Ecological models explaining the success of distinctive sperm and eggs (oogamy)

Several lineages have independently evolved from isogamy (all sexes producing similar gametes) through anisogamy (dissimilar gametes) to the familiar male (producing sperm) and female (producing eggs) condition of most large, multicellular organisms (oogamy). A variety of hypotheses explaining the selective mechanisms causing such evolution and the success of these lineages have been proposed, but little evidence and some confusion persists. Here, a few simplifying assumptions are used to extract and compare the essential features of the various ecological hypotheses. The comparisons reveal that the critical need is to identify a selective advantage of large, immobile gametes (eggs). Assumptions about the effect of sperm size on swimming speed are not important. The classic assumption of increasing zygote success with large size requires a relationship even stronger than survival proportional to volume, which seems unlikely and lacks empirical support. An assumption that eggs produce a pheromone sperm attractant leads, by established physical principles, to a more than sufficient advantage of large egg size. Without pheromones, combinations of increased target size and weaker increased zygote fitness or increased gamete longevity also provide sufficient selection.     

Selection for high gamete encounter rates explains the success of male and female mating types

Sexual reproduction occurs in many small eukaryotes by fusion of similar gametes (isogamy). In the absence of distinguishable sperm and eggs, male and female mating types are missing. However, species with distinct males and females have so prospered that almost all familiar plants and animals have these mating types. Why has sexual reproduction involving sperm and eggs been so successful? An answer is obtained by considering physical limitations on encounter rates between gametes. A biophysical model based on well-established relationships produces fitness landscapes for the evolution of gamete size and energy allocation between motility and pheromone production. These landscapes demonstrate that selection for high gamete encounter rates favors large, pheromone-producing eggs and small, motile sperm. Thus, broadcast-spawning populations with males and females can reproduce at lower population densities and survive under conditions where populations lacking males and females go extinct. It appears that physical constraints on gamete encounter rates are sufficient to explain the first two steps in the isogamy-->anisogamy-->oogamy-->internal fertilization evolutionary sequence observed in several lineages of the eukaryotes. Unlike previous models, assumptions concerning zygote fitness or decreasing speed of swimming with increasing gamete size are not required.     

Gametic conflict versus contact in the evolution of anisogamy

Anisogamy refers to gametes that differ in size, and characterizes the difference between males and females. The evolution of aniosgamy is widely interpreted as involving conflict between gamete producers with small sperm parasitizing on the investment made by the eggs. Using a population genetic model for evolution at a locus that codes jointly for sperm and egg sizes of a hermaphrodite, we show that the origin of anisogamy in an externally spawning population need not involve conflict between gamete producers. Gamete size dimorphism may be an adaptation that increases gamete encounter rates when large zygotes are selected, and we show this in a mechanistically general individual selection model. We use the Vance survival function without specific allometric assumptions to model the zygote fitness dependence on its size, and hence obtain ecological and life-history correlates of isogamy and anisogamy, which we successfully compare with data from Volvocales.     

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.     

The population genetics of anisogamy

This paper analyses the population genetics of anisogamy controlled by a single locus, in both the haploid and diploid cases. The conclusions of Parker et al. (1972), based on computer calculations, are confirmed analytically. The effects of the existence of two mating types on the evolution of anisogamy are examined. Close linkage between a mating type locus and the gamete size locus may produce non-random associations of alleles, leading to disassortative fusion with respect to gamete size. With loose linkage, there is random association of alleles, but selection favours closer linkage.     

Sexual selection without sexual dimorphism: Bateman gradients in a simultaneous hermaphrodite

One of the most general patterns in sexual selection is stronger selection on mating activity in males than in females. This asymmetry is thought to result from the higher energetic cost of producing one female compared to one male gamete (anisogamy). However, most studies focused on gonochoric species with strong sexual dimorphism, in which males and females are necessarily under different selection regimes. The question remains whether anisogamy alone would suffice to produce such differences. In simultaneous hermaphrodites one can compare sexual selection on the male and female functions in the absence of sexual dimorphism. Here we quantify sexual selection in the hermaphroditic freshwater snail Physa acuta under laboratory conditions. We combine exhaustive behavioral records of mating activity in mating groups and molecular paternity assignment to measure the mating success and reproductive success of 120 individuals. Our results validate the prediction of stronger selection to gain mating partners in the male than in the female function. Moreover, we did not detect cross‐sex effects on fitness, or correlations between male and female production of offspring over the course of our experiment. We conclude that with respect to sexual selection P. acuta is comparable to gonochorists, confirming that anisogamy is a sufficient explanation for the differences in sexual selection regimes between sexes.     

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     

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.     

The evolution of anisogamy: a game-theoretic approach

A popular theory has proposed that anisogamy originated through disruptive selection acting on an ancestral isogamous population, though recent work has emphasized the importance of other factors in its evolution. We re-examine the disruptive selection theory, starting from an isogamous population with two mating types and taking into account the functional relationship, g(m), between the fitness of a gamete and its size, m, as well as the relationship, f(S), between the fitness of a zygote and its size, S. Evolutionary game theory is used to determine the existence and continuous stability of isogamous and anisogamous strategies for the two mating types under various models for the two functions g(m) and f(S). In the ancestral unicellular state, these two functions are likely to have been similar; this leads to isogamy whether they are sigmoidal or concave, though in the latter case allowance must be made for a minimal gamete size. The development of multicellularity may leave g(m) relatively unchanged while f(S) moves to the right, leading to the evolution of anisogamy. Thus, the disruptive selection theory provides a powerful explanation of the origin of anisogamy, though other selective forces may have been involved in the subsequent specialization of micro- and macrogametes.     

A comparative test of a theory for the evolution of anisogamy

Why are sperm small and eggs large? The dominant explanation for the evolution of gamete size dimorphism envisages two opposing selection pressures acting on gamete size: small gametes are favoured because many can be produced, whereas large gametes contribute to a large zygote with consequently increased survival chances. This model predicts disruptive selection on gamete size (i.e. selection for anisogamy) if increases in zygote size confer disproportional increases in fitness (at least over part of its size range). It therefore predicts that increases in adult size should be accompanied by stronger selection for anisogamy. Using data from the green algal order Volvocales, we provide the first phylogenetically controlled test of the model''s predictions using a published phylogeny and a new phylogeny derived by a different method. The predictions that larger organisms should (i) have a greater degree of gamete dimorphism and (ii) have larger eggs are broadly upheld. However, the results are highly sensitive to the phylogeny and the mode of analysis used.     

Cooperation and the evolution of anisogamy

In the lights of the concept of cooperation wholes, I discuss why the differentiation of sperm and ova can occur with a mathematical model. Most of Parker's explanations for anisogamy are not completely proper, because it is proved that sperm competition is neither sufficient nor necessary for anisogamy and cooperation to deal with fertilization risks is the real key to understand the evolution of anisogamy. According to the computer simulation results, the transport of gametes between different individuals, risks of the transport, the consequent inequality of sperm and eggs and competition among different individuals were the main causes of gamete differentiation. But these factors have different roles and effects. The transport risk is the main reason for individuals of different mating types to cooperate and differentiate into sperm and egg producers. The transported gametes have an advantage to evolve into sperm to seek for a larger gamete number over the fixed gametes, because they suffer more risks as they can encounter the same fixed gamete and less sibling competition as they can be dispersed better. Gamete competition among different individuals just causes the transported gametes to become as small as possible if they have already become smaller beyond a critical state. In the final discussion, I further put the evolution of anisogamy into a broader background of levels of selection and of the evolution of cooperation, the most important existential mode of matters that makes life as life.     

Having sex,yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types

The advantage of sex has been among the most debated issues in biology. Surprisingly, the question of why sexual reproduction generally requires the combination of distinct gamete classes, such as small and large gametes, or gametes with different mating types, has been much less investigated. Why do systems with alternative gamete classes (i.e. systems with either anisogamy or mating types or both) appear even though they restrict the probability of finding a compatible mating partner? Why does the number of gamete classes vary from zero to thousands, with most often only two classes? We review here the hypotheses proposed to explain the origin, maintenance, number, and loss of gamete classes. We argue that fungi represent highly suitable models to help resolve issues related to the evolution of distinct gamete classes, because the number of mating types vary from zero to thousands across taxa, anisogamy is present or not, and because there are frequent transitions between these conditions. We review the nature and number of gamete classes in fungi, and we attempt to draw inferences from these data on the evolutionary forces responsible for their appearance, loss or maintenance, and number.     

Lonely hearts or sex in the city? Density-dependent effects in mating systems

Two very basic ideas in sexual selection are heavily influenced by numbers of potential mates: the evolution of anisogamy, leading to sex role differentiation, and the frequency dependence of reproductive success that tends to equalize primary sex ratios. However, being explicit about the numbers of potential mates is not typical to most evolutionary theory of sexual selection. Here, we argue that this may prevent us from finding the appropriate ecological equilibria that determine the evolutionary endpoints of selection. We review both theoretical and empirical advances on how population density may influence aspects of mating systems such as intrasexual competition, female choice or resistance, and parental care. Density can have strong effects on selective pressures, whether or not there is phenotypic plasticity in individual strategies with respect to density. Mating skew may either increase or decrease with density, which may be aided or counteracted by changes in female behaviour. Switchpoints between alternative mating strategies can be density dependent, and mate encounter rates may influence mate choice (including mutual mate choice), multiple mating, female resistance to male mating attempts, mate searching, mate guarding, parental care, and the probability of divorce. Considering density-dependent selection may be essential for understanding how populations can persist at all despite sexual conflict, but simple models seem to fail to predict the diversity of observed responses in nature. This highlights the importance of considering the interaction between mating systems and population dynamics, and we strongly encourage further work in this area.     

Anisogamy selects for male-biased care in self-consistent games with synchronous matings

We reexamine the influential parental investment hypothesis proposed by Trivers for the causal relationship between anisogamy and widespread female-biased parental care. We build self-consistent versions of Maynard Smith's simple evolutionary game between males and females over parental care, and incorporate consequences of anisogamy for gamete production and its trade-off with parental care, and for patterns of mate limitation. As male mating opportunities are limited by females, frequency-dependent selection acts on male strategies. Assuming synchrony of matings in the population, our analytical models find either symmetric sex roles or male-biased care as an evolutionarily stable strategy (ESS), in contrast to Trivers' hypothesis. We simulate evolution in asynchronously mating populations and find that diverse parental roles, including female care, can be ESS depending on the parameters. When caring males can also remate, or when females can increase the clutch size by deserting, there is stronger selection for male-biased care. Hence, we argue that the mating-caring trade-off for males is neither a necessary consequence of anisogamy nor sufficient to select for female-biased care. Instead, the factors excluded from our models—costly competitive traits, sexual selection, and partial parentage—may be necessary for the parental investment hypothesis to work.     

Selection on non-random fusion of gametes during the evolution of anisogamy

Correction of an error in earlier simulations which show how anisogamy could evolve by selection on individuals (Parker et al., 1971) now indicates that anisogamy can evolve when the range of gamete size is very much smaller than previously thought. These models assumed random fusion of gametes, external fertilization, and that zygote viability is dependent on the volume of provisioning it receives from one or both gametes.The present analysis concerns the success of strategies for selective fusion of gametes arising in a randomly-fusing parental population. On a priori grounds selection is expected to favour assortative fusion in ova but disassortative fusion in sperm; anisogamy can persist only if genes for assortative fusion of ova will not spread, and “perfect” anisogamy where genes for disassortative fusion fixate. Mutant strategies for assortatively-fusing ova may not be successful if such ova must compete with sperm for fusions with the randomly-fusing ova. Particularly at high levels of anisogamy, very few of the mutant ova will be fused by the time all other ova have become zygotes; hence their spread may be checked by the enhanced chances of death before fusion, or by problems associated with selfing if they do manage to fuse. In contrast, disassortatively-fusing sperm generally have an advantage when anisogamy would be favoured under random fusion. Genetic simulations (involving two loci, one with alleles for fusion behaviour and the other with alleles for gamete size) were used to confirm these conclusions. Where there is some degree of asynchrony of spawning, disassortative fusion alleles do even better than with perfect synchrony.Simulations with various sex-limited fusion strategies show that non-limited disassortative fusion, i.e. for both ova and sperm, is likely to be an ESS at high anisogamy against all strategies but the one which plays random fusion in ova, disassortative fusion in sperm. This is the ultimate ESS and it does not disrupt anisogamy, but at high anisogamy it has an extremely small advantage over non-limited disassortative fusion. The reasons for the establishment of non-limited disassortative fusion are probably related to avoiding selfing, and to the cost of maintaining random-fusion in ova (in terms of motility, etc.) outweighing the benefits of becoming obligatorily disassortative (non-motile).     

Why do organisms produce gametes of only two different sizes? Some theoretical aspects of the evolution of anisogamy

This paper extends the population genetic model of (the evolution of) anisogamy of Charlesworth (1978), which is based on the model of Parker, Baker & Smith (1972). The effect of parthenogenesis on the evolution of anisogamy is examined; this effect turns out to be only quantitative. Furthermore, the problem of the occurrence of only two different gamete sizes is considered. It is shown that a stable polymorphism with three different gamete sizes cannot exist. This result is robust to changes in the mating structure (random or disassortative gamete fusion) and to changes in the mode of reproduction (only sexual or partially parthenogenetic).     

Evolution of gamete size in primitive taxa without mating types

An ESS model to better understand the evolutionary dynamics of a primitive non-mating type gamete size was developed with reference to the PBS (Parker, Baker and Smith’s) theory, which was based on total numbers of zygotes formed and the zygote survival rates. We did not include mating types since it has been suggested that primitive mating systems did not have mating types. As input parameters, we used experimental data on gamete motility of marine green algae. Based on hard sphere collision mechanics, we detailed the fertilization kinetics of gametes that swim in water prior to fusing with their partners through a set of coupled, non-linear differential equations. These equations were integrated numerically using typical values of the constant parameters. To estimate the relative zygote survival rate, we used a function that is sigmoid in shape and examined some evolutionarily stable strategies in mating systems that depend on optimizing values of the invasion success ratio.     

Cytoplasmic inheritance of organelles in brown algae

Brown algae, together with diatoms and chrysophytes, are a member of the heterokonts. They have either a characteristic life cycle of diplohaplontic alternation of gametophytic and sporophytic generations that are isomorphic or heteromorphic, or a diplontic life cycle. Isogamy, anisogamy and oogamy have been recognized as the mode of sexual reproduction. Brown algae are the characteristic group having elaborated multicellular organization within the heterokonts. In this study, cytoplasmic inheritance of chloroplasts, mitochondria and centrioles was examined, with special focus on sexual reproduction and subsequent zygote development. In oogamy, chloroplasts and mitochondria are inherited maternally. In isogamy, chloroplasts in sporophyte cells are inherited biparentally (maternal or paternal); however, mitochondria (or mitochondrial DNA) derived from the female gamete only remained during zygote development after fertilization. Centrioles in zygotes are definitely derived from the male gamete, irrespective of the sexual reproduction pattern. Female centrioles in zygotes are selectively broken down within 1–2 h after fertilization. The remaining male centrioles play a crucial role as a part of the centrosome for microtubule organization, mitosis, determination of the cytokinetic plane and cytokinesis, as well as for maintaining multicellularity and regular morphogenesis in brown algae.     

Postmating sexual selection: the effects of male body size and recovery period on paternity and egg production rate in a water strider

The role of male body size in postmating sexual selection wasexplored in a semiaquatic insect, the water strider Gerris lateralis.To separate effects of male size per se from those due to numericsperm competition, male recovery period (shown here to be proportionalto ejaculate size) was manipulated independently of body sizein a factorial experiment where virgin females were mated firstwith sterile males and then with focal males. Both relativemale fertilization success and female reproductive rate were measured.The number of sperm transferred increased with male recoveryperiod, an effect that was mediated by longer copulation duration,but there were no effects of body size on ejaculate size. Neithermale size nor recovery period had any significant direct effectson male fertilization success. However, copulation durationinfluenced relative fertilization success, suggesting that malesable to transfer more sperm also achieved higher fertilizationsuccess. Females exercised cryptic female choice by modulatingtheir reproductive rate in a manner favoring large males andmales that were successful in terms of achieving high relativefertilization success. Thus, successful males gained a twofoldadvantage in postmating sexual selection. This study has important implicationsfor previous estimates of sexual selection in this group of insectsbecause pre- and postmating sexual selection will be antagonisticdue to limitations in male sperm production: males mating frequently(high mating success) will on average transfer fewer sperm ineach mating and will hence tend to fertilize fewer eggs permating (low fertilization success).