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

Elvira Hörandl,Franz Hadacek

doi:10.1038/s41437-020-0317-9

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.

Highlights

We will argue that these physiological adaptations to oxidative stress offer explanations why we find sessile and motile life forms, and how these life forms promote the evolution of two or more sexes in multicellular complex organisms
The following sections will focus on the adult, differentiated organisms and their basic physiological constraints, which we propose to determine their sexual systems
We propose that physiological constraints, such as maintenance of redox homeodynamics, might have contributed fundamentally to shaping of the evolution of sexes, albeit in indirect ways

Summary

1234567890();,: 1234567890();,: Introduction

Understanding why and how eukaryotic sex evolved remains one of the key unresolved questions in evolutionary biology. We will argue that these physiological adaptations to oxidative stress offer explanations why we find sessile and motile life forms, and how these life forms promote the evolution of two or more sexes in multicellular complex organisms (animals, fungi, and plants). In this context, we will not focus on protists due to lack of cell differentiation, but provide arguments on why we have separate sexes in the great majority of metazoans, but combined sexes in most plants. In animals with separate sexes, only about 50% of individuals, the females, can produce offspring—but with a higher certainty of reproductive success and quality of offspring because of motility, sensory organs, and mating behavior allowing for sexual selection. Animals require a qualityoriented sexual system to meet the physiological constraints of motility, and they optimize it by differentiation of two sexes (Fig. 1)

Conclusions and outlook

Findings

Compliance with ethical standards