Inducible Anisogamy and the Evolution of Oogamy from Isogamy

The initial and decisive step in the evolution of oogamy fromisogamy involves the generation of size different gamete typesin isogamous ancestors. Recent data with isogamous dioeciousChlamydomonas species reveal a potential for the evolution ofanisogamy which can be demonstrated experimentally. These speciespossess, in each sex, two different pathways of gametogenesis.A vegetative cell may produce just one large gamete by intracellulardifferentiation or may produce four small gametes by means oftwo gametogenic mitoses. Combination of sexually complementarygametes of different production modes creates phenotypicallya distinctly anisogamous copulation. At this developmental potential,any mutation which fixes one or the other mode of gametogenesiswill establish micro- or macrogamete producers. Such geneticallyanisogamous lines will then be subjected to selection for increasinglydivergent evolution of the gametic differentiation. Chlamydomonas spp, anisogamy, oogamy, evolution     

Positive size–speed relationships in gametes and vegetative cells of Chlamydomonas reinhardtii; implications for the evolution of sperm

It is commonly held that differences in gametes of the two sexes (anisogamy) evolved from ancestors whose gametes were similar in size and behavior (isogamy). Underlying many hypotheses explaining anisogamy are assumed relationships between cell size and speed in the ancestral isogamous population. Using the isogamous alga Chlamydomonas reinhardtii, we explored size–speed distributions in vegetative and gamete cells of 10 cell lines, and clonal data from within two cell lines. We applied an independent speed selection approach to gamete populations of C. reinhardtii, monitoring correlated responses in size following selection for high speed. We demonstrate positive size–speed relationships in clones, cell lines, and artificially selected speed selection lines. We found different size–speed relationships in the two cell types of C. reinhardtii even though they overlap in size, suggesting that cell composition and/or programs of gene expression are capable of altering this relationship, and that the relationship is evolvable. The positive genetic size‐speed correlation means that the division of parent vegetative cells into numerous gametes trades off against not only size, but also speed, a trade‐off that has not received previous attention. Our results support reevaluating the role of speed selection in the evolution of anisogamy.     

Underwater fertilization dynamics of marine green algae

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.     

The evolution of anisogamy: the adaptive significance of damage, repair and mortality

Classic theory on the evolution of anisogamy focuses on the trade-off between gamete productivity and provisioning and mechanisms associated with post-zygotic survival. In this article, the role of mortality acting on both zygotes and gametes is explored as a factor influencing the evolution of different sized gametes. In particular, variable mortality through differential survival or metabolic damage is shown to affect the persistence of isogamy, the evolution of more than two sexes and the evolution of anisogamy. Evolutionary stable isogamous states are shown to be locally unstable and disruptive selection can induce the evolution of anisogamy. Analysis of both the isogamous and anisogamous ESS points reveals that the persistence of either of these conditions is not always assured. The implications of variable survival on the evolution of anisogamy are discussed.     

Parasite diversity and the evolution of diploidy, multicellularity and anisogamy

It may be reasonably assumed that a diversity of parasite genotypes in any one cell or organism is more harmful than a population of uniform genotypes. If this is accepted the following consequences follow: (i) Parasite mixing, due to cytoplasm mixing, at the time of zygote formation is a new and additional cost of sex. The rapid divisions typical of zygotic cleavage may be viewed as an adaptation to minimize the degree of mixing of parasites in each daughter cell. The faster the divisions the less chance parasite populations have to grow and mix. Mitosis is the fastest form of cell division. Prolongation of the diploid phase follows as a consequence of mitosis in a diploid zygote. This view is unusual in that it demands no advantage per se to the possession of two chromosome sets. (ii) The cells of the blastula formed from rapid zygotic divisions are different as regards their symbiotic inclusions. If the right to gametogenesis is restricted, then every replicator symbiont and nuclear genome alike and hence every cell of the developing embryo, will have an incentive to compete. Selection between the clonal blastula cells would result in the cells of low parasite diversity forming the gametes. Thus, germ line restriction is in the interests of the nuclear genome. Controlling the right to gametogenesis is only possible if the blastula remains intact. Hence, multicellularity might have evolved so as to enable the limitation of the right to gametogenesis and hence reduce the parasite diversity of gametes. Inter-cell competition during embryogenesis is central to Buss's seminal notion of the evolution of developmental complexity within the metazoa. The above theory provides the missing motive force behind such competition. (iii) For a given zygote size, the fittest zygotes are those produced by the gametes most disparate in size because these have a lower diversity of parasites. This may be the advantage of anisogamy. The novelty of this new view of anisogamy is that it puts a premium on sperm being very small, in order to exclude parasites from sperm cytoplasm. The hypothesis is briefly tested by examining if there are alternative means of parasite limitation in organisms with large gametes.     

The costs of sex due to deleterious intracellular parasites

A major problem in evolutionary theory is to explain the widespread occurrence of sexual recombination. This is particularly difficult in anisogamous species where the familiar ‘two-fold cost of sex’ is encountered. Another cost has recently been identified: that fusion of gametes allows intracellular parasites or deleterious ‘selfish’ genomes to invade a population. These costs of anisogamy and the ability of cytoplasmic agents to invade a sexual population are quantified, allowing the costs and consequences of different modes of reproduction to be compared. It is found that the costs of selfish elements are likely to be very high and, in particular, that isogamous sexual reproduction (the putative ‘primitive’ form) is not cost-free, but incurs a fitness reduction of the order of 90%; thus a large selective disadvantage occurs in the initial evolution of sex which is ignored in standard analysis. Even once anisogamy has evolved, the low levels of ‘paternal leakage’ observed in many extant organisms may allow selfish cytoplasmic elements to spread, resulting in moderate to large decreases in host population fitness. However, much of the cost of selfish elements is avoided in sexual lifecycles with a large number of asexual cellular divisions between sexual reproduction: this greatly impedes the spread of selfish agents and reduces the fitness loss attributable to selfish elements.     

Phototaxis and the evolution of isogamy and 'slight anisogamy' in marine green algae: insights from laboratory observations and numerical experiments

The evolution of anisogamy in marine algae was studied through numerical simulations of gamete mating behaviour in three dimensions, using observed traits of marine green algae as input parameters. The importance of phototaxis became apparent from the numerical experiments: all gametes with phototactic systems are favoured over those without, but this advantage is reduced with increasing tank depth or shorter search times. Phototactic gametes were advantaged over non-phototactic gametes if the water was shallower than about 30–40 mm when the time available for gamete encounter was 1000 time steps (5.55 min). If gametes of both sexes are positively phototactic, slightly anisogamous species are at a disadvantage to isogamous species, which invalidates the sperm-limitation theory as a driver for the evolution of slight anisogamy. Conflicting selection forces of search efficiency and zygote fitness may be needed.  © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society , 2004, 144 , 321–327.     

Gametic differentiation in Chlamydomonas reinhardi: cell cycle dependency and rates in attainment of mating competency

Withdrawal of a utilizable nitrogen source during mid G₁ of the cell cycle induces gametic differentiation in synchronously grown vegetative cultures of Chlamydomonas reinhardi. Cell division accompanies gametic differentiation in such cultures, and the ability of mid G₁ vegetative cells to form gametes is matched by their ability to undergo a round of cell division after nitrogen withdrawal. Synchronously grown cultures require up to 19 hr in nitrogen-free medium to complete a round of division and to form mating-competent cells. Asynchronously grown liquid cultures require less time after nitrogen withdrawal (generally 5–8 hr) to achieve mating competency. In these cultures cell division did not necessarily accompany gametic differentiation since gametic differentiation took place in induced cultures at high cell concentrations which prevented cell division. Maximum mating competency was achieved in less than 2 hr after induction of vegetative cells grown on agar plates. Little cell division was observed during that short induction interval. The relationship between the attainment of mating competency (gametogenesis) and other physiological events resulting from nitrogen withdrawal is discussed.     

Simulation of gamete behaviors and the evolution of anisogamy: reproductive strategies of marine green algae

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.     

Population genetic aspects of deleterious cytoplasmic genomes and their effect on the evolution of sexual reproduction.

A conflict of interest may arise between intra-cellular genomes and their host cell. The example explicitly investigated is that of a 'selfish' mitochondrion which increases its own rate of replication at the cost of reduced metabolic activity which is deleterious to the host cell. The results apply to deleterious cytoplasmic agents in general, such as intracellular parasites. Numerical simulation suggests that selfish mitochondria are able to invade an isogamous sexual population and are capable of reducing its fitness to below 5% of that prior to their invasion. Their spread is enhanced by decreasing the number of mitotic divisions between meioses, and this may constitute a significant constraint on the evolution of lifecycles. The presence of such deleterious cytoplasmic agents favours a nuclear mutation whose expression prevents cytoplasm from the other gamete entering the zygote at fertilization, resulting in uniparental inheritance of cytoplasm. Such a mutation appears physiologically plausible and can increase in frequency despite its deleterious effect in halving the amount of cytoplasm in the zygote. It is suggested that these were the conditions under which anisogamy evolved. These results have implications for the evolution of sexual reproduction. Standard theory suggests there is no immediate cost of sex, a twofold cost being incurred later as anisogamy evolves. The analysis described here predicts a large, rapid reduction in fitness associated with isogamous sexual reproduction, due to the spread of deleterious cytoplasmic agents with fitness only subsequently rising to a maximum twofold cost as uniparental inheritance of cytoplasm and anisogamy evolve.     

On sexual agglutination and mating type substances in isogamous dioecious Chlamydomonads: IV. Unilateral inactivation of the sex contact capacity in compatible and incompatible taxa by α-mannosidase and snake venom protease

Sex cell contact at fertilization is analysed in the mating type reaction of isogamous Chlamydomonas species. Contact is based upon a complementarity between special mating type substances, sex and species specific glycoprotein complexes. In three related taxa, the contact capactiy of their (+) gamete type is sensitive to snake venom protease (α-protease) and depends decisively on terminal α-glycosidically bound mannose residues. Enzymatic removal of these residues by α-mannosidase incapacitates live (+) gametes and inactivates isolated (+) mating type substance. (+) gametes inactivated by α-mannosidase or α-protease do not agglutinate with (?) gametes nor respond to isolated (?) mating type substance. Isolated (?) substance is adsorbed to and inactivated by the homologous (+) gametes. (+) gametes incapacitated by α-mannosidase or α-protease do not adsorb nor inactivate the isolated (?) substance. The agglutinability of live (?) gametes and the contact capacity of isolated (?) mating type substance is not affected by α-mannosidase or α-protease. The mannose residues react only within the species-typical complementarity. Some additional feature(s) of the (+) mating type substances must effect their species specificity and account for gametic isolation and sexual incompatibility between species.     

Letter: Notes on "heat loss from a Newtonian animal"

Parker, Baker &; Smith (1972) have demonstrated mathematically that given the evolution of sexual reproduction, disruptive selection for the production of either many small gametes or a few large gametes may occur, resulting in a stable polymorphism of “sperm” and “egg” producers. Their model for the evolution of anisogamy requires only that zygote fitness (F) increase steeply with increases in zygote volume (V) (for Foc∝ V^x, x must be greater than 1·5) and that a sufficiently broad range of zygote productivity-size variants exist in the population (the higher the value of x, the broader the range needed). They suggest that anisogamy is almost universal in multicellular organisms but relatively rare in unicellular organisms because only for the former is an investment in extra gametic reserves at the expense of the number of gametes produced likely to be worthwhile in terms of increasing the survival probability of the zygote. In this note a graphical analysis and evidence from the anisogamous Protista will be presented concerning this hypothesis.     

Differentiation of generative and vegetative cells in angiosperm pollen

 Cellular differentiation of a generative and a vegetative cell is an important event during microspore and pollen development and is requisite for double fertilization in angiosperms. The generative cell produces two sperm cells, or male gametes, whereas the vegetative cell produces an elongated pollen tube, a gametophytic cell, to deliver the male gametes to the embryo sac. For typical differentiation of the gametic and gametophytic cells, cell polarity, including nuclear positioning, must be established prior to microspore mitosis and be maintained during mitosis. Microtubules are closely involved in the process of asymmetric cell division. On the other hand, alteration of the chromatin composition seems to be responsible for the differential gene expression between the generative and vegetative cells. Cytoplasmic regulatory molecules, which affect chromatin configuration, are postulated to be unequally distributed to the two cells at the asymmetric cell division. Thus, typical differentiation of the cells is accomplished by a cellular mechanism and a molecular mechanism, which might be independent of each other. These results are discussed in relation to one model that accounts for the different fates of generative and vegetative cells during sexual plant reproduction. Received: 3 September 1996 / Revision accepted: 23 September 1996     

Production of anisogametes and gamete motility dimorphism in Monostroma angicava

 The reproductive strategy of a marine alga with a heteromorphic biphasic life cycle was studied by analyzing various sexual reproductive characters in light of the evolution of anisogamy. Gametophytes of Monostroma angicava were dioecious and their gametes were slightly anisogamous. Volume of gametangium, density of gametangia and area of mature gametangial parts on each gametophyte did not differ from male to female. Therefore, the reproductive biomass investment for gamete production was considered to be the same for each sex. Anisogamy in this alga appeared to be derived from the difference in the number of cell divisions during gametogenesis, because the majority of male gametangia each produced 64 (2⁶) gametes and the female produced 32 (2⁵) gametes. This corresponded with measurements of cell size in male and female gametes. Further, the sex ratio was 1:1 for sexually mature plants sampled at Charatsunai. Therefore, it was suggested that in the field twice as many male gametes are released as female gametes. Liberated gametes of both sexes showed positive phototaxis. The swimming velocity of freshly liberated male gametes was a little higher than that of female gametes. Male gametes had the potential to swim for ca. 72 h and female gametes for ca. 84 h. The difference in gamete motility between the two sexes seemed to be related to cell size. Planozygotes were negatively phototactic and swam more rapidly than gametes of either sex. Received: 5 March 1997 / Revision accepted: 18 July 1997     

Auxosporulation of Licmophora communis (Bacillariophyta) and a review of mating systems and sexual reproduction in araphid pennate diatoms

The auxosporulation of Licmophora communis is allogamous and dioecious. Pairing between sessile, shortstalked cells of compatible clones is followed by meiosis and gametogenesis, to form two gametes in each gametangium. The behavior of the gametes differs between the gametangia. In the male gametangium, the gametes detach from the frustule, round up, and migrate out of the gametangium after its dehiscence at the broader, unattached pole. In the female gametangium, both gametes remain attached to the adjacent theca over almost their whole length and do not move. Plasmogamy therefore occurs within the female gametangium and this is where the zygotes are formed and remain. After fertilization, the zygotes detach from the thecae of the female gametangia, contract, and become ellipsoidal, before expanding parallel to the apical axis of the gametangium. We review the types of auxosporulation in other pennate diatoms and the systems used for classifying these. Dioecy and cis‐type anisogamy (in which one gametangium produces active gametes and the other produces passive gametes), as in L. communis, are probably primitive within the pennate group (although there is no information on the AsterionellopsisRhaphoneis clade). However, size can also be restored in various araphid pennates by allogamous sexual reproduction involving the formation of only one gamete per gametangium, or in rare cases by automixis or (apparently) vegetative enlargement.     

Gamete signalling underlies the evolution of mating types and their number

The gametes of unicellular eukaryotes are morphologically identical, but are nonetheless divided into distinct mating types. The number of mating types varies enormously and can reach several thousand, yet most species have only two. Why do morphologically identical gametes need to be differentiated into self-incompatible mating types, and why is two the most common number of mating types? In this work, we explore a neglected hypothesis that there is a need for asymmetric signalling interactions between mating partners. Our review shows that isogamous gametes always interact asymmetrically throughout sex and argue that this asymmetry is favoured because it enhances the efficiency of the mating process. We further develop a simple mathematical model that allows us to study the evolution of the number of mating types based on the strength of signalling interactions between gametes. Novel mating types have an advantage as they are compatible with all others and rarely meet their own type. But if existing mating types coevolve to have strong mutual interactions, this restricts the spread of novel types. Similarly, coevolution is likely to drive out less attractive mating types. These countervailing forces specify the number of mating types that are evolutionarily stable.This article is part of the themed issue ‘Weird sex: the underappreciated diversity of sexual reproduction’.     

Morphology and evolution of sexual reproduction in the Volvocaceae (Chlorophyta)

Morphological features of sexual reproduction in the Volvocaceae are reviewed, focusing particularly on gametic union and zygote gemination. Both of the two conjugating gametes of the isogamous generaPandorina, Volvulina andYamagishiella bear a tubular mating structure (mating papilla), and plasmogamy is initiated by union of the papillae tips. On zygote germination, a single biflagellate gone cell is released from the zygote wall. Although all the anisogamous and oogamous genera of the Volvocaceae produce “sperm packets” during gametogenesis and a single gone cell at zygote germination, some difference can be recognized in the male gametes. The male gametes ofEudorina bear a tubular cytoplasmic protuberance (putative mating papllla) near the base of the flagella, whereas such a structure recognized at the light microscopic level is not evident inPleodorina andVolvox. Evolution of the sexual reproduction characteristics of volvocacean algae is discussed on the basis of recent cladistic analysis of morphological data as well as of the ribosomal (r) RNA phylogeny and large subunit of the ribulose-1, 5-biphosphate carboxylase/oxygenase(rbcL) gene trees. Dedicated to Emeritus Prof. Hideo Kasaki (Tokyo Metropolitan University) on the occasion of his 77th birthday. Recipient of the Botanical Society Award for Young Scientists, 1994.     

Tipping and mating-structure activation induced in Chlamydomonas gametes by flagellar membrane antisera

Antisera raised against vegetative and gametic flagella of Chlamydomonas reinhardi have been used to probe dynamic properties of the flagellar membranes. The antisera, which agglutinate cells via their flagella, associate with antigens that are present on both vegetative and gametic membranes and on membranes of both mating types (mt+ and mt-). Gametic cells respond to antibody presentation very differently from vegetative cells, mobilizing even high concentrations of antibody towards the flagellar tips; the possibility is discussed that such "tipping" ability reflects a differentiated gametic property relevant to sexual agglutinability. Gametic cells also respond to antibody agglutination by activating their mating structures, the mt+ reaction involving a rapid polymerization of microfilaments. Several impotent mt+ mutant strains that fail to agglutinate sexually are also activated by the antisera and procede to form zygotes with normal mt- gametes. Fusion does not occur between activated cells of like mating type. Monovalent (Fab) preparations of the antibody fail to activate mt+ gametes, suggesting that the cross-linking properties of the antisera are essential for their ability to mimic, or bypass, sexual agglutination.     

Unilateral tunicamycin sensitivity of gametogenesis in dioecious isogamous chlamydomonas species

Sex cell adhesion in isogamous chlamydomonads is caused by a complementarity between sex-specific mating type substances, glycoproteins anchored in the flagella membrane of (+) and (\documentclass{article}\pagestyle{empty}\begin{document}$ \mathop - \limits^. $\end{document}) gametes. The systems of mating type substances are species-specific and condition, by their individuality, gametic incompatibility between species. The adhesion systems of several species share one common feature: the attainment of the agglutination capacity is sensitive to tunicamycin, but in one sex only. The effect is interpreted as due to the interference of tunicamycin with the synthesis of the mating type substances by blocking of their glycosylation in one but not in the other sex. It is postulated that the tunicamycin-sensitive gametic adhesiveness depends, within the mating-type-specific glycoprotein, on an N-glycosidically bound ligand of carbohydrate nature. A concept on the origin of sibling species by mutative modulations within the proper ligands of the glycoproteinaceous mating type substances is developed.