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Tatsuya Togashi - One of the best experts on this subject based on the ideXlab platform.
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The Evolution of AnIsogamy: A Fundamental Phenomenon Underlying Sexual Selection - The evolution of anIsogamy: A fundamental phenomenon underlying sexual selection
2020Co-Authors: Tatsuya TogashiAbstract:Introduction Paul Alan Cox 1. The origin and maintenance of two sexes (anIsogamy), and their gamete sizes by gamete competition Geoff A. Parker 2. The evolutionary instability of Isogamy Hiroyuki Matsuda and Peter A. Abrams 3. Contact, not conflict, causes the evolution of anIsogamy Joan Roughgarden and Priya Iyer 4. Nucleo-cytoplasmic conflict and the evolution of gamete dimorphism Rolf F. Hoekstra 5. Adaptive significance of egg size variation of aquatic organisms in relation to mesoscale features of aquatic environments Kinya Nishimura and Noboru Hoshino 6. Gamete encounters David B. Dusenbery 7. Evolution of anIsogamy and related phenomena in marine green algae Tatsuya Togashi and John L. Bartelt Index.
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Evidence for equal size cell divisions during gametogenesis in a marine green alga Monostroma angicava
Scientific Reports, 2015Co-Authors: Tatsuya Togashi, Yusuke Horinouchi, Hironobu Sasaki, Jin YoshimuraAbstract:In cell divisions, relative size of daughter cells should play fundamental roles in gametogenesis and embryogenesis. Differences in gamete size between the two mating types underlie sexual selection. Size of daughter cells is a key factor to regulate cell divisions during cleavage. In cleavage, the form of cell divisions (equal/unequal in size) determines the developmental fate of each blastomere. However, strict validation of the form of cell divisions is rarely demonstrated. We cannot distinguish between equal and unequal cell divisions by analysing only the mean size of daughter cells, because their means can be the same. In contrast, the dispersion of daughter cell size depends on the forms of cell divisions. Based on this, we show that gametogenesis in the marine green alga, Monostroma angicava , exhibits equal size cell divisions. The variance and the mean of gamete size (volume) of each mating type measured agree closely with the prediction from synchronized equal size cell divisions. Gamete size actually takes only discrete values here. This is a key theoretical assumption made to explain the diversified evolution of Isogamy and anIsogamy in marine green algae. Our results suggest that germ cells adopt equal size cell divisions during gametogenesis.
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evolutionary trajectories explain the diversified evolution of Isogamy and anIsogamy in marine green algae
Proceedings of the National Academy of Sciences of the United States of America, 2012Co-Authors: Tatsuya Togashi, John L Bartelt, Jin Yoshimura, Keiichi TainakaAbstract:The evolution of anIsogamy (the production of gametes of different size) is the first step in the establishment of sexual dimorphism, and it is a fundamental phenomenon underlying sexual selection. It is believed that anIsogamy originated from Isogamy (production of gametes of equal size), which is considered by most theorists to be the ancestral condition. Although nearly all plant and animal species are anisogamous, extant species of marine green algae exhibit a diversity of mating systems including both Isogamy and anIsogamy. Isogamy in marine green algae is of two forms: Isogamy with extremely small gametes and Isogamy with larger gametes. Based on disruptive selection for fertilization success and zygote survival (theory of Parker, Baker, and Smith), we explored how environmental changes can contribute to the evolution of such complex mating systems by analyzing the stochastic process in the invasion simulations of populations of differing gamete sizes. We find that both forms of Isogamy can evolve from other isogamous ancestors through anIsogamy. The resulting dimensionless analysis accounts for the evolutionary stability of all types of mating systems in marine green algae, even in the same environment. These results imply that evolutionary trajectories as well as the optimality of gametes/zygotes played an important role in the evolution of gamete size.
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Underwater fertilization dynamics of marine green algae.
Bellman Prize in Mathematical Biosciences, 2006Co-Authors: Tatsuya Togashi, John L BarteltAbstract:We studied the fertilization dynamics of marine green algae with both analytical methods and numerical simulations. In this study, we focused on a new factor, gametic investment per unit volume of the space in which gametes searched for their partners, and compared the numbers of zygotes formed at lower investments with those at higher investments. As a function of the gametic investment for various anIsogamy ratios, we found there was generally a crossover region for each series where, for gametic investments larger than the crossover region, Isogamy prevailed with the highest number of zygotes formed, while for gametic investments smaller than the crossover region, anIsogamy dominated. These results may explain both the stable maintenance of Isogamy in shallow water and the distribution of anisogamous species in deep water, since in shallow water the gametic investments typically exceed this crossover region and vice versa. Comparisons of field data from marine green algae are consistent with this hypothesis. Also, we showed that the cost of sex was approximately twofold in zygote formation when comparing isogamous species with mating types to those without mating types.
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Simulation of gamete behaviors and the evolution of anIsogamy: reproductive strategies of marine green algae
Ecological Research, 2004Co-Authors: Tatsuya Togashi, John L BarteltAbstract:In marine green algae, isogamous or slightly anisogamous species are taxonomically widespread. They produce positively phototactic gametes in both sexes. We developed a new numerical simulator of gamete behavior using C++ and pseudo-parallelization methods to elucidate potential advantages of phototaxis. Input parameters were set based on experimental data. Each gamete swimming in a virtual rectangular test tank was tracked and the distances between the centers of nearby male and female were measured at each step to detect collisions. Our results shed light on the roles of gamete behavior and the mechanisms of the evolution of anIsogamy and more derived forms of sexual dimorphism. We demonstrated that not only gametes with positive phototaxis were favored over those without, particularly in shallow water. This was because they could search for potential mates on the 2-D water surface rather than randomly in three dimensions. Also, phototactic behavior clarified the difference between Isogamy and slight anIsogamy. Isogamous species produced more zygotes than slightly anisogamous ones only under the phototactic conditions. Our results suggested that ‘sperm limitation’ might be easily resolved particularly in the slightly anisogamous species. Some more markedly anisogamous species produce the smaller male gametes without any phototactic devices and the larger positively phototactic female gametes. In such species, female gametes attract their partners using a sexual pheromone. This pheromonal attraction system might have played a key role in the evolution of anIsogamy, because it could enable markedly anisogamous species achieve 2-D search efficiencies on the water surface. The mating systems appear to be tightly tuned o the environmental conditions of their habitats.
Jin Yoshimura - One of the best experts on this subject based on the ideXlab platform.
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Evidence for equal size cell divisions during gametogenesis in a marine green alga Monostroma angicava
Scientific Reports, 2015Co-Authors: Tatsuya Togashi, Yusuke Horinouchi, Hironobu Sasaki, Jin YoshimuraAbstract:In cell divisions, relative size of daughter cells should play fundamental roles in gametogenesis and embryogenesis. Differences in gamete size between the two mating types underlie sexual selection. Size of daughter cells is a key factor to regulate cell divisions during cleavage. In cleavage, the form of cell divisions (equal/unequal in size) determines the developmental fate of each blastomere. However, strict validation of the form of cell divisions is rarely demonstrated. We cannot distinguish between equal and unequal cell divisions by analysing only the mean size of daughter cells, because their means can be the same. In contrast, the dispersion of daughter cell size depends on the forms of cell divisions. Based on this, we show that gametogenesis in the marine green alga, Monostroma angicava , exhibits equal size cell divisions. The variance and the mean of gamete size (volume) of each mating type measured agree closely with the prediction from synchronized equal size cell divisions. Gamete size actually takes only discrete values here. This is a key theoretical assumption made to explain the diversified evolution of Isogamy and anIsogamy in marine green algae. Our results suggest that germ cells adopt equal size cell divisions during gametogenesis.
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evolutionary trajectories explain the diversified evolution of Isogamy and anIsogamy in marine green algae
Proceedings of the National Academy of Sciences of the United States of America, 2012Co-Authors: Tatsuya Togashi, John L Bartelt, Jin Yoshimura, Keiichi TainakaAbstract:The evolution of anIsogamy (the production of gametes of different size) is the first step in the establishment of sexual dimorphism, and it is a fundamental phenomenon underlying sexual selection. It is believed that anIsogamy originated from Isogamy (production of gametes of equal size), which is considered by most theorists to be the ancestral condition. Although nearly all plant and animal species are anisogamous, extant species of marine green algae exhibit a diversity of mating systems including both Isogamy and anIsogamy. Isogamy in marine green algae is of two forms: Isogamy with extremely small gametes and Isogamy with larger gametes. Based on disruptive selection for fertilization success and zygote survival (theory of Parker, Baker, and Smith), we explored how environmental changes can contribute to the evolution of such complex mating systems by analyzing the stochastic process in the invasion simulations of populations of differing gamete sizes. We find that both forms of Isogamy can evolve from other isogamous ancestors through anIsogamy. The resulting dimensionless analysis accounts for the evolutionary stability of all types of mating systems in marine green algae, even in the same environment. These results imply that evolutionary trajectories as well as the optimality of gametes/zygotes played an important role in the evolution of gamete size.
Hisayoshi Nozaki - One of the best experts on this subject based on the ideXlab platform.
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New "missing link" genus of the colonial volvocine green algae gives insights into the evolution of oogamy.
BMC Evolutionary Biology, 2014Co-Authors: Hisayoshi Nozaki, Toshihiro Yamada, Fumio Takahashi, Ryo Matsuzaki, Takashi NakadaAbstract:Background The evolution of oogamy from Isogamy, an important biological event, can be summarized as follows: morphologically similar gametes (isogametes) differentiated into small “male” and large “female” motile gametes during anIsogamy, from which immotile female gametes (eggs) evolved. The volvocine green algae represent a model lineage to study this type of sex evolution and show two types of gametic unions: conjugation between isogametes outside the parental colonies (external fertilization during Isogamy) and fertilization between small motile gametes (sperm) and large gametes (eggs) inside the female colony (internal fertilization during anIsogamy and oogamy). Although recent cultural studies on volvocine algae revealed morphological diversity and molecular genetic data of sexual reproduction, an intermediate type of union between these two gametic unions has not been identified.
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New “missing link” genus of the colonial volvocine green algae gives insights into the evolution of oogamy
BMC Evolutionary Biology, 2014Co-Authors: Hisayoshi Nozaki, Fumio Takahashi, Ryo Matsuzaki, Toshihiro K Yamada, Takashi NakadaAbstract:Background The evolution of oogamy from Isogamy, an important biological event, can be summarized as follows: morphologically similar gametes (isogametes) differentiated into small “male” and large “female” motile gametes during anIsogamy, from which immotile female gametes (eggs) evolved. The volvocine green algae represent a model lineage to study this type of sex evolution and show two types of gametic unions: conjugation between isogametes outside the parental colonies (external fertilization during Isogamy) and fertilization between small motile gametes (sperm) and large gametes (eggs) inside the female colony (internal fertilization during anIsogamy and oogamy). Although recent cultural studies on volvocine algae revealed morphological diversity and molecular genetic data of sexual reproduction, an intermediate type of union between these two gametic unions has not been identified. Results We identified a novel colonial volvocine genus, Colemanosphaera , which produces bundles of spindle-shaped male gametes through successive divisions of colonial cells. Obligately anisogamous conjugation between male and female motile gametes occurred outside the female colony (external fertilization during anIsogamy). This new genus contains 16- or 32-celled spheroidal colonies similar to those of the volvocine genera Yamagishiella and Eudorina . However, Colemanosphaera can be clearly distinguished from these two genera based on its sister phylogenetic position to the enigmatic flattened colonial volvocine Platydorina and external fertilization during anIsogamy. Two species of Colemanosphaera were found in a Japanese lake; these species are also distributed in European freshwaters based on a published sequence of an Austrian strain and the original description of Pandorina charkowiensis from Ukraine. Conclusions Based on phylogeny and morphological data, this novel genus exhibits a missing link between Platydorina and the typical spheroidal colonial volvocine members such as Pandorina or Yamagishiella . Considering the external obligate anIsogamy, oogamy evolution may have been preceded by the transition from external to internal fertilization during anIsogamy within the volvocine green algae.
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Origin of Female/Male Gender as Deduced by the Mating-Type Loci of the Colonial Volvocalean Greens
Sexual Reproduction in Animals and Plants, 2014Co-Authors: Hisayoshi NozakiAbstract:Colonial Volvocales (green algae) are a model lineage for the study of the evolution of sexual reproduction because Isogamy, anIsogamy, and oogamy are recognized within the closely related group, and several mating type (sex)-specific genes were identified in the closely related unicellular Chlamydomonas reinhardtii during the past century. In 2006, we first identified a sex-specific gene within the colonial Volvocales using the anisogamous colonial volvocalean alga Pleodorina starrii, namely, a male-specific gene called “OTOKOGI,” which is a homologue of the minus mating type-determining gene MID of the isogamous C. reinhardtii. Thus, it was speculated that the derived or minus mating type of C. reinhardtii is homologous to the male in the anisogamous/oogamous members of the colonial Volvocales. The discovery of the male-specific gene facilitated comparative studies of the mating-type locus (MT) (primitive sex chromosomal region) because it must be localized in MT. Recently, our international research group determined the genome sequence of MT in the oogamous Volvox carteri. V. carteri MT shows remarkable expansion and divergence relative to that from C. reinhardtii. Five new female-limited “HIBOTAN” genes and ten male-limited genes (including “OTOKOGI”) were identified in V. carteri MT. These observations suggest that the origins of femaleness and maleness are principally affected by the evolution of MT, which has undergone a remarkable expansion and gain of new male- and female-limited genes. Our recent results regarding the evolution of the volvocalean MT gene MAT3/RB are also discussed in relationship to the evolution of male–female sexual dimorphism.
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The Evolution of Male-Female Sexual Dimorphism Predates the Gender-Based Divergence of the Mating Locus Gene MAT3/RB
Molecular Biology and Evolution, 2013Co-Authors: Rintaro Hiraide, Ryo Matsuzaki, Takashi Hamaji, Hiroko Kawai-toyooka, James G. Umen, Kaoru Kawafune, Hiroyuki Sekimoto, Hisayoshi NozakiAbstract:The molecular bases for the evolution of male–female sexual dimorphism are possible to study in volvocine algae because they encompass the entire range of reproductive morphologies from Isogamy to oogamy. In 1978, Charlesworth suggested the model of ag amete size gene becoming linked to the sex-determinin go r mating type locus (MT )a s am echanism for the evolution of anIsogamy. Here, we carried out the first comprehensive study of a candidate MT-linked oogamy gene, MAT3/RB, across the volvocine lineage. We found that evolution of anIsogamy/oogamy predates the extremely high male–female divergence of MAT3 that characterizes the Volvox carteri lineage. These data demonstrate very little sex-linked sequence divergence of MAT3 between the two sexes in other volvocine groups, though linkage between MAT3 and the mating locus appears to be conserved. These data implicate genetic determinants other than or in addition to MAT3 in the evolution of anIsogamy in volvocine algae.
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A new male-specific gene “OTOKOGI” in Pleodorina starrii (Volvocaceae, Chlorophyta) unveils the origin of male and female
Biologia, 2008Co-Authors: Hisayoshi NozakiAbstract:Eukaryotic sex was initially isogametic and it is assumed that anIsogamy/oogamy evolved independently in many lineages including animals, land plants and volvocine green algae. The exact evolutionary mechanisms that were responsible for the evolution of oogamy from Isogamy were poorly understood until Nozaki et al. (2006) introduced the use of molecular-genetic data in elucidating the evolutionary origin of oogamy from Isogamy in the colonial volvocacean Pleodorina starrii . In the close relative Chlamydomonas reinhardtii , sexual reproduction is isogametic with mating-types plus and minus. Mating type minus represents a “dominant sex” because the MID (“minus-dominance”) gene of C. reinhardtii is both necessary and sufficient to cause the cells to differentiate as isogametes of the minus mating type. No sex-specific genes had been identified in the volvocine green algae until Nozaki et al. (2006a) successfully cloned the MID gene of P. starrii . This “ OTOKOGI ” ( PlestMID ) gene is present only in the male genome, and encodes a protein localized abundantly in the nuclei of mature sperm. Thus, P. starrii maleness evolved from the dominant sex (mating type minus) of its isogamous ancestor. This breakthrough provides an opportunity to address various extremely interesting questions regarding the evolution of oogamy and the male-female dichotomy.
Keiichi Tainaka - One of the best experts on this subject based on the ideXlab platform.
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evolutionary trajectories explain the diversified evolution of Isogamy and anIsogamy in marine green algae
Proceedings of the National Academy of Sciences of the United States of America, 2012Co-Authors: Tatsuya Togashi, John L Bartelt, Jin Yoshimura, Keiichi TainakaAbstract:The evolution of anIsogamy (the production of gametes of different size) is the first step in the establishment of sexual dimorphism, and it is a fundamental phenomenon underlying sexual selection. It is believed that anIsogamy originated from Isogamy (production of gametes of equal size), which is considered by most theorists to be the ancestral condition. Although nearly all plant and animal species are anisogamous, extant species of marine green algae exhibit a diversity of mating systems including both Isogamy and anIsogamy. Isogamy in marine green algae is of two forms: Isogamy with extremely small gametes and Isogamy with larger gametes. Based on disruptive selection for fertilization success and zygote survival (theory of Parker, Baker, and Smith), we explored how environmental changes can contribute to the evolution of such complex mating systems by analyzing the stochastic process in the invasion simulations of populations of differing gamete sizes. We find that both forms of Isogamy can evolve from other isogamous ancestors through anIsogamy. The resulting dimensionless analysis accounts for the evolutionary stability of all types of mating systems in marine green algae, even in the same environment. These results imply that evolutionary trajectories as well as the optimality of gametes/zygotes played an important role in the evolution of gamete size.
Scott Pitnick - One of the best experts on this subject based on the ideXlab platform.
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Intensity of sexual selection along the anIsogamy–Isogamy continuum
Nature, 2006Co-Authors: Adam Bjork, Scott PitnickAbstract:Research into the evolution of giant sperm has uncovered a paradox within the foundations of sexual selection theory. Postcopulatory sexual selection on males (that is, sperm competition and cryptic female choice) can lead to decreased sperm numbers by favouring the production of larger sperm^ 1 . However, a decline in sperm numbers is predicted to weaken selection on males and increase selection on females^ 2 , 3 . As Isogamy is approached (that is, as investment per gamete by males approaches that by females), sperm become less abundant, ova become relatively less rare, and competition between males for fertilization success is predicted to weaken. Sexual selection for longer sperm, therefore, is expected to be self limiting. Here we examine this paradox in Drosophila along the anIsogamy–Isogamy continuum using intraspecific experimental evolution techniques and interspecific comparative techniques. Our results confirm the big-sperm paradox by showing that the sex difference in sexual selection gradients^ 4 decreases as sperm size increases. However, a resolution to the paradox is provided when this finding is interpreted in concert with the ‘opportunity for selection’ and the ‘opportunity for sexual selection’^ 5 , 6 . Furthermore, we show that most of the variation in measures of selection intensity is explained by sperm length and relative investment in sperm production.
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intensity of sexual selection along the anIsogamy Isogamy continuum
Nature, 2006Co-Authors: Adam Bjork, Scott PitnickAbstract:Research into the evolution of giant sperm has uncovered a paradox within the foundations of sexual selection theory. Postcopulatory sexual selection on males (that is, sperm competition and cryptic female choice) can lead to decreased sperm numbers by favouring the production of larger sperm1. However, a decline in sperm numbers is predicted to weaken selection on males and increase selection on females2,3. As Isogamy is approached (that is, as investment per gamete by males approaches that by females), sperm become less abundant, ova become relatively less rare, and competition between males for fertilization success is predicted to weaken. Sexual selection for longer sperm, therefore, is expected to be self limiting. Here we examine this paradox in Drosophila along the anIsogamy–Isogamy continuum using intraspecific experimental evolution techniques and interspecific comparative techniques. Our results confirm the big-sperm paradox by showing that the sex difference in sexual selection gradients4 decreases as sperm size increases. However, a resolution to the paradox is provided when this finding is interpreted in concert with the ‘opportunity for selection’ and the ‘opportunity for sexual selection’5,6. Furthermore, we show that most of the variation in measures of selection intensity is explained by sperm length and relative investment in sperm production.
