Economy, Speed and Size Matter: Evolutionary Forces Driving Nuclear Genome Miniaturization and Expansion

Cavalier‐Smith, Thomas

doi:10.1093/aob/mci010

Cited by 334 publications

(312 citation statements)

References 134 publications

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“…Similar arguments have been made with respect to the evolution of ploidy level in unicellular organisms (Lewis, 1985), heterochromatic content (Cavalier-Smith, 2005) and genome size (Elser et al, 2000a;Hessen et al, 2008Hessen et al, , 2010. Of most direct relevance to our hypothesis is empirical evidence from algae and yeast suggesting that haploids are better competitors than diploids in low-P environments (Adams and Hansche, 1974;Destombe et al, 1993;Zeyl, 2004; but see Mable, 2001).…”

Section: Consequences Of High P Content For Asexual Ecologysupporting

confidence: 73%

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Can resource costs of polyploidy provide an advantage to sex?

2012

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The predominance of sexual reproduction despite its costs indicates that sex provides substantial benefits, which are usually thought to derive from the direct genetic consequences of recombination and syngamy. While genetic benefits of sex are certainly important, sexual and asexual individuals, lineages, or populations may also differ in physiological and life history traits that could influence outcomes of competition between sexuals and asexuals across environmental gradients. Here, we address possible phenotypic costs of a very common correlate of asexuality, polyploidy. We suggest that polyploidy could confer resource costs related to the dietary phosphorus demands of nucleic acid production; such costs could facilitate the persistence of sex in situations where asexual taxa are of higher ploidy level and phosphorus availability limits important traits like growth and reproduction. We outline predictions regarding the distribution of diploid sexual and polyploid asexual taxa across biogeochemical gradients and provide suggestions for study systems and empirical approaches for testing elements of our hypothesis.

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Section: Consequences Of High P Content For Asexual Ecologysupporting

confidence: 73%

“…Higher ploidy is generally associated with increased nuclear DNA content (Leitch and Bennett, 2004;Cavalier-Smith, 2005;Gregory, 2001Gregory, , 2005. This increased per-cell nuclear DNA content, however, does not necessarily translate into higher whole-organism P concentration.…”

Section: Polyploidy and Organismal Phosphorus Economicsmentioning

confidence: 99%

Can resource costs of polyploidy provide an advantage to sex?

2012

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“…Enslavement could have started as early as shown, but the major gene transfers into host chromosomes probably postdated the nuclear envelope (Cavalier-Smith in press). (viii) Endoplasmic reticulum (ER) cisternae attached to heterochromatin via the nuclear lamina to protect DNA from shearing damage by new cytoplasmic motors (Cavalier-Smith 2005); evolution of nuclear pore complexes from the same novel eukaryotic gene family as vesicle coats (Devos et al 2004) prevented lethal complete fusion; plugging their lumen and novel nucleocytoplasmic transport proteins excluded ribosomes, allowing mitochondrial group II introns transferred to host DNA to become spliceosomal introns only afterwards (Cavalier-Smith 1991b)-not before as Martin & Koonin (2006) mistakenly suggest. (b) Logic of the bacterial cell cycle involves DNA attachment to the cell surface by proteins and membrane division between attachment sites (Cavalier-Smith 1981, 1987b.…”

Section: Mapping the Tree Onto The Fossil Record (A) The Age Of Eukarmentioning

confidence: 99%

Cell evolution and Earth history: stasis and revolution

Cavalier‐Smith

2006

Phil. Trans. R. Soc. B

249

282

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This synthesis has three main parts. The first discusses the overall tree of life and nature of the last common ancestor (cenancestor). I emphasize key steps in cellular evolution important for ordering and timing the major evolutionary innovations in the history of the biosphere, explaining especially the origins of the eukaryote cell and of bacterial flagella and cell envelope novelties. Second, I map the tree onto the fossil record and discuss dates of key events and their biogeochemical impact. Finally, I present a broad synthesis, discussing evidence for a three-phase history of life. The first phase began perhaps ca 3.5 Gyr ago, when the origin of cells and anoxic photosynthesis generated the arguably most primitive prokaryote phylum, Chlorobacteria (ZChloroflexi), the first negibacteria with cells bounded by two acyl ester phospholipid membranes. After this 'chlorobacterial age' of benthic anaerobic evolution protected from UV radiation by mineral grains, two momentous quantum evolutionary episodes of cellular innovation and microbial radiation dramatically transformed the Earth's surface: the glycobacterial revolution initiated an oxygenic 'age of cyanobacteria' and, as the ozone layer grew, the rise of plankton; immensely later, probably as recently as ca 0.9 Gyr ago, the neomuran revolution ushered in the 'age of eukaryotes', Archaebacteria (arguably the youngest bacterial phylum), and morphological complexity. Diversification of glycobacteria ca 2.8 Gyr ago, predominantly inhabiting stratified benthic mats, I suggest caused serial depletion of 13 C by ribulose 1,5-bis-phosphate caboxylase/oxygenase (Rubisco) to yield ultralight late Archaean organic carbon formerly attributed to methanogenesis plus methanotrophy. The late origin of archaebacterial methanogenesis ca 720 Myr ago perhaps triggered snowball Earth episodes by slight global warming increasing weathering and reducing CO 2 levels, to yield runaway cooling; the origin of anaerobic methane oxidation ca 570 Myr ago reduced methane flux at source, stabilizing Phanerozoic climates. I argue that the major cellular innovations exhibit a pattern of quantum evolution followed by very rapid radiation and then substantial stasis, as described by Simpson. They yielded organisms that are a mosaic of extremely conservative and radically novel features, as characterized by De Beer's phrase 'mosaic evolution'. Evolution is not evenly paced and there are no real molecular clocks.

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“…Polyploids often have a somewhat lower genome size than expected from their diploid relatives (Song et al 1995;Leitch and Bennett 2004;Cavalier-Smith 2005). The mechanisms, which lead to genome downsizing in polyploids are still not understood although there are many analyses which have shown that the elimination of duplicated genes and loss of repetitive sequences could be the reasons.…”

Section: Genome Of C Albummentioning

confidence: 99%

Comparative cytogenetic analysis of diploid and hexaploid Chenopodium album Agg

2011

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Two cytotypes of Chenopodium album, diploid (2n=2x=18) and hexaploid (2n=6x=54), were analysed using flow cytometry and a FISH experiment. The genome size was indicated as 1.795 pg for the diploid and 3.845 pg for the hexaploid plants which suggested genome downsizing in the evolution of hexaploid cytotype. Double FISH with 25S rDNA and 5S rDNA allowed three to five homologue chromosome pairs to be distinguished depending on the cytotype. The variation in size and number of rDNA sites between the polyploid C. album and its putative diploid ancestor indicated that rDNA loci underwent rearrangements after polyploidization.Flow cytometry measurements of the relative nuclear DNA content in the somatic tissue of C. album revealed extensive endopolyploidization resulting in tissues comprising a mixture of cells with a different DNA content (from 2C to 32C) in varying proportions. The pattern of endopolyploidy was characteristic for the developmental stage of the plant and for the individual organ. Polysomaty was not observed in the embryo tissues however endopolyploidization had taken place in most tested organs of seedlings. The endopolyploidy in diploid and hexaploid C. album was compared to find any relationship between the pattern of polysomaty and polyploidy level in this species. This revealed that polyploid plants showed a decline in the number of endocycles as well as in the frequency of endopolyploidy cells compared to diploid plants.

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Economy, Speed and Size Matter: Evolutionary Forces Driving Nuclear Genome Miniaturization and Expansion

Abstract: The quantitatively proportional correlation between genome size and cell size cannot be explained by purely mutational theories, as eukaryote cell volumes are causally determined by cell cycle control genes, not by DNA amounts.

Cited by 334 publications

References 134 publications

Can resource costs of polyploidy provide an advantage to sex?

Can resource costs of polyploidy provide an advantage to sex?

Cell evolution and Earth history: stasis and revolution

Comparative cytogenetic analysis of diploid and hexaploid Chenopodium album Agg

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