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The Origin and Evolution of Gamete Dimorphism and the Male-Female Phenomenon

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The Origin and Evolution of Gamete Dimorphism and the Male-Female Phenomenon See discussions, stats, and author profiles for this publication at: http://www.researchgate.net/publication/18089267 The origin and evolution of gamete dimorphism and the male-female phenomenon. J Theor Biol ARTICLE in JOURNAL OF THEORETICAL BIOLOGY · OCTOBER 1972 Impact Factor: 2.3 · DOI: 10.1016/0022-5193(72)90007-0 · Source: PubMed CITATIONS DOWNLOADS VIEWS 249 459 604 3 AUTHORS, INCLUDING: Geoff A. Parker University of Liverpool 219 PUBLICATIONS 21,278 CITATIONS SEE PROFILE Available from: Geoff A. Parker Retrieved on: 22 September 2015 J. theor. Biol. (1972) 36,529-553 G. A. PARKER Department of Zoology, Universitj of Liverpool, Liverpool L69 3BX, England R. R. BAKER Department of Zoology, University of NewcastIe-upon-Tyne Newcastle NE1 7RU, England AND V. G. F. SMITH Department of Biological Sciences, Ah& BeUo University, Zanb, Nigeria (Received 14 February 1972) The classical theory for the origin of anisoqamy is that the greate8t number of successful fusions occurs when the gametic material available for the population is divided with a high degas okanisogamy. This assumes that a fkd amount of reserve material is necesky for dmlopment of the zygote and that only disassortative fusions occur (i.e. between small and large &ametes). Assuming (as in previous literatunz) that a gjven gametic mass can be produced in unit time, then individual variations in gamete sizz may arise either from di&ences in the production th$e, or in the number of cell divisions at the time of production. where *te 6tness is in some way related to zygote volume’, relative rtproducti\ie rates can be calculated for a range of variants with dMerent gamete prQductivitie8 (and thcnfore difkent gamete sizm). This model yields eitherdrive for small-producing (where the advantage of high productivity qxeeds that of increased provisioning for the zygote) or drive for large4producing (in the reverse case). However in certain conditions (over park of the range of x where zygote fitness is proportional to volumet) a ,marked disruptive etlbct canbegcneratedinwhichthetwoex-~(largeandsmaugametc production) are favoured. Reasons are given why selection should always lead to the establishment of a stable dimorphism in multicell~ar organisms. When the model is mod&d to include inhexi of gamete siz by simple mcndclian dominance, it is shown that as theTit ‘tial range of variants is imead, the ran& of x (where fitness is prop&tional to volume9 which 530 G. A. PARKER, R. R. BAKER AND V. G. F. SMITH 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 through- out, 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 assortatively- fusing 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. 1. Introduction Why are gametes dimorphic and why are there two sexes ? Though most multicellular organisms have a pronounced anisogamy, the origin of gamete dimorphism has attracted very little attention (see below). Isogamy is common in unicellular species, and hence sexual reproduction does not lead automatically to anisogamy. In multicellular forms, the provision of large amounts of cytoplasmic reserves in the ovum confers advantages on the zygote in its development to adulthood. Though females are now specialized to produce gametes with cytoplasmic reserves, this does not directly explain the origin of gamete dimorphism. Anisogamy may have evolved by disruptive selection from isogamy; or from a situation where a range of gamete sizes were found, but without an obvious isogametic peak. A third and perhaps less likely possibility is that true anisogamy was preceded by the production of gamete-like phage particles (Baker & Parker, in press). The theory presented in the present paper examines the origin of anisogamy by disruptive selection from isogamy or from a population with a range of gamete sizes. The classical theory for the origin of anisogamy dates back to Kalmus (1932), and has recently been examined more rigorously by Scudo (1967). The theory can be summarized as follows. Where there is a fixed amount of reserve material available in a population for gametogenesis, and where the united gametes require a certain quantity of reserve for development of the zygote, the greatest number of successful fusions occurs when the gametic material is divided with a high degree of anisogamy than with isogamy. This assumes that fusions occur only between the two gametic morphs; fusions between like gametes do not occur. However, though Kalmus’ ingenious theory indicates an important advantage associated with anisogamy once evolved (and specialized for fusions only between the two forms of gamete), it does not readily outline the origin and mechanism of evolution of the EVOLUTION OF GAMETE DIHORPHISM 531 system. A possible mechanism of evolution has been suggested by Kalmus & Smith (1960). They envisaged as one possibility a diploid population homo- xygous for gene a (which produces small gametes) in which a dominant gene A arises (producing large gametes). “These gametes which will carry A will thus provide the zygotes with more reserves and thus be advantageous; hence the gene A may be expected to spread through the population. This spread will, however, be checked by the dithculty of union between these large, relatively static gametes, so that the advantage will only remain while there are a sufficient number of small gametes also present. Hence this situation may be expected to lead to an equilibrium in which both dominant and recessive types persist, and most fertile unions are between large and small gametes.” An alternative theory for the origin and evolution of anisogamy is proposed in the present paper. 2. Selective Pressure Acting on#Gamete Size The selective forces determining the optimum sixes for the gametes of a species must be numerous and complex. However, in view of the apparently near universal adoption of dimorphic gamete systems by multicellular organisms it seems reasonable to search for an explanation in terms of the most obvious selective pressures. Two very fundamental pressures immedi- ately appear obvious; both would be related to gamete size and would act in opposition. These are numerical producrioity (i.e. the number of gametes produced in unit time by a given parent) and z$gotefiitness (i.e. a measure of the probability that a zygote will survive to reach adulthood and reproduce, and in the shortest time). There would be a selective advantage in producing the maximum number of gametes, provided that this leads to an increase in the net reproductive rate of a given parent. Productivity would pro ably have the following sort of relationship with the size of gametes pro ! ,uced. Assuming the energy intake of all the adults in the population to be roughly similar, then over unit time the amount of material available for organization into gametes would also be roughly similar. The volume (V) of material available can be subdivided into virtually as many subunits as is possible without cutting down the nuclear material itself. Thus a fairly definite relationship can be predicted between productivity and gamete sir.e (= volume), varying in the series : V/l, V/2, V/3, V4 . etc. where the fraction expresses the gamete size and the denominator represents the productivity. Biochemical and energetic arguments can be levied against a perfectly precise relationship of this type; it is not felt that these would make it invalid as an approximation. 532 G. A. PARKER, R. R. BAKER AND V. G. F. SMITH All other things being equal, the maximum selective advantages is to be gained by producing as many gametes as possible without reducing the nuclear material. This would assume that cytoplasmic inheritance is insignifi- cant relative to that conveyed by the chromosomes, so that smaller gametes provide an equal genetic contribution to the zygote as do larger ones. Where V/n approximates to the nuclear size plus the minimum possible cytoplasm, n would represent the most favourable productivity. However, a zygote produced from the fusion of two such gametes may not have high fitness for a multicellular organism. Over a certain range the ability of a zygote to survive, and the speed with which it reaches adulthood, will be increased by having a greater amount of cytoplasm. There would not necessarily be a total drive to produce n gametes if parents producing fewer but larger gametes experienced a compensating advantage because of the greater fitness of their offspring. 3. Sonrce of Variation in Gamete Size It is envisaged that variation in gamete size would arise in two main ways. Firstly, the time taken accumulating protoplasm before dividing it up into gametes may vary. This assumes that a fixed number of cell divisions occur to form the gametes, but that the interval between the production of separate batches varies. Functionally the same thing would occur where gametes, after formation, accumulate protoplasm for varying periods of time (proportional to their size at release). Both could yield continuous variation in gamete size; but the relationship between productivity in unit time and gamete size should remain as outlined in the previous section. A second source of variation, that of the number of cell divisions (d) used in dividing the available protoplasm, should lead to a rather more clearly defined series of variants. For a fixed time between the production of the batches of gametes, the productivity would vary as 2d, and hence the gamete size would vary as V/2d.
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