The concept of the sexual reproduction cycle and its evolutionary significance

Abstract

The concept of a "sexual reproduction cycle (SRC)" was first proposed by Bai and Xu (2013) to describe the integration of meiosis, sex differentiation, and fertilization. This review discusses the evolutionary and scientific implications of considering these three events as part of a single process. Viewed in this way, the SRC is revealed to be a mechanism for efficiently increasing genetic variation, facilitating adaptation to environmental challenges. It also becomes clear that, in terms of cell proliferation, it is appropriate to contrast mitosis with the entire SRC, rather than with meiosis alone. Evolutionarily, it appears that the SRC was first established in unicellular eukaryotes and that all multicellular organisms evolved within that framework. This concept provides a new perspective into how sexual reproduction evolved, how generations should be defined, and how developmental processes of various multicellular organisms should properly be compared.

Keywords: fertilization; generation; heterogametogenesis; meiosis; sexual reproduction cycle.

FIGURE 1

Illustration of the role of cohesins in the origin of meiosis. (A) Cohesins hold sister chromosome together during mitosis. (B) Cohesins mistakenly hold non-sister but homologous chromosomes together, enhanced by kinetochore-associated protein Mei-332/Sgo1 during meiosis. Modified from Marston and Amon (2004), by permission of Nature Publishing Group.

FIGURE 2

Comparison of life cycles of various autotrophic organisms emphasizing the divergence points resulting in dimorphic structures related to heterogametogenesis. From left to right: life cycles of selected species representing unicellular green algae (Chlamydomonas), multicellular green algae (Ulva), mosses (Polytrichum), ferns Ploypodium), gymnosperms (Pinus), and angiosperms (Arabidopsis) are briefly outlined. Green arrows indicate morphological transitions in sporophyte generations. Light green arrows indicate morphological transitions in gametophyte generations. Red triangles indicate the major divergence points leading to dimorphic development for heterogametogenesis. The major divergence points are shifted from post-meiosis in green algae, mosses, and ferns (in some species like Ploypodium) to before meiosis in gymnosperms and angiosperms. Reprinted from Bai and Xu (2013), by permission of Elsevier.

FIGURE 3

Diagram of the sexual reproduction cycle (SRC). (A) A regular cell cycle for proliferation, through which one cell becomes two, and environmental conditions trigger or affect the cycle at various points in the process. (B) A “SRC.” Three hypothetically random and independent events, “primitive meiosis,” “primitive fertilization,” and “primitive sex,” occasionally integrated and were selected for advantages in adaptation. The net result of the SRC is that one cell becomes two, just as in the regular cell cycle, regardless of how these events evolved and were integrated (of which little is known). (C) Core processes of the life cycles of multicellular organisms. From the perspective of the SRC, it is clear that all multicellular structures arose in the interval phases of the SRC through the regular cell cycle and cellular differentiation, whether diploid (in almost all organisms) or haploid (mainly in plants and fungi). Modified from Bai and Xu (2013), by permission of Elsevier.

FIGURE 4

Comparison of morphogenetic strategies of animals, fungi, and plants in the framework of SRC. Yellowish background indicates diploid phase and bluish haploid phase. In the intervals between zygote and germ cells, multicellular structures of animals (red) and plants (green) are interpolated, while there are none in fungi (pink). In the intervals between meiotically produced cells and gametogenic cells, multicellular structures are interpolated for fungi and plants but not animals.