Oogamy: Inventing the Sexes
2006; Elsevier BV; Volume: 16; Issue: 24 Linguagem: Inglês
10.1016/j.cub.2006.11.015
ISSN1879-0445
Autores Tópico(s)Biocrusts and Microbial Ecology
ResumoThe male–female dichotomy has evolved independently in nearly all lineages of multicellular organisms. Why this should be the case is still uncertain, but recent studies of mating-type genes in green algae open a promising new way to explore molecular-genetic aspects of the evolution of dichotomous sexes. The male–female dichotomy has evolved independently in nearly all lineages of multicellular organisms. Why this should be the case is still uncertain, but recent studies of mating-type genes in green algae open a promising new way to explore molecular-genetic aspects of the evolution of dichotomous sexes. We probably all feel that, as private individuals, we have an intimate knowledge of sex, but biologists who study sex have long felt compelled to admit the extent of their ignorance. This is well illustrated by three quotes from knowledgeable pundits spanning more than a century: "we do not even in the least know why new beings should be produced by the union of two sexual elements, instead of by…parthenogenesis" [1Darwin C. The two forms, or dimorphic condition, in the species of Primula, and on their remarkable sexual relation.J. Proc. Linn. Soc. (Botany). 1862; 6: 77-96Crossref Google Scholar]; "sex has always been an embarrassment to population biologists" [2Bell G. The evolution of anisogamy.J. Theor. Biol. 1978; 73: 247-270Crossref PubMed Scopus (75) Google Scholar]; and "empirically, we really know very little about sex" [3Agrawahl A.F. Evolution of sex: Why do organisms shuffle their genotypes?.Curr. Biol. 2006; 16: R696-R704Abstract Full Text Full Text PDF PubMed Scopus (124) Google Scholar]. Two questions in particular have puzzled evolutionary biologists for many generations [1Darwin C. The two forms, or dimorphic condition, in the species of Primula, and on their remarkable sexual relation.J. Proc. Linn. Soc. (Botany). 1862; 6: 77-96Crossref Google Scholar, 2Bell G. The evolution of anisogamy.J. Theor. Biol. 1978; 73: 247-270Crossref PubMed Scopus (75) Google Scholar, 3Agrawahl A.F. Evolution of sex: Why do organisms shuffle their genotypes?.Curr. Biol. 2006; 16: R696-R704Abstract Full Text Full Text PDF PubMed Scopus (124) Google Scholar, 4Geddes P. Thompson J.A. The Evolution of Sex.Second Edition. Scott, New York1901Crossref Google Scholar, 5Parker G.A. Baker R.R. Smith V.G.F. The origin and evolution of gamete dimorphism and the male–female phenomenon.J. Theor. Biol. 1972; 36: 529-553Crossref PubMed Scopus (365) Google Scholar, 6Williams G.C. Sex and Evolution. Princeton University Press, Princeton, NJ1975Google Scholar, 7Maynard Smith J. The Evolution of Sex. Cambridge University Press, London1978Google Scholar, 8Bell G. The Masterpiece of Nature: The Evolution and Genetics of Sexuality. University of California Press, Berkeley, CA1982Google Scholar, 9Ghiselin M.T. The evolution of sex: A history of competing points of view.in: Michod R.E. Levin B.R. The Evolution of Sex: An Examination of Current Ideas. Sinauer, Sunderland, MA1988: 7-23Google Scholar]. First, given that sexually reproducing organisms pass on only half as many genes to each of their offspring as organisms that reproduce parthenogenetically, why is parthenogenesis so rare, and sexual reproduction so common among eukaryotes? And second, as eukaryotic sex was almost certainly initially isogametic — involving fusion of morphologically similar gametes — what selective advantage accounts for the fact that there have been so many independent evolutionary inventions of oogamy, in which tiny, motile male gametes fuse with large, immotile female gametes? (The many groups in which oogamy has evolved independently include animals, fungi, red algae, brown algae and several different kinds of green algae, including the ancestors of the land plants and the algal group that will be discussed below.) A number of answers have been proposed for each of those questions, but the point has not yet been reached where either question has been answered to the satisfaction of all of those who worry about such things [8Bell G. The Masterpiece of Nature: The Evolution and Genetics of Sexuality. University of California Press, Berkeley, CA1982Google Scholar, 9Ghiselin M.T. The evolution of sex: A history of competing points of view.in: Michod R.E. Levin B.R. The Evolution of Sex: An Examination of Current Ideas. Sinauer, Sunderland, MA1988: 7-23Google Scholar, 10Randerson J.P. Hurst L.D. A comparative test of a theory for the evolution of anisogamy.Proc. Roy. Soc. Lond. B. 2001; 268: 879-884Crossref PubMed Scopus (36) Google Scholar]. However, a study by Nozaki et al.[11Nozaki H. Mori T. Misumi S. Koroiwa T. Males evolved from the dominant isogametic mating type.Curr. Biol. 2006; 16: R1018-R1020Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar], reported in this issue of Current Biology, opens a highly promising new route for elucidating the molecular nature — if not the ultimate cause — of the evolutionary pathway from isogamy to oogamy in a group of closely related, recently evolved organisms known as the volvocine green algae. It has been said of the volvocine algae that "Few groups…hold such a fascination for evolutionary biologists… It is almost as if [they] were designed to exemplify the process of evolution" [12Bell G. The origin and early evolution of germ cells as illustrated by the Volvocales.in: Halvorson H.O. Monroy A. The Origin and Evolution of Sex. Alan R. Liss, New York1985: 221-256Google Scholar]. Members of this group range in size and complexity from Chlamydomonas, a biflagellate unicell, to Volvox, a spherical multicellular organism with a division of labor between thousands of small, terminally differentiated, biflagellate somatic cells, and a few large, non-motile reproductive cells. Between those phylogenetic extremes lies an assortment of colonial genera that have traditionally been included in the family Volvocaceae, such as Gonium, Pandorina and Eudorina, which contain 8, 16 or 32 identical biflagellate, Chlamydomonas-like cells, plus Pleodorina, which never has more than 128 cells, but exhibits a germ–soma division of labor resembling that of Volvox. Nozaki et al.[11Nozaki H. Mori T. Misumi S. Koroiwa T. Males evolved from the dominant isogametic mating type.Curr. Biol. 2006; 16: R1018-R1020Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar] studied a newly discovered species of Pleodorina called P. starrii[13Nozaki H. Ott F.D. Coleman A.W. Morphology, molecular phylogeny and taxonomy of two new species of Pleodorina (Volvocaceae, Chlorophyceae).J. Phycol. 2006; 42: 1072-1080Crossref Scopus (47) Google Scholar]. A simplified version of a molecular phylogeny of the volvocine algae, including P. starrii, that was based on comparative sequencing of five chloroplast genes [13Nozaki H. Ott F.D. Coleman A.W. Morphology, molecular phylogeny and taxonomy of two new species of Pleodorina (Volvocaceae, Chlorophyceae).J. Phycol. 2006; 42: 1072-1080Crossref Scopus (47) Google Scholar, 14Nozaki H. Origin and evolution of the genera Pleodorina and Volvox (Volvocales).Biologia (Bratislava). 2003; 58: 425-431Google Scholar], is shown in Figure 1. A considerable amount of effort has gone into exploring the cellular and molecular changes that underly the evolution of multicellularity and cellular differentiation in this group of algae [15Kirk D.L. A twelve-step program for evolving multicellularity and a division of labor.BioEssays. 2004; 27: 299-310Crossref Scopus (209) Google Scholar]. But new work of Nozaki et al.[11Nozaki H. Mori T. Misumi S. Koroiwa T. Males evolved from the dominant isogametic mating type.Curr. Biol. 2006; 16: R1018-R1020Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar] opens the way for an entirely new kind of study: a molecular-genetic analysis of the evolution of oogamy. In the unicellular alga C. reinhardtii, sexual reproduction is isogamous; that is, it involves fusion of gametes that are of two different mating types — mating-type plus (MT+) and mating-type minus (MT−) — but are similar in size and motility. Several of the smaller colonial volvocine algae are similarly isogamous. But other volvocaceans, and particularly the larger ones, are oogamous (Figure 1): in these species, small, motile sperm produced by males find and fuse with large, non-motile eggs produced by females (Figure 2). Indeed, it has been shown that in these volvocaceans there is a statistically significant increase in the ratio of egg volume to sperm volume with increasing adult size [2Bell G. The evolution of anisogamy.J. Theor. Biol. 1978; 73: 247-270Crossref PubMed Scopus (75) Google Scholar, 10Randerson J.P. Hurst L.D. A comparative test of a theory for the evolution of anisogamy.Proc. Roy. Soc. Lond. B. 2001; 268: 879-884Crossref PubMed Scopus (36) Google Scholar, 12Bell G. The origin and early evolution of germ cells as illustrated by the Volvocales.in: Halvorson H.O. Monroy A. The Origin and Evolution of Sex. Alan R. Liss, New York1985: 221-256Google Scholar], just as the dominant model for the evolution of gamete dimorphism [5Parker G.A. Baker R.R. Smith V.G.F. The origin and evolution of gamete dimorphism and the male–female phenomenon.J. Theor. Biol. 1972; 36: 529-553Crossref PubMed Scopus (365) Google Scholar] predicts. Ferris and Goodenough [16Ferris P. Goodenough U.W. Mating type in Chlamydomonas is specified by mid, the minus-dominance gene.Genetics. 1997; 146: 859-869PubMed Google Scholar] laid the groundwork for the work of Nozaki et al.[11Nozaki H. Mori T. Misumi S. Koroiwa T. Males evolved from the dominant isogametic mating type.Curr. Biol. 2006; 16: R1018-R1020Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar] by cloning the MID (minus-dominance) gene of C. reinhardtii, and showing that it encodes a putative transcriptional regulator that is both necessary and sufficient to cause C. reinhardtii cells to differentiate and mate as MT− cells. Nozaki et al.[11Nozaki H. Mori T. Misumi S. Koroiwa T. Males evolved from the dominant isogametic mating type.Curr. Biol. 2006; 16: R1018-R1020Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar] used primers based on the C. reinhardtii MID gene sequence to amplify and clone the MID ortholog of an oogamous species, P. starrii, and have demonstrated that this 'PlestMID' gene is present only in the male strain, is expressed in males only after spermatogenesis has been induced by starvation, and encodes a protein that eventually becomes localized abundantly in the nuclei of mature sperm. From these observations, Nozaki et al.[11Nozaki H. Mori T. Misumi S. Koroiwa T. Males evolved from the dominant isogametic mating type.Curr. Biol. 2006; 16: R1018-R1020Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar] infer that P. starrii males are descendents of the dominant (MT−) strain of their isogamous ancestor. This is the first time that a genetic connection has been established between one of the sexes of an oogamous species and one of the mating types of its isogamous ancestor. The story certainly will not end there, however, because the MID gene of Gonium pectorale has already been cloned, and efforts to clone the MID genes of other volvocaceans and study their action are now underway (H. Nozaki, personal communication). This breakthrough provides an opportunity to address any number of extremely interesting questions, of which the following are but a sample. Can the connection between MID and maleness be generalized to other species of oogamous volvocaceans? In particular, does that connection exist in species on the V. rousseletii branch of the family tree (Figure 1), where it appears that oogamy may have arisen independently? Will a MID transgene turn a female volvocacean into a male? (So far, V. carteri is the only species in which this question could be addressed, because that is the only oogamous species for which a nuclear transformation system has been developed.) Is the MID gene present in 'homothallic' Volvox species, which produce eggs and sperm within a single clone [17Starr R.C. Cellular differentiation in Volvox.Proc. Natl. Acad. Sci. USA. 1968; 59: 1082-1088Crossref PubMed Scopus (36) Google Scholar]? If so, does MID get selectively activated in sexual male cells and/or repressed in sexual female cells? It has been reported that, under certain circumstances, ultra-violet irradiation of a male strain of V. carteri causes a high-frequency, heritable gender reversal, producing 'she-males' [18Starr R.C. Jaenicke L. Cell differentiation in Volvox carteri (Chlorophyceae): the use of mutants in understanding pattern and control.in: Coleman A.W. Goff L.J. Stein J.R. Algae as Experimental Systems. Alan R. Liss, New York1989: 135-147Google Scholar]. What is the state of the MID locus in such she-males? Pandorina morum exists in nature as at least 20 reproductively isolated syngens, each of which consists of two mating types [19Coleman A.W. Sexual isolation in Pandorina morum.J. Protozool. 1959; 6: 249-264Crossref Scopus (58) Google Scholar]. Is there greater variation at the MID locus in P. morum than in other volvocacean species? Or is all the variation between syngens in the genes whose expression is regulated by MID? And, finally (at least for the moment), what are the genes that are under the control of the MID locus, and how different are they in isogamous and oogamous species? It appears that the breakthrough reported by Nozaki et al.[11Nozaki H. Mori T. Misumi S. Koroiwa T. Males evolved from the dominant isogametic mating type.Curr. Biol. 2006; 16: R1018-R1020Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar] will provide enough exciting new opportunities to keep them and many other investigators busy for some time to come!
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