Let's talk about sex

Abstract

Most people know that using the word “sex” in a title will get you many more “clicks.” So, now that you are here, how do I hold your attention? By doing two things: (i) tell you about one of the most beautiful scientific articles I ever encountered, and (ii) explain how the process of eukaryotic “meiotic” sex illustrates exquisitely that biology can only be understood as the interplay of historical accident and physio-chemical constraints. I will start with (ii). Though the studies about meiotic sex fill libraries, most researchers focus on just a few basic, interrelated, questions: Why settle for only giving half your genome to a new generation (if lucky enough to be able to) instead of just cloning yourself?; How did this elaborate, complex, process evolve and under which selective pressures?; How do selective forces during its origins relate to present-day advantages (if any)?

Thus, simply put: Meiotic sex, what is it good for? To present just a few answers: (i) The Red Queen “arms race” model, stating that as species (constituting prey, predator, host, and pathogen) are constantly pitted against other rapidly evolving opposing species, they have to change quickly, and only sex enables this^[1]; (ii) The first model can be seen as a specific instance of a more general framework: recombination, implicit in meiotic sex, allows a much faster probing of the space of combinatorial possibilities: selecting winners and weeding out losers^[2]; (iii) Overcoming the limitations imposed by Muller's Ratchet: the process leading to accumulated, irreversible, deleterious mutations. Absent purifying sexual recombination, only organisms combining small genomes and low mutational loads can survive. Thus, without meiotic sex, the larger genomes of eukaryotes would be unsustainable.

Here we come to the crucial insight illustrating the interaction of historical accidents and nature's laws in biology. All the hypotheses mentioned explain the possible advantages, but as evolution has no foresight, only the last framework can be used to explain the emergence of meiotic sex and its presence in the last eukaryotic common ancestor, because it invokes direct adaptation to actual selection forces, instead of later advantages. Many researchers now accept that eukaryotes emerged from the merger of an (Asgard) archaeon and an alpha-proteobacterial endosymbiont, capable of oxidative respiration, which would become the mitochondrion.^[3] Thus, the evolving organism would have had to contend with an initial genome doubling in size and (much) higher mutation rates because of internal reactive oxygen species (ROS) formation. Considering Muller's Ratchet: a deadly combination. Archaeal genome repair mechanisms evolved into full blown meiotic sex next.^[4] If that reconstruction is correct, all eukaryotes including anaerobic lineages (Parabasalia, Fornicata, and Preaxostyla) must have come from ancestors with aerobic mitochondria, because ancestral meiotic processes have been retained. Invoking older, anaerobic endosymbionts in these groups^[5] is thus unlikely.

So far, theoretical considerations have dominated. Are there empirical data to test hypotheses? Here my favorite study comes in. Darwin was already very interested in a later instance of meiotic sex, that is, sexual selection, the process in which partners are selected by “male competition” and “female choice”; here behavior and looks are essential. Gage and colleagues introduced the perfect setup to study this, using red flour beetle populations.^[6] These were bred for 7 years (∼50 generations), under different conditions of sexual selection or in its absence. In a beautiful twist, following the different regimens, specimens were challenged with uninterrupted inbreeding, in a 3-year extinction assay. What came out of >10 years of meticulous research? Populations without sexual selection indeed succumb to Muller's Ratchet, but prior selection significantly extended population survival times. In these experiments, male competition was more effective than female choice. Everybody should read this elegant contribution to evolutionary science: it is a joy. Alas, I never got to meet Professor Gage, who died prematurely in 2022. His touching obituary highlights his many contributions to evolutionary ecology.^[7]