pearson, G., Kautsky, L., and Brawley, S. H. (1996). Successful external fertilization in turbulent environments. Proceedings of the National Academy of Sciences of the United States of America, 93, 5286–5290.CrossRefGoogle ScholarPubMed
Starr, R. C., Marner, F. J., and Jaenicke, L. (1995). Chemoattraction of male gametes by a pheromone produced by female gametes of Chlamydomonas. Proceedings of National Academy of Sciences of the United States of America, 92, 641–645.CrossRefGoogle ScholarPubMed
Stratmann, J., Paputsoglu, G., and Oertel, W. (1996). Differentiation of Ulva mutabilis (Chlorophyta) gametangia and gamete release are controlled by extracellular inhibitors. Journal of Phycology, 32, 1009–1021.CrossRefGoogle Scholar
Tatewaki, M. (1966). Formation of a crustaceous sporophyte with unilocular sporangia in Scytosiphon lomentaria. Phycologia, 6, 62–66.CrossRefGoogle Scholar
Tatewaki, M. (1969). Culture studies on the life histories of some species of the genusMonostroma. Scientific Papers of the Institute of Algological Research, Faculty of Science, Hokkaido University, 6, 1–56.Google Scholar
Tatewaki, M. (1972). Life history and systematics in Monostroma. In Abbott, A. and Kurogi, M. (editors), Contributions to the Systematic of the Benthic Marine Algae of the North Pacific. Kobe: Japanese Society of Phycology, pp. 1–16.Google Scholar
Tatewaki, M. (1977). Life history of Bryopsis ryukyuensis YAMADA. Bulletin of the Japanese Society of Phycology, 25, 353–360.Google Scholar
Tatewaki, M. and Iima, M. (1984). Life histories of Blidingia minima (Chlorophyceae), especially sexual reproduction. Journal of Phycology, 20, 368–376.CrossRefGoogle Scholar
Togashi, T. (1998). Reproductive Strategies, Mating Behaviors and the Evolution of Anisogamy in Marine Green Algae. Unpublished Ph.D. thesis, Hokkaido University.Google Scholar
Togashi, T. and Cox, P. A. (2001). Tidal-linked synchrony of gamete release in the marine green alga, Monostroma angicava Kjellman. Journal of Experimental Marine Biology and Ecology, 264, 117–131.CrossRefGoogle Scholar
Togashi, T. and Cox, P. A. (2004). Phototaxix and the evolution of isogamy and “slight anisogamy” in marine green algae: insights from laboratory observations and numerical experiments. Botanical Journal of the Linnean Society, 144, 321–327.CrossRefGoogle Scholar
Togashi, T. and Cox, P. A. (2008). Equal sex ratios of a marine green alga, Bryopsis plumosa (Hudson) C. Agardh. Journal of Integrative Plant Biology, 50, 648–652.CrossRefGoogle Scholar
Togashi, T., Bartelt, J. L. and, Cox, P. A. (2004). Simulation of gamete behaviors and the evolution of anisogamy: reproductive strategies of marine green algae. Ecological Research, 19, 563–569.CrossRefGoogle Scholar
Togashi, T., Cox, P. A., and Bartelt, J. L. (2007). Underwater fertilization dynamics of marine green algae. Mathematical Biosciences, 209, 205–221.CrossRefGoogle ScholarPubMed
Togashi, T., Motomura, T., and Ichimura, T. (1997). Production of anisogametes and gamete motility dimorphism in Monostroma angicava. Sexual Plant Reproduction, 10, 261–268.CrossRefGoogle Scholar
Togashi, T., Motomura, T., and Ichimura, T. (1998). Gamete dimorphism in Bryopsis plumosa. Phototaxis, gamete motility and pheromonal attraction. Botanica Marina, 41, 257–264.CrossRefGoogle Scholar
Togashi, T., Motomura, T., Ichimura, T., and Cox, P. A. (1999). Gametic behavior in a marine green alga, Monostroma angicava: an effect of phototaxis on mating efficiency. Sexual Plant Reproduction, 12, 158–163.CrossRefGoogle Scholar
Togashi, T., Nagisa, M., Miyazaki, T., et al. (2006). Gamete behaviors and the evolution of “marked anisogamy”: reproductive strategies and sexual dimorphism in Bryopsidales marine green algae. Evolutionary Ecology Research, 8, 617–628.Google Scholar
Togashi, T., Sakisaka, Y., Miyazaki, T., et al. (in press). Evolution of gamete size in primitive taxa without mating types. Population Ecology.
Tsubo, Y. (1961). Chemotaxis and sexual behavior in Chlamydomonas. Journal of Protozoology, 8, 114–121.CrossRefGoogle Scholar
Vance, R. R. (1973). On reproductive strategies in marine bottom invertebrates. Amrican Naturalist, 107, 339–352.CrossRefGoogle Scholar
Vogel, H., Czihak, G., Chang, P., and Wolf, W. (1982). Fertilization kinetics of sea urchin eggs. Mathematical Biosciences, 58, 189–216.CrossRefGoogle Scholar
Wiese, L. (1981). On the evolution of anisogamy from isogamous monoecy and on the origin of sex. Journal of Theoretical Biology, 89, 573–580.CrossRefGoogle ScholarPubMed
Wiese, L., Wiese, W., and Edwards, D. A. (1979). Inducible anisogamy and the evolution of oogamy from isogamy. Annals of Botany, 44, 131–139.CrossRefGoogle Scholar

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