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

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.

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

10.1101/2020.03.21.001685 ◽

2020 ◽

Author(s):

Marco Colnaghi ◽

Nick Lane ◽

Andrew Pomiankowski

Keyword(s):

Gene Transfer ◽

Genome Size ◽

Lateral Gene Transfer ◽

Genetic Material ◽

Theoretical Models ◽

Deleterious Mutations ◽

Strong Constraint ◽

Muller's Ratchet ◽

Muller’S Ratchet ◽

Recombination Length

ABSTRACTProkaryotes generally reproduce clonally but can also acquire new genetic material via lateral gene transfer (LGT). Like sex, LGT can prevent the accumulation of deleterious mutations predicted by Muller’s ratchet for asexual populations. This similarity between sex and LGT raises the question why did eukaryotes abandon LGT in favor of sexual reproduction? Understanding the limitations of LGT provides insight into this evolutionary transition. We model the evolution of a haploid population undergoing LGT at a rate λ and subjected to a mutation rate μ. We take into account recombination length, L, and genome size, g, neglected by previous theoretical models. We confirm that LGT counters Muller’s ratchet by reducing the rate of fixation of deleterious mutations in small genomes. We then demonstrate that this beneficial effect declines rapidly with genome size. Populations with larger genomes are subjected to a faster rate of fixation of deleterious mutations and become more vulnerable to stochastic frequency fluctuations. Muller’s ratchet therefore generates a strong constraint on genome size. Importantly, we show that the degeneration of larger genomes can be resisted by increases in the recombination length, the average number of contiguous genes drawn from the environment for LGT. Large increases in genome size, as in early eukaryotes, are only possible as L reaches the same order of magnitude as g. This requirement for recombination across the whole genome 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.

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Can biochemical properties serve as selective pressure for gene selection during inter-species and endosymbiotic lateral gene transfer?

Systems Biology ◽

10.1049/ip-syb:20050082 ◽

2006 ◽

Vol 153 (4) ◽

pp. 212 ◽

Cited By ~ 2

Author(s):

C. Ringemann ◽

O. Ebenhöh ◽

R. Heinrich ◽

H. Ginsburg

Keyword(s):

Gene Transfer ◽

Lateral Gene Transfer ◽

Gene Selection ◽

Selective Pressure ◽

Biochemical Properties

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Horizontal Gene Transfers from Bacteria toEntamoebaComplex: A Strategy for Dating Events along Species Divergence

Journal of Parasitology Research ◽

10.1155/2016/3241027 ◽

2016 ◽

Vol 2016 ◽

pp. 1-10 ◽

Cited By ~ 2

Author(s):

Miguel Romero ◽

R. Cerritos ◽

Cecilia Ximenez

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Entamoeba Histolytica ◽

Lateral Gene Transfer ◽

Adaptive Radiation ◽

Fossil Record ◽

Evolutionary History ◽

Divergence Time ◽

Eukaryotic Evolution ◽

History Of

Horizontal gene transfer has proved to be relevant in eukaryotic evolution, as it has been found more often than expected and related to adaptation to certain niches. A relatively large list of laterally transferred genes has been proposed and evaluated for the parasiteEntamoeba histolytica. The goals of this work were to elucidate the importance of lateral gene transfer along the evolutionary history of some members of the genusEntamoeba, through identifying donor groups and estimating the divergence time of some of these events. In order to estimate the divergence time of some of the horizontal gene transfer events, the dating of someEntamoebaspecies was necessary, following an indirect dating strategy based on the fossil record of plausible hosts. The divergence betweenE. histolyticaandE. nuttalliiprobably occurred 5.93 million years ago (Mya); this lineage diverged fromE. dispar9.97 Mya, while the ancestor of the latter separated fromE. invadens68.18 Mya. We estimated times for 22 transferences; the most recent occurred 31.45 Mya and the oldest 253.59 Mya. Indeed, the acquisition of genes through lateral transfer may have triggered a period of adaptive radiation, thus playing a major role in the evolution of theEntamoebagenus.

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