Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity

  1. Michael Freeling1,3 and
  2. Brian C. Thomas2
  1. 1 Department of Plant and Molecular Biology, University of California–Berkeley, Berkeley, California 94720, USA;
  2. 2 College of Natural Resources, University of California–Berkeley, Berkeley, California 94720, USA

Abstract

Controversy surrounds the apparent rising maximums of morphological complexity during eukaryotic evolution, with organisms increasing the number and nestedness of developmental areas as evidenced by morphological elaborations reflecting area boundaries. No “predictable drive” to increase this sort of complexity has been reported. Recent genetic data and theory in the general area of gene dosage effects has engendered a robust “gene balance hypothesis,” with a theoretical base that makes specific predictions as to gene content changes following different types of gene duplication. Genomic data from both chordate and angiosperm genomes fit these predictions: Each type of duplication provides a one-way injection of a biased set of genes into the gene pool. Tetraploidies and balanced segments inject bias for those genes whose products are the subunits of the most complex biological machines or cascades, like transcription factors (TFs) and proteasome core proteins. Most duplicate genes are removed after tetraploidy. Genic balance is maintained by not removing those genes that are dose-sensitive, which tends to leave duplicate “functional modules” as the indirect products (spandrels) of purifying selection. Functional modules are the likely precursors of coadapted gene complexes, a unit of natural selection. The result is a predictable drive mechanism where “drive” is used rigorously, as in “meiotic drive.” Rising morphological gain is expected given a supply of duplicate functional modules. All flowering plants have survived at least three large-scale duplications/diploidizations over the last 300 million years (Myr). An equivalent period of tetraploidy and body plan evolution may have ended for animals 500 million years ago (Mya). We argue that “balanced gene drive” is a sufficient explanation for the trend that the maximums of morphological complexity have gone up, and not down, in both plant and animal eukaryotic lineages.

Footnotes

  • 3 Corresponding author.

    3 E-mail freeling{at}nature.berkeley.edu; fax (510) 642-4995.

  • Article is online at http://www.genome.org/cgi/doi/10.1101/gr.3681406

  • 4 Autopolyploidy, where one chromosomal set doubles, is the easiest sort of tetraploid to model because the new tetraploid is assumed to be the sum of its genomes. Allotetraploidy, where two different genomes combine, adds complications to these predictions, complications that probably reflect reality. Selection for polyploidy in the first place, given its expected lowered fitness due to mis-segregations, is easier to explain if the parents are of different genotypes, and the special characteristics of the tetraploid increase fitness. Recent studies on synthetic allopolyploids in plants show that gene silencing is common, and “subfunctionalized” silencing occurs; in general, the parental genotypes are not equally expressed (Adams and Wendel 2005). Evidence for rapid intrachromosomal genome changes following allopolyploidy, and ideas about mechanisms that may be involved, have been reviewed (Osborn et al. 2003). Genes from one of the two parents in an allotetraploid might be preferentially coadapted. As has and will be further documented, coexpressed genes tend to be positioned together in chromosomes. Such clusters might be coregulated at the chromatin level, and might tend to stay together during tetraploid fractionation. Even though chromosome-level regulation, such as incomplete or organ-specific silencing, could buffer gene dosage in allotetraploids, the gene dosage hypothesis accurately predicts changes in gene content following tetraploidy.

  • 5 Subfunctionalization (Force et al. 1999) was originally put forth specifically as a mechanism to explain over-retention of duplicates following tetraploidy, and has generated much theory (Lynch and Force 2000; Prince and Pickett 2002; Lynch and Conery 2003; Force et al. 2005). It is a neutral process where different, dispensable cis-functional parts of a gene are compensatorily lost such that both duplicates are required to specify the original function. Subfunctionalization is a two-hit mutational mechanism that locks in pairs only after the tetraploid evolves. Alternatively, the Gene Balance Hypothesis predicts that pairs will be preserved—by resisting purifying selection, a zero-hit mechanism—because particular multi-subunit machines or cascades cannot end up in a haploinsufficient state, and, as we have shown, predicts correctly the GO-term content of retained genes. Therefore, subfunctionalization is probably not a primary mechanism for pair retention, although it certainly occurs once a pair is retained.

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