.

umerous clonal genomes have revealed great adaptive potential.

To understand why sex has evolved, we must answer two crucial questions: i) what are the key differences between eukaryotes and bacteria and ii) why do some eukaryotes use asexual reproduction.

Sexual reproduction is not characterized by only recombination and sex should be defined as a process which combines recombination, meiosis, gametogenesis and syngamy. Although some fungi seem show multiple mating types, the definition of sex centers on the nature of sexual cell being produced [see Hurst, 1996], so that it could be reasoned that there are only two sexes: males with motile sperm and females with larger eggs. Further, it may be thought that isogamy is been the ancestral state.

The oldest eukaryotes appeared more than 3 billion years [Javaux et al., 2010], so it is plausible that proto-eukaryotes diverged from prokaryotes very early in the evolutionary history.  Genetic exchanges appear to be a very archaic process, and sex may originate from horizontal gene transfer occurring in primitive steps of proto-cell development in primitive prebiotic "bubbles".

Indeed, the evolution of sex can alternatively be described as a kind of horizontal gene exchange that is independent from reproduction. According to the Thierry Lodé's "libertine bubble theory", sex originated from an archaic gene transfer process among prebiotic bubbles [Lodé 2011a, b, c].

At the origin, a macromolecular replicating system of polymers could be encapsulated within a membrane-bounded bubble. It can be suggested that the difference of cell proto-membranes built the first major evolutionary bifurcation between bacteria and eukaryotes. The proto-membrane should have kept a partial permeability, whereas the peptidoglycan cell wall of bacteria served as protection against severe primitive environmental conditions, maybe because the proto-eukaryotes were housed in hollows of the primitive substrate. Genetic drift entails that bubbles progressively differed from a fold to another. Selective porosity of proto-cell membranes, i.e. sensibility, should be selected as long as the process favors the exchange and the possible replication of compatible genetic material. Further, the evolution of nuclear compartment in proto-eukaryotic cells could result from physicochemical forces.

The contact among the pre-biotic bubbles could, through simple food or parasitic reactions, promote the transfer of genetic material from one bubble to another in promiscuitous conditions.  As a physical process of the exchange of DNA, recombination may also be a blind way for a self-promoting element to spread. That interactions between two organisms be in balance appear to be a sufficient condition to make these interactions evolutionarily efficient, i.e. to select bubbles that tolerate these interactions (“libertine” bubbles) through a blind evolutionary process of self-reinforcing gene correlations and compatibility

The "libertine bubble theory" proposes that meiotic sex evolved in proto-eukaryotes to solve a problem that bacteria did not have, namely a large amount of DNA material [Lodé 2012, JMB], occurring in an archaic step of proto-cell formation and genetic exchanges. Sex could stem from a signal that leads to increased reproductive output of all interacting individuals and evolved as a more and more efficient specialized interaction.

This evolutionary scenario seems reasonable because genetic exchanges renovate the set of proteins involved in metabolic reactions and may result in adaptations for dealing with stress, especially in overcrowding conditions. So that, rather than providing selective advantages through reproduction, sex could be thought of as a series of separate events which combines step-by-step some very weak benefits of recombination, meiosis, gametogenesis and syngamy.

Then, gametes developed in specialized containers of DNA able to be dispersed and specific sexual traits evolved to attract congeners of the opposite sex, and thereby to favor sexual reproduction. It has been also suggested that eukaryotic lineages evolved from ancestors that could adopt both male and female roles [see also Crews 2012]. Most descriptions of asexual reproduction in eukaryotes are particularly confused [see Lodé 2013]. It could be argued that most of these populations have lost sex by adopting a form of endomitosis reproduction, often with a normal meiosis preceded by a replication. In numerous plants, apomixy occurs with a meiosis in which one division is suppressed.


Male-like behaviour in female Aspidoscelis whiptail lizard (parthenogenic sp)

Therefore, current sexual species could be descendants of primitive organisms that practiced more stable exchanges in the long term, while asexual species have emerged, much more recently in evolutionary history, from the conflict of interest resulting from anisogamy. Sexual conflict results in sex loss in certain eucaryotic organisms such as rotifers or Aspidoscellis whiptail lizard.

 SEX IS A PRIMITIVE INTERACTION


see also Lodé Thierry 2011 La biodiversité amoureuse, sexe & évolution. Eds O Jacob.
Video at http://www.youtube.com/watch?v=6GxjUgTAxlI

References

Crews D 2012: The (bi)sexual brain. Embo Rep. (in press, 2012) 
Hurst LD 1996 : Why are there only two sexes ? Proc R Soc Lond B 263:415-422.
Javaux EJ, Marshall CP, Bekker A 2010 : Organic-walled microfossils in 3.2 billion-year-old shallow-marine siliciclastic deposits. Nature 463:934-938.