Oxygen, life forms, and the evolution of sexes in multicellular eukaryotes

Abstract

The evolutionary advantage of different sexual systems in multicellular eukaryotes is still not well understood, because the differentiation into male and female individuals halves offspring production compared with asexuality. Here we propose that various physiological adaptations to oxidative stress could have forged sessility versus motility, and consequently the evolution of sexual systems in multicellular animals, plants, and fungi. Photosynthesis causes substantial amounts of oxidative stress in photoautotrophic plants and, likewise, oxidative chemistry of polymer breakdown, cellulose and lignin, for saprotrophic fungi. In both cases, its extent precludes motility, an additional source of oxidative stress. Sessile life form and the lack of neuronal systems, however, limit options for mate recognition and adult sexual selection, resulting in inefficient mate-searching systems. Hence, sessility requires that all individuals can produce offspring, which is achieved by hermaphroditism in plants and/or by multiple mating types in fungi. In animals, motility requires neuronal systems, and muscle activity, both of which are highly sensitive to oxidative damage. As a consequence, motility has evolved in animals as heterotrophic organisms that (1) are not photosynthetically active, and (2) are not primary decomposers. Adaptations to motility provide prerequisites for an active mating behavior and efficient mate-searching systems. These benefits compensate for the "cost of males", and may explain the early evolution of sex chromosomes in metazoans. We conclude that different sexual systems evolved under the indirect physiological constraints of lifestyles.

cROStalk for Life: Uncovering ROS Signaling in Plants and Animal Systems, from Gametogenesis to Early Embryonic Development

“…Although ROS are constitutive by-products of essential functions, such as respiration in mitochondria, photosynthesis, and photorespiration in chloroplasts/peroxisomes [ 33 ], their production nevertheless increases during exposure to biotic and abiotic stresses, which therefore are referred to as “oxidative stresses” [ 34 ]. In particular, the sessile nature of plants forces them to heavily rely on stress resilience strategies rather than stress avoidance [ 35 ]. Therefore, plant cells, more than animal cells, must keep steady-state levels of the various ROS under strict control, to avoid any ROS damaging effect on the macromolecules (lipids, DNA, and proteins).…”

“…As a matter of fact, transcriptome analysis performed of plant female gametophyte gene expression revealed common molecular pathways affecting gamete (syngamy) and nuclear fusion (karyogamy) between those lineages [ 295 ]. Several reproductive patterns of angiosperms evolved similar to those in mammals, for instance, the embryo development surrounded by a maternal environment providing nutrients, the programmed arrest of the mature gamete before fertilization event, the presence of common parental imprinting evolved in both groups, and a selection based on male–male competition [ 35 , 296 , 297 , 298 , 299 , 300 , 301 , 302 ]. In animals, ROS is involved in sperm activation and in egg activation and fertilization [ 214 , 284 , 303 , 304 ].…”

Were eukaryotes made by sex?

“…[ 10 ] Horandl, Hadacek, and Speijer suggested that sex evolved in response to the massive amounts of ROS internally released by the newly acquired mitochondria. [ 11–13,67 ] A further recent theory by Tilquin, Christie, and Kokko [ 14 ] suggested that sex started with cell fusion to enable mitochondrial complementation to overcome mitochondrial decay by a mutational Muller's ratchet. Very recently Colnaghi, Lane, and Pomiankowski proposed that meiosis had to replace HGT to stop Muller's ratchet in view of the massive increase in genome size of eukaryotes.…”

“…These theories thus disregarded the conditions that we presently assume to have existed in early endosymbiotic eukaryotes. An exception to this are several recent hypotheses [10][11][12][13][14][15] that will be briefly described below.…”

“…I hypothesize that the appearance of sex enabled early eukaryotes to merge the genome of endosymbionts and host and to evolve into our highly complex common ancestor LECA (Last Eurkaryotic Common Ancestor). LECA already had all the molecular tools of meiotic sex [ 13 ] and the vast majority of the many exciting forms of life that descended from it perform, at least occasionally, sex to this day. I further suggest that sex continues to be vital for regulating DNA insertions from various sources into the genome.…”