Did meiosis evolve before sex and the evolution of eukaryotic life cycles?

Abstract

Biologists have long theorized about the evolution of life cycles, meiosis, and sexual reproduction. We revisit these topics and propose that the fundamental difference between life cycles is where and when multicellularity is expressed. We develop a scenario to explain the evolutionary transition from the life cycle of a unicellular organism to one in which multicellularity is expressed in either the haploid or diploid phase, or both. We propose further that meiosis might have evolved as a mechanism to correct for spontaneous whole-genome duplication (auto-polyploidy) and thus before the evolution of sexual reproduction sensu stricto (i.e. the formation of a diploid zygote via the fusion of haploid gametes) in the major eukaryotic clades. In addition, we propose, as others have, that sexual reproduction, which predominates in all eukaryotic clades, has many different advantages among which is that it produces variability among offspring and thus reduces sibling competition.

A few of our favorite things: Pairing, the bouquet, crossover interference and evolution of meiosis

“…1, 2). Moreover, the current evolved process differs substantially in different organisms, likely with more variants as yet to be discovered.…”

On the evolution of bacterial multicellularity

“…The evolution of multicellularity as a stress response is an intriguing idea as it puts it in a category shared with other significant evolutionary advances. For example, meiosis in eukaryotes may have originally been a response to adverse conditions or accidental increases in ploidy [35]. Likewise, recombination enzymes that evolved to repair damaged DNA were co-opted to share DNA and shuffle genes within a population, greatly accelerating the rate of evolution [36].…”

The evolution of the plant genome-to-morphology auxin circuit

“…Nevertheless, even though considerable progress has been made at both ends of attempts to construct a 'genometo-morphology' map, a review of the primary literature justifies the perception that the gap between understanding how the genome functions and how this functionality evokes plant morphogenesis remains large (Niklas et al 2014(Niklas et al , 2016. For example, despite the elegant work that has revealed the genomics and physiology of, perhaps, the most extensively researched plant hormone auxin (i.e., indole-3-acetic acid, IAA), not a single complete sequence of events has been discovered that links IAA-response genes directly to a discrete morphogenetic event at the cellular or organismic level.…”

“…One example of the recruitment of an epigenetic system in plant development is the polycomb group (PcG) protein complex. By virtue of one of the three SET domain proteins (i.e., CURLY LEAF, CLF; SWINGER, SWN; or MEDEA, MEA), which act as a catalytic subunit, the PcG complex methylates lysine 27 on histone 3 (H3K27me3) (Lachner et al 2003;Nekrasov et al 2005 Kutschera 2009, 2010;Niklas et al 2014). For example, FIE is involved in the megagametophyte-to-sporophyte transition in the life cycle of the flowering plants (Goodrich 1998;Kohler et al 2003).…”