The maintenance of sex

Having drawn a scenario for the origins of sex, and thought of ways in which the various steps might be selected for, we are left with explaining its persistence and prevalence. It is clear that those lineages that evolved sex have gone on to diversify into millions of species that have largely retained sex. In some, however, clonal reproduction has secondarily arisen (these are normally called parthenogens). Is the commonness of sex due to the rarity of reversal to the clonal state? It is undoubtedly part of the answer. Some animals and plants, for example, have no known parthenogens, despite being species rich and well known. They include birds, mammals, and gymnosperms (conifers and their kin). In each of these three groups, mechanisms are known that are likely to have prevented reversal to the clonal state.

In birds,parthenogenetic individuals sometimes arise but these fail to persist as unisexual lines. The reason is that in birds the female is the hetero-gametic sex (with a 'Z' and a 'W' chromosome). During parthenogenesis, chromosome doubling occurs as normal, but there is only one subsequent division, leaving diploid eggs. Many of these will contain two Z chromosomes, leading to male production,and hence maintaining both sexes (Crews 1994). This is a big pity for short-term poultry production! If in birds, females were the homogametic sex (two X chromosomes), all parthenogenetic offspring would also have to be female. Given that in mammals females are the homogametic sex, one would imagine that cattle, sheep, and pig producers would have had more luck, but here prevention of parthenogenesis comes from another source.

In mammals the phenomenon that prevents parthenogenesis is known as genomic imprinting. The phenomenon was first noticed when researchers tried but failed to get embryos to develop by fusion of two egg nuclei. The reason is that early zygote development requires genes from both parents that have different levels of activation: if the genes come from the same parent the activation levels are all wrong. We will encounter this phenomenon again in Chapter 7,but,briefly,the reason is likely to be that in mammals parents conflict over what level of gene activation in the zygote is preferred, setting up an offensive/defensive gene activation war (e.g. Burt and Trivers 1998).

In gymnosperms the mystery is more clear-cut: although the egg provides most of the organelles for the zygote, it is the pollen that provides the chloro-plasts. Unisexual gymnosperms would lack the ability to photosynthesize. Provision of an essential organelle is also the likely reason for general rarity of animal parthenogenesis, and also for the strange forms it takes when present. In many animals, the sperm provides a centriole to the zygote. In many parthenogenetic animals, including most clonal vertebrates, parthenogenesis is 'sperm-dependent': the eggs need to be 'fertilized' by sperm of another species for successful development, though the sperm genome never makes it into the next generation (Beukeboom and Vrijenhoek 1998).

Though obstacles to reversal are one important reason why sex is still prevalent, it is not the whole story. Many plants, for example, could easily persist from generation to generation in a clonal state by vegetative reproduction. Yet, where they exist, wholly clonal plants, and parthenogenetic organisms in general, appear to be relatively recent phenomena. For example, most are isolated species in genera that are predominantly sexual. In a few cases, genetic and other techniques have been used to estimate the actual ages of clones and their sexual parents. In the case of the genus Poeciliopsis, a guppy fish that inhabits streams in southern United States and Mexico, sexual species are up to 3 My old, but their sperm-dependent parthenogens are mostly less than a few thousand (Figure 2.5). Interestingly, the oldest surviving clone is also the only one where the sperm genome finds

Fig. 2.5 The unisexual fish Poeciliopsis 2monacha-lucida. This species is a sperm-dependent parthenogen, meaning it relies on the sperm of another species for reproduction. However, the genome of the sperm donor is not expressed in the offspring which are genetically identical to their mother. This species suffers more from parasites than its sexual relatives, hence supports the 'Red Queen' hypothesis for the maintenance of sex. Photo courtesy of Bob Vrijenhoek.

Fig. 2.5 The unisexual fish Poeciliopsis 2monacha-lucida. This species is a sperm-dependent parthenogen, meaning it relies on the sperm of another species for reproduction. However, the genome of the sperm donor is not expressed in the offspring which are genetically identical to their mother. This species suffers more from parasites than its sexual relatives, hence supports the 'Red Queen' hypothesis for the maintenance of sex. Photo courtesy of Bob Vrijenhoek.

expression in the fish phenotype, the so called 'hybridogen' (it is later excluded from gamete production though). Only recent originations persist probably because earlier originations have largely gone extinct while their sexual relatives have not (Vrijenhoek 1994). There are a relatively few higher taxa that have persisted for millions of years, popularly known as the 'ancient asexu-als'. Our theories for why parthenogens might have high extinction rates should ideally account for these exceptions.

The problem of the relative persistence of sexual species versus asexual clones has traditionally been thought of in terms of the so-called 'two-fold cost' of sex. Female parthenogens can increase in number at twice the rate of their sexual counterparts because they do not give birth to males, which cannot themselves give birth (Figure 2.6). Sexual organisms may even suffer a number of additional costs, such as finding a mate. All of this suggests that sexual organisms should be the ones with the higher extinction rates. It was this problem that eventually became the focus of Hamilton's research: why was it that clones, once they arose, did not quickly send their sexual parents extinct? Hamilton became convinced that the answer lay with one of the short-term advantages of recombination, in particular the Red Queen hypothesis. There is evidence to support his contention. First, some

Fig. 2.6 The two-fold cost of sex. Here a species is shown which always has two offspring per generation, except that in the sexual form half of these are male, which mate with the females (dotted arrows), while the unisexual form can have offspring without mating. By the third generation, there are four females in the unisexual line but only one female in the sexual line.

Generation 1

Generation 2

Generation 3

Generation 1

Generation 2

Generation 3

Fig. 2.6 The two-fold cost of sex. Here a species is shown which always has two offspring per generation, except that in the sexual form half of these are male, which mate with the females (dotted arrows), while the unisexual form can have offspring without mating. By the third generation, there are four females in the unisexual line but only one female in the sexual line.

of the so-called ancient asexuals are obligate mutualists. These include some mycorrhizal fungi, which inhabit the roots of plants, and the fungi that are the food for leaf-cutter ants. In contrast to parasites, which experience directional selection from their hosts, mutualists would be expected to experience stabilizing selection to aid the efficiency of the interaction. This, as Maynard Smith showed, can select for an absence of recombination. In addition, we have direct measures from some asexual clones that they carry higher parasite loads than their sexual counterparts. This is true, for example, of the Poeciliopsis clones (Vrijenhoek 1994, Figure 2.5).

Clones, of course, may also suffer a higher load of deleterious mutations, as Kondroshov showed, contributing to their extinction rate. In Poeciliopsis, there is also evidence for this. By a clever series of crosses, it has been possible to express the hybridogen genes that are normally dominated by those of the sperm donor. These show several developmental defects compared with the parental or hybrid genotypes.

In addition to Kondrashov's mechanism, an alternative long-term mechanism can account for this, known as Muller's ratchet. Muller's ratchet is in some ways more general than Kondrashov's theory, for it does not rely on synergistic mutations; mutations merely have to be of small effect. It also only works in small populations, but that is probably a fairly general phenomenon. When mutations are of small effect, the distribution of those mutations at equilibrium among individuals will be approximately bell-shaped: few will be completely free of them, most will have a few, and only a few will have a lot (Figure 2.4).In a small population, however, the categories of individual with no mutations is easily lost by chance events, even if they are the most fit. In a clonal population, these can never be recovered. Of course, the category of individuals with most mutations can also be lost, but those are replaced by subsequent mutation.

Overall then, in a clonal population, the load of slightly deleterious mutations continually cranks up, ratchet-like. In a sexual population, however, recombination recreates individuals free of mutation, and the genetic load remains stable despite stochastic loss of the fittest individuals (Figure 2.4). Note that because of the long-term nature of the mechanism, it cannot be invoked to explain the origination of recombination, merely its persistence relative to clonal reproduction.

In general, should we be searching for long- or short-term mechanisms to explain the persistence of sex? Hamilton was convinced that the latter was necessary largely because of competition between clone and sexual parent. Is there in fact evidence for this? Do clones actually displace their sexual parents, and is there a risk of them being sent entirely extinct? In general, we might expect, in the absence of short-term advantage, that the clone would successfully displace the parent from part of its former range, but that existing genetic diversity among the parent would allow the parent to persist in parts of its range to which the clone is less adapted. In Poeciliopsis, the diversity of species is inversely related to the diversity of clones, suggesting some competitive exclusion. In many plants, such as the dandelions, parthenogenetic forms also appear prevalent in some environments, especially at high altitudes and latitudes. This in turn suggests that the costs and benefits of each form of reproduction vary spatially, and also that short-term advantages of sex are not always initially enough to compensate for any costs.

To summarize, the maintenance of sex has been influenced by the following processes: first, constraints to reversal among a number of lineages, particularly animals. Second, clones can successfully displace their sexual competitors from some environments, suggesting a severe cost to sex. However, directional selective forces can compensate for these costs in some environments, and, combined with increased genetic loads, send most clones extinct relatively rapidly.

How does the evolution of sex compare with the other major transitions? Maynard Smith and Szathm√°ry identify several common features of the transitions (Table 2.1). Of these, sex is very illustrative. Entities have combined together, through the evolution of syngamy, to form a sexual population from previously independent clones. Further, reversal of sex to the clonal state is sometimes difficult because sex has developed a complex machinery for reproduction. Sex has probably led to conflict between entities, such as between organelles in the parent gametes for representation

Table 2.1 The common features of the major transitions in evolution

Feature

Molecules in compartments

Chromosomes

protein

Eukaryotes

Multicellular life

Sex

Social colonies

Language

Entities

Yes

Yes

No

Yes

Yes

Yes

Yes

No

combine?

New ways

No

No

Yes

No

No

Yes

No

Yes

of

information

transmission?

Reversal

Yes

Yes

Yes

Yes

Yes

Yes

Yes

?

difficult?

Conflict

Yes

Yes

No

Yes

Yes

Yes

Yes

No

between

entities?

Mechanisms

Yes

Yes

No

Yes

Yes

Yes

Yes

No

to prevent

conflict?

Division of

Yes

Yes

Yes

Yes

Yes

Yes

Yes

No

labour?

in the zygote. To solve this, mechanisms, such as uniparental inheritance have evolved. Sex has led to division of labour among the combining entities, such as male and female gametes. In the evolution of sex, there has been no new method of transmitting information developed. That has only occurred in three of the transitions: in the origin of DNA and protein from RNA, in the origin of language, and in the origin of epigenesis (gene activation) in the origin of multicellular life.

In this chapter we have been postulating processes that have caused change within lineages through natural selection, a theme that will continue in the next several chapters. I cannot help but end here with a well-known quote from Aldous Huxley who once said that 'an intellectual is a person who has discovered something more interesting than sex'. There is a certain irony in this quote for evolutionary ecologists. Many of them would argue, on purely intellectual grounds, that there is in fact nothing more interesting than sex, full stop.

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