During evolution from the earliest tetrapoda, newly-recruited genes are increasingly paralogues of existing genes and distribute non-randomly among the chromosomes

Abstract

Background: The present availability of full genome sequences of a broad range of animal species across the whole range of evolutionary history enables one to ask questions as to the distribution of genes across the chromosomes. Do newly recruited genes, as new clades emerge, distribute at random or at non-random locations?

Results: We extracted values for the ages of the human genes and for their current chromosome locations, from published sources. A quantitative analysis showed that the distribution of newly-added genes among and within the chromosomes appears to be increasingly non-random if one observes animals along the evolutionary series from the precursors of the tetrapoda through to the great apes, whereas the oldest genes are randomly distributed.

Conclusions: Randomization will result from chromosome evolution, but less and less time is available for this process as evolution proceeds. Much of the bunching of recently-added genes arises from new gene formation as paralogues in gene families, near the location of genes that were recruited in the preceding phylostratum. As examples we cite the KRTAP, ZNF, OR and some minor gene families. We show that bunching can also result from the evolution of the chromosomes themselves when, as for the KRTAP genes, blocks of genes that had previously been on disparate chromosomes become linked together.

Keywords: Chromosomes; Gene ages; Gene distribution; Gene evolution; Newly-recruited genes; Paralogues; Phylostratigraphy.

Fig. 1

Distribution of newly recruited genes across the autosomal human chromosomes for phylostrata 19.2 (left) and 12 (middle) and for the zebrafish chromosomes for phylostratum 12 (right). The data are presented as the ratio of the content of the genes from the respective phylostratum to the gene content of the whole chromosome (as %), divided by the median of each data set and arranged in order of increasing gene content

Fig. 2

The distribution of newly recruited genes across the autosomal chromosomes of H. sapiens, measured as MAD values (see Methods) as a function of phylostratum number. The open circles in each figure show the data for the phylostratum numbers found as the modal values for the 13 ortholog search engines studied. The red circles in A show the data taken, for every gene, from the lowest estimate among the 13 sources while the blue circles show these for the highest estimate among the 3 sources. In B, the red circles show the data obtained as the median of those obtained for those three sources that, over the entire genome gave the lowest age estimates, while the blue circles were from the three sources that similarly gave the highest overall age estimates

Fig. 3

Distribution of newly recruited genes across the autosomal human chromosomes. A: All the genes assigned to phylostrata 15 through 19 by a majority of the 13 ortholog search engines. B: Those similarly assigned to phylostrata 1 through 13. The data are presented as the ratio of the total number of the genes from the respective phylostratum grouping to the gene content of the whole chromosome (as %), and arranged in order of increasing % gene content. In part A, chromosome 19 is on the extreme right, whereas in part B it is on the extreme left

Fig. 4

Regression of the content of (A) “young” genes (those assigned to phylostrata 15 through 19 or (B) “old” genes (those assigned to phylostrata 1 through 13) against the GC content of the chromosomes. The red-encircled points in both figures depict chromosome 5 while the blue-encircled points show chromosome 19

Fig. 5

The distribution of newly recruited genes across the autosomal chromosomes, measured as MAD values – see Methods - as a function of phylostratum number, for eight animal species. The horizontal lines drawn are the median, and the 25% and the 75% limits, computed for all the data through to phylostratum 12, the euteleostomii (the jawed fish)

Fig. 6

Heat maps of the distribution across the 20 sections (the columns) of human chromosome 19 of all its genes (upper figure) and of only its Zinc Finger (ZNF) genes (lower figure), the rows of the map being data for each numbered phylostratum in the 20 sections. For the full genome, the numbers are the percentage of all the genes of the phylostratum denoted, while for the ZNF data the denominator is the number of ZNF genes in the denoted phylostratum

Fig. 7

(A) The Zinc Finger (ZNF) genes of the human genome as a function of phylostratum age (left) or as their chromosome location (right); (B) similarly for the Keratin-Associated Protein (KRTAP) genes; (C) similarly again for the Olfactory Receptor (OR) genes