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The Evolution of Male-Female Dimorphism: Older Than Sex?

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The Evolution of Male-Female Dimorphism: Older Than Sex? J. Genet. Vol. 69, No. 1, April 1990, pp. 11-15. 9 Printed in India. The evolution of male-female dimorphism: Older than sex? ROLF F. HOEKSTRA Department of Genetics, Agricultural University, Dreijenlaan 2, 6703 HA Wageningen, The Netherlands Abstract. This contribution considers the evolution of a dimorphism with respect to cell fusion characteristics in a population of primitive cells. These cells reproduce exclusively asexually. The evolution towards asymmetric fusion behaviour of cells is driven by selection promoting horizontal transfer of an endosymbiontic replicator. It is concluded that evolution of asymmetric cell fusion in this scenario is more likely than evolution of sexual differentiation in a sexually reproducing population. Pre-existing dimorphism with respect to cell fusion may thus have been the basis for the establishment of sexual differentiation at the level of gamete fusion, and this in turn is fundamental to the evolution of two different sexes, male and female. Keywords. Sexes; mating type; horizont;d transmission; evolution. 1. Introduction Sex is a composite phenomenon characterized by the succession of fusion, recombination, and division. Fusion, the bringing together of the hereditary material from two nuclei (which are generally derived from different individuals), is " effected by a preceding fusion of two specialized cells (gametes) which are, as far as we know, always of different types. In anisogamous species, where the gametes differ in size, the two types are denoted male and female; in isogamous species the two gamete types do not differ morphologically and are called mating types. This characteristic difference between the two gametes fusing to form a zygote is the basis for the sexual differentiation into males and females. If we want to understand why there are males and females, we should understand why zygotes are formed by two gametes of different type. Evolutionary scenarios for the evolution of mating types have been studied by Hoekstra (1982, 1987) and Hoekstra et al. (1990). These models consider the evolution of two mating types in an initially undifferentiated population in which every gamete can fuse with any other gamete. The model organism is an aquatic unicellular isogamous 'alga' with a haptontic life cycle. All models studied share the following features: there are three types of gametes in a population: an undifferentiated type, which can fuse with all three types, and two differentiated mating types that are unable to fuse with their own type, but can fuse with the other two types. The success rates of the different combinations are supposed to differ, such that a fusion between two undifferentiated gametes has the lowest fitness, and a fusion between two differentiated gametes the highest. The models differ in the assumptions concerning the population structure (homogeneous or ctonal) and the mating kinetics, but it is nevertheless possible to draw a general conclusion, namely that great selective differences between different gamete combinations are required for the evolution towards the exclusive existence of two differentiated mating types in a population. In other words, strong selection is needed to remove the supposedly original undifferentiated gamete type from the 11 12 Rolf F. Hoekstra population. In a way this situation is not unlike that with regard to the (many) models for the evolution of sex: although various advantages for sex above parthenogenesis can be recognised, it is hard to overcome the two-tbld disadvantage of sex. Rather curiously, there appears to be also a two-fold disadvantage for differentiation into two mating types: at low frequency the undifferentiated mating type has a two-fold advantage over the differentiated types, because the latter can fuse with only half of the gamete population. This paper explores a wholly different idea, namely that sexual fusions have been asymmetric (i.e. between different types) from the very beginning of the origin of eukaryote sex. This implies that there must have been evolution of asymmetric cell fusion prior to the evolution of sex as a composite process. 2. Evolution of asymmetric cell fusion Consider a population of primitive eukaryote cells. Reproduction is by asexual fission, sex does not exist. Furthermore, suppose that some cells contain an endosymbiontic replicator, for example a virus. This virus can be transmitted vertically during cell division. There is however a probability (1 -p) of virus loss per cell division, in which case the newly formed cell does not contain the virus. Moreover, the virus can induce its host cell to fuse temporarily with another cell, thus infecting the other cell. Suppose that the probability of successful horizontal transmission of the virus is given by t (the parameter t reflects among other things the defense of the 'receptor' cell). There is a cost c to cell fusion, which comprises the loss in growth rate during the time of the fusion and subsequent separation and also the loss in fitness due to an enhanced risk of additional infection by other types of viruses. It is assumed that effects of the virus on the growth rate of the host cell can be neglected. The transmission cycle is modelled in a discrete-generation deterministic model as follows (see figure 1). The population of cells consists of two types: virus-free cells (frequency Xo) and cells containing the virus (frequency xl). The cells meet randomly in pairs, and if at least one of the cells in a pair contains the virus, horizontal transmission can be effected by fusion and subsequent separation. Then cell division occurs, during which vertical transmission of the virus may occur (with probability p). These assumptions lead to the following recurrence relations: Wx~ =x o [Xo+(1-c)(1-tp)xl] +(1-p)(1-c)xl ] Wx'1 = xlp(1 - c)(1 + tXo) ~ ' (1) where W= 1 -c(1 -x2). It is easily deduced from (1) that the existence of virus-free cells in the population is guaranteed (the fixed point Xo=0 is always unstable), alid that the frequency of infected cells increases when rare (i.e. the fixed point x~ =0 is unstable) if p(1-c)(l + t)> l. (2) This condition is easily fulfilled if the probabilities for horizontal and vertical transmission (t and p) are not too different from 1, and c (the cost of fusion) not too high. Male-female dimorphism 13 horizontaI vertical • 1.p Figure 1. Transmission cycle of the model organism. The population consists of two types of cells, virus-free (frequency xo) and infected (frequency x~). Cells meet randomly, and horizontal transmission of the virus may occur with probability t. There is a cost c attached to cell fusion and subsequent separation. During (asexual) replication the virus may be transmitted vertically with probability p. A stable equilibrium between the two types will be established if inequality (2) is satisfied. The equilibrium frequencies are given by the quadratic c2c2-tp(1 - c) ~o + (1 -c)(1 - p) = 0. (3) Now consider introduction into the population of a mutant virus (frequency x2) which causes its host to avoid fusion with an already infected cell. Thus cells contain- ing this mutant virus will only fuse with virus-free cells. This implies of course that the host cell, when in contact with another cell, must have the ability to detect the presence of a virus in the other cell, Presumably the easiest way to accomplish this is by specific recognition of the structures in the cell membrane which play a role in the fusion process. Now the population consists of three types of cells, and the dynamics of its composition are described by the following set of recurrence relations: wx~ = x0 [Xo + (1 - Xo)(1 - c){2- p (1 - t)}] + (l - p) [(1 - Xo) 2 - cx~], Wx'1 =pxl [(1 -e) {(1 + t)Xo+Xl} +x23 ] Wx'2=px2 [(1 -e)(1 +t)Xo+X 1 +x2] ~ ' (4) where W equals the sum of the right hand sides. The stability of the fixed point x 2=0 can be analysed by linearizing the third 14 Roll F. Hoekstra equation in (4). This results in the following condition for instability (guaranteeing initial increase of the mutant): (1 - c)(1 + t) 2 o + 1 - 20 > (1 - c)(1 + t2o), (5) where 20 is given by (3). However, there is no need to substitute an explicit expression for 2 o into (5), because for all possible values of 2 o inequality (5) is satisfied. Furthermore, we can write from (4) Xt2__X2[ (1--C)(I+t)Xo+X~+Xzj x'l xl (t--c)(l+t)xo+xt+Xz--CX t ' (6) from which it follows that cells containing the mutant virus will completely replace the cells with the original virus. Therefore, the population will finally consist of two types, namely virus-free cells and cells containing the virus, which induces horizontal transmission only upon contact with a virus-free cell. Thus the only fusions occurring in the population are asymmetric, namely between a virus-free cell and a cell carrying a virus. 3.' Discussion The model analysed in the preceding section suggests that under broad conditions evolution towards asymmetric cell fusion may occur. It would be very speculative indeed to build upon this result a further scenario for the evolution of sex. This is not the purpose of this paper. Basically, two different possibilities see m to suggest themselves. The first is that a "virus'-driven process such as analysed in this paper for the evolution of asymmetric cell fusions has formed one of the starting points for subsequent evolution towards (some form of) sex. It has been suggested by Hickey (1982) and Rose (1983) that sex might have originated as a consequence of a contagious genetic element which induced sex to promote its (horizontal) transmission.
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