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.     

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.     

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.     

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.     

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.     

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     

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.     

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.     

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.     

Selection for high gamete encounter rates explains the evolution of anisogamy using plausible assumptions about size relationships of swimming speed and duration

A previous general model describing physical constraints on gamete encounter rates was modified to incorporate assumptions that increased size causes decreased swimming speed and increased fertile period (or other proportional enhancement to gamete fertility). The analysis indicates that with moderately strong size dependence of fertile period and a range of speed dependencies, selection for high encounter rates pressures mating systems that develop any heritable difference in size between the gametes of different mating types to exaggerate the difference and evolve from isogamy to anisogamy. The smaller gamete has an optimal size, but the larger faces continuing selection for increased size. This continues to a size that is estimated to be sufficient to make pheromone production of sperm attractants practical. This mechanism then bridges the missing link between isogametes and oogamy in a previous analysis of the effectiveness of pheromones in explaining the success of male-female mating systems. The evolution and success of anisogamy and oogamy can be explained solely on the basis of physical effects on the encounter process.     

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.     

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.     

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).     

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.     

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.     

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.     

Gamete evolution and sperm numbers: sperm competition versus sperm limitation

Both gamete competition and gamete limitation can generate anisogamy from ancestral isogamy, and both sperm competition (SC) and sperm limitation (SL) can increase sperm numbers. Here, we compare the marginal benefits due to these two components at any given population level of sperm production using the risk and intensity models in sperm economics. We show quite generally for the intensity model (where N males compete for each set of eggs) that however severe the degree of SL, if there is at least one competitor for fertilization (N − 1 ≥ 1), the marginal gains through SC exceed those for SL, provided that the relationship between the probability of fertilization (F) and increasing sperm numbers (x) is a concave function. In the risk model, as fertility F increases from 0 to 1.0, the threshold SC risk (the probability q that two males compete for fertilization) for SC to be the dominant force drops from 1.0 to 0. The gamete competition and gamete limitation theories for the evolution of anisogamy rely on very similar considerations: our results imply that gamete limitation could dominate only if ancestral reproduction took place in highly isolated, small spawning groups.     

Evolution of hierarchical cytoplasmic inheritance in the plasmodial slime mold Physarum polycephalum

A striking linear dominance relationship for uniparental mitochondrial transmission is known between many mating types of plasmodial slime mold Physarum polycephalum. We herein examine how such hierarchical cytoplasmic inheritance evolves in isogamous organisms with many self-incompatible mating types. We assume that a nuclear locus determines the mating type of gametes and that another nuclear locus controls the digestion of mitochondria DNAs (mtDNAs) of the recipient gamete after fusion. We then examine the coupled genetic dynamics for the evolution of self-incompatible mating types and biased mitochondrial transmission between them. In Physarum, a multiallelic nuclear locus matA controls both the mating type of the gametes and the selective elimination of the mtDNA in the zygotes. We theoretically examine two potential mechanisms that might be responsible for the preferential digestion of mitochondria in the zygote. In the first model, the preferential digestion of mitochondria is assumed to be the outcome of differential expression levels of a suppressor gene carried by each gamete (suppression-power model). In the second model (site-specific nuclease model), the digestion of mtDNAs is assumed to be due to their cleavage by a site-specific nuclease that cuts the mtDNA at unmethylated recognition sites. Also assumed is that the mtDNAs are methylated at the same recognition site prior to the fusion, thereby being protected against the nuclease of the same gamete, and that the suppressor alleles convey information for the recognition sequences of nuclease and methylase. In both models, we found that a linear dominance hierarchy evolves as a consequence of the buildup of a strong linkage disequilibrium between the mating-type locus and the suppressor locus, though it fails to evolve if the recombination rate between the two loci is larger than a threshold. This threshold recombination rate depends on the number of mating types and the degree of fitness reduction in the heteroplasmic zygotes. If the recombination rate is above the threshold, suppressor alleles are equally distributed in each mating type at evolutionary equilibrium. Based on the theoretical results of the site-specific nuclease model, we propose that a nested subsequence structure in the recognition sequence should underlie the linear dominance hierarchy of mitochondrial transmission.