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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).

That sperm size seems to be inversely related to body mass in mammals has been regarded as a scientific curiosity for many years, but does not appear to have been rigorously investigated. This is surprising, given the intense interest in the evolution of anisogamy and sexuality in general (1).

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.

There are at least four conceivable factors which could be responsible for the maintenance of anisogamous sex: (1) long-term group selection, (2) short-term ecological, natural selection, (3) trade-offs between female sexual fertility and parthenogenetic fertility and (4) female dependence on a male gametic contribution. There is evidence for the action of each of the first three factors, while the fourth seems to be evolutionarily impossible, at first sight. But selection on male and female gamete production physiology could, in principle, produce female germ lines which depend on male gametes for their perpetuation. There is circumstantial evidence that this has in fact occurred in the Mammalia, and critical experiments to test this hypothesis are proposed.

Sexual reproduction is a widespread phenomenon. In most higher organisms it is the only mode of reproduction, while many lower organisms have the capacity to reproduce both asexually and sexually. There are few species in which sexual reproduction never has been observed. Sex can be characterized by the following three processes: fusion of two haploid sex cells (called gametes) into a (diploid) zygote, recombination of the genetic information from both gametes, and production of a new generation of haploid gametes. Although the processes involved are known into considerable detail, there is still no satisfactory functional explanation for the evolution of sex. In short, the problem is that it is difficult to explain the origin and maintenance of sex in terms of any benefit to individual fitness (fitness is a measure of the probability of survival and reproduction). The conclusion from theoretical analysis is that there should be strong selection pressure favouring the abandonment of sex by females, and the adoption of asexual reproduction instead. An extensive discussion of this matter can be found in Maynard Smith (1978).

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.

The slightly anisogamous gametes of Ulva lactuca exhibit a cruciate flagellar root system consisting of 4 microtubular roots (4-2-4-2 system) and an elaborate system of fibrous roots associated with the 2-stranded microtubular roots. Two fibres (32-nm striation periodicity; system I fibres) closely underlie each of the 2-stranded roots, while different fibres (150-nm striation periodicity; system II fibres) run parallel to the root microtubules, and are 150–200 nm more internally located. Female gametes have 4 system II fibres, 3 of which are combined into a compound fibre associated with one microtubular root, while the fourth fibre is associated with the opposite root. In male gametes only 2 system II fibres are present, each underlying one of the two 2-stranded roots. A special region of the plasmalemma of both gamete types about 0.5 mum away from the basal bodies and located between 2 adjacent microtubular roots is structurally specialized and acts as a mating structure in gametic fusion. The region is oval-shaped and up to I.I mum long with a maximum diameter of 0.7 mum. A continuous electron-dense boundary layer underlies the plasmalemma at the edges of the mating structure. In both gamete types the mating structure consists of a fuzzy layer of material underlying the plasmalemma and special granules (60 nm diameter) are associated with this layer on its cytoplasmic side. In addition diffuse material overlies the mating structure, especially in male gametes. The mating structure is connected to 3 different kinds of flagellar roots: the boundary layer is linked to a 2-stranded microtubular root and its associated system I fibre; the fuzzy layer of the mating structure is connected with a system II fibre; and in female gametes this is the compound system II fibre. The ultrastructural changes which occur after mixing the 2 gamete types have been followed. Mating structure activation involves contraction of system II fibres (change of striation periodicity to 100 nm), detachment of special granules from the fuzzy layer of the mating structure and their replacement by electron-transparent vesicles at the prospective cell fusion site. Furthermore, release of electron-dense contents from Golgi-derived vesicles in the anterior part of both gamete types precedes cell fusion. Cell fusion is exclusively initiated in a region delimited by the 2 mating structures. After partial dissolution the 2 plasma membranes unite within the mating structure regions. The ultrastructure of gametic fusion in Ulva lactuca is compared to that of other green algae and the significance of flagellar roots in the mating process of green algae is discussed.

The differing inheritance patterns of cytoplasmic genes and the sex chromosomes from the Mendelian autosomal patterns can be used to divide the genome into fractions whose defining rule is that the fitness of all genes in a set is maximized in the same way. Each set will be selected to modify the phenotype of the organism in a way which maximally propagates the genes comprising the set, and hence in ways inconsistent with the other sets which comprise the total genome. The coexistence of such multiple sets in the same genome creates intragenomic conflict. Evidence is presented in which the fitness of cytoplasmic and other non-autosomal genetic sets are increased at the expense of the autosomal genetic set. The relationship of such intragenomic conflict to the evolution of anisogamy, dioecy, skewed sex ratios, differential male mortality, systems of sex determination, and altruism is discussed.

The classical theory for the origin of anisogamy is that the greatest number of successful fusions occurs when the gametic material available for the population is divided with a high degree of anisogamy. This assumes that a fixed amount of reserve material is necessary for development of the zygote and that only disassortative fusions occur (i.e. between small and large gametes). Assuming (as in previous literature) that a given gametic mass can be produced in unit time, then individual variations in gamete size may arise either from differences in the production time, or in the number of cell divisions at the time of production. Where zygote fitness is in some way related to zygote volumex, relative reproductive rates can be calculated for a range of variants with different gamete productivities (and therefore different gamete sizes). This model yields either', drive for small-producing (where the advantage of high productivity exceeds that of increased provisioning for the zygote) or drive for large-producing (in the reverse case). However in certain conditions (over part of the range of x where zygote fitness is proportional to volumex) a marked disruptive effect can be generated in which the two extremes, (large and small gamete production) are favoured. Reasons are given why selection should always lead to the establishment of a stable dimorphism in multicellular organisms. When the model is modified to include inheritance of gamete size by simple mendelian dominance, it is shown that as the initial range of variants is increased, the range of x (where fitness is proportional to volumes) which generates stable dimorphism also increases. As high anisogamy is approached, the disadvantageous dominant homozygote is lost leaving two sexes (sperm producers and ovum producers) in a stable 1 : 1 ratio. Stages in the evolution of dissortative fusions are outlined. Though males with sperm which fused only with ova would be favoured throughout, females with assortatively-fusing ova may have been favoured initially. Because of a faster rate of adaptation in sperm than ova, or because of the instability of an isogametic population with assortativelyfusing ova, females face an evolutionary impasse in which the only stable solution is total committment to disassortative fusions. Males are dependent on females and propagate at their expense, rather as in a parasite-host relationship.

Publisher Summary This chapter discusses the mechanisms of gametic approach in plants. The chemotactic and chemotropic reactions participate in the sexual reproduction of a widespread variety of plants. The evidence varies from the simple observation of aggregation of sperm and the apparent directed growth of various sexual structures to conclusive evidence obtained with cell-free extracts, partially purified preparations and, in the case of pollen, presumably the factor itself. Five types of systems having at least one gamete motile are considered in the chapter: (1) isogamy in which all gametes are equally and fully motile, (2) physiological and morphological anisogamy, (3) oogamy in which the egg is released from the oogonium, (4) oogamy, in which the eggs are retained within oogonia, and (5) those plants in which the egg is encased in a multicellular sex organ—the archegonium—into which the motile sperm must swim to reach the egg. The four chemotropic substances are discussed in the chapter are zygophores, antheridial hyphae, trichogynes, and pollen tubes. For each of the basic types mentioned there exists good experimental evidence that the growth of the various sexual elements is directed by chemical agents.

One of the basic principles of sexual selection is that male reproductive success should be skewed towards strong males in species with anisogamous sex. Studies on primate multi-male groups, however, suggest that other factors than male fighting ability might also affect male reproductive success. The proximate mechanisms leading to paternity in multi-male primate groups still remain largely unknown since in most primate studies mating rather than reproductive success is measured. Furthermore, little research focuses on a female’s fertile phase. The aim of this study was to investigate the relative importance of male monopolisation and female direct mate choice for paternity determination. We also investigated the extent to which paternity was decided post-copulatory, i.e. within the female reproductive tract. We used a combined approach of behavioural observations with faecal hormone and genetic analysis for assessment of female cycle stage and paternity, respectively. The study was carried out on a group of wild long-tailed macaques living around the Ketambe Research Station, Gunung Leuser National Park, Indonesia. Our results suggest that both male monopolisation and post-copulatory mechanisms are the main determinants of male reproductive success, whereas female direct mate choice and alternative male reproductive strategies appear to be of little importance in this respect. Female cooperation may, however, have facilitated male monopolisation. Since paternity was restricted to alpha and beta males even when females mated with several males during the fertile phase, it seems that not only male monopolisation but also post-copulatory mechanisms may operate in favour of high-ranking males in long-tailed macaques, thus reinforcing the reproductive skew in this species.

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.

We describe analytical and numerical models to study gamete encounters in two and three dimensions between differently sized gametes without assuming pre-existing mating types. Our results indicate that an isogamous population can be successfully invaded by a gametangium if it produces gametes of a different size. The existence of a low adaptive peak for isogamy and a much higher adaptive peak for anisogamy suggests that stochastic forces may be initially important in driving isogamy through the fitness saddle to anisogamy.

THE apparent absence of sexual reproduction in the Prasiolaceae has been one of the notable features of this family. It was of considerable interest, therefore, when two decades ago, Yabe1 announced that sexual reproduction occurs in the freshwater species Prasiola japonica Yatabe and is effected by the fusion of anisogamous biflagellated gametes. Fujiyama2,3, also using material of P. japonica, has confirmed Yabe's observations in the main essentials, except that he considers the female gamete to be non-motile. For all that, doubts about the sexual reproduction of Prasiola have been expressed quite recently by Fritsch4 and Smith5, although Fujiyama's second paper could not have been seen by these authors at the time they wrote.

The adaptive value of various modes of reproduction can be studied through simplified mathematical models using the same tools which classical statistical mechanics applies to the collision of particles. This approach may for instance be employed for calculating: (1) the rate of unions in a population of gametes having a uniform spatial distribution; (2) the rate at which matings take place (and, hence, the birth rate) in a population of crossbreeding animals, also having a uniform spatial distribution. The former problem, with which this paper is concerned, was first considered by Kalmus (1932). Our own considerations are based on biological assumptions rather similar to those of Kalmus but are developed somewhat more rigorously. Among unicellular autotrophic organisms, requiring little or no reserve material, morphological isogamy2 is very common, while the gametes of almost all pluricellular forms, which need a certain amount of reserve material to support the first stages of embryonic life, show a marked anisogamy. With the aim of working out

In a recent paper in Current Biology, Nozaki et al. [1] report evidence that males of the anisogamous Volvocine alga, Plerodina starri, have an active copy of a gene PsPlesMID, which is similar in sequence to the CrMID gene of the green alga Chlamydomonas reinhardtii. In C. reinhardtii, there is no size difference between male and female gametes — it is isogamous — but gametes are divided into two mating types (MT+ and MT−), controlled by a complex genetic locus mt, such that zygotes can only be formed by fusions of gametes with different mating types [2,3].