Genome expansion in early eukaryotes drove the transition from lateral gene transfer to meiotic sex.

Marco Colnaghi,Nick Lane,Andrew Pomiankowski

doi:10.7554/elife.58873

Abstract

Prokaryotes acquire genes from the environment via lateral gene transfer (LGT). Recombination of environmental DNA can prevent the accumulation of deleterious mutations, but LGT was abandoned by the first eukaryotes in favour of sexual reproduction. Here we develop a theoretical model of a haploid population undergoing LGT which includes two new parameters, genome size and recombination length, neglected by previous theoretical models. The greater complexity of eukaryotes is linked with larger genomes and we demonstrate that the benefit of LGT declines rapidly with genome size. The degeneration of larger genomes can only be resisted by increases in recombination length, to the same order as genome size - as occurs in meiosis. Our results can explain the strong selective pressure towards the evolution of sexual cell fusion and reciprocal recombination during early eukaryotic evolution - the origin of meiotic sex.

Highlights

Understanding the origin and maintenance of sex in the face of multiple costs was long considered the ‘Queen of problems in evolutionary biology’ (Bell, 1982)
Asexual organisms are well known to be vulnerable to the effects of drift, which reduces the genetic variation within a population, causing the progressive and inescapable accumulation of deleterious mutations known as Muller’s ratchet (Muller, 1964; Haigh, 1978; Otto, 2009)
The exchange of genetic material does occur through transformation, the lateral gene transfer (LGT) and recombination of environmental DNA

Summary

Introduction

Understanding the origin and maintenance of sex in the face of multiple costs was long considered the ‘Queen of problems in evolutionary biology’ (Bell, 1982). Sexual reproduction breaks up advantageous combinations of alleles, halves the number of genes transmitted to the offspring, and is less efficient and energetically more costly than asexual reproduction (Bell, 1982; Otto and Lenormand, 2002; Otto, 2009). In spite of these disadvantages sex is a universal feature of eukaryotic life. The selective pressures that gave rise to the origin of meiotic sex must be understood in the context of early eukaryotic evolution

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