Concerted and birth-and-death evolution of multigene families

Abstract

Until around 1990, most multigene families were thought to be subject to concerted evolution, in which all member genes of a family evolve as a unit in concert. However, phylogenetic analysis of MHC and other immune system genes showed a quite different evolutionary pattern, and a new model called birth-and-death evolution was proposed. In this model, new genes are created by gene duplication and some duplicate genes stay in the genome for a long time, whereas others are inactivated or deleted from the genome. Later investigations have shown that most non-rRNA genes including highly conserved histone or ubiquitin genes are subject to this type of evolution. However, the controversy over the two models is still continuing because the distinction between the two models becomes difficult when sequence differences are small. Unlike concerted evolution, the model of birth-and-death evolution can give some insights into the origins of new genetic systems or new phenotypic characters.

Figure 1

Three different models of evolution of multigene families. Open circles stand for functional genes and closed circles for pseudogenes.

Figure 2

Molecular structures of rRNA gene repeats in different organisms.

Figure 3

Genomic structures of histone gene (a) and ubiquitin gene repeats (b). The red square box in human histone gene repeats represents a pseudogene. Expressed histone genes are shown in blue, and an arrow indicates the direction of transcription when known. Each box in the poly-u gene complex represents one copy of ubiquitin gene. Poly-uΨ shows a poly-u pseudogene. A monomeric ubiquitin locus is composed of a ubiquitin gene and a ribosomal protein gene with 52 codons (Mono52) or 80 codons (Mono80).

Figure 4

(a) Phylogenetic tree of MHC class I genes from vertebrates. (b) Phylogenetic tree of heat shock protein genes (hsp70) from two species of nematodes, Drosophila melanogaster, and yeast. CYT, ER, and MT stand for the genes expressed in cytoplasm, endoplasmic reticulum, and mitochondria, respectively. The * sign indicates a highly heat-inducible gene. Modified from Nei et al. (96) and Nikolaidis & Nei (109).

Figure 5

Orthologous relationships of class II OR genes between mouse (Mm) and human (Hs) genomic clusters. OR gene genomic clusters are indicated by chromosome number and Giemsa-stained band number in each species. Only a few chromosomes are presented. Long and short vertical bars show the locations of functional and nonfunctional OR genes, respectively. A vertical bar above a horizontal line indicates the transcriptional direction opposite to that below a horizontal line. Different colors represent different phylogenetic clades. Red and blue lines connecting mouse and human OR genes represent orthologous gene pairs. A red line indicates that transcriptional directions of orthologous genes are conserved between mice and humans, whereas a blue line indicates that they are inverted. Alphabetical letters such as A, J, G, and AQ represent different phylogenetic clades. Arrows show the location of the β-globin gene cluster (βGL). From Niimura & Nei (103).

Figure 6

Evolutionary changes of functional OR genes. (a) The most recent common ancestor (MRCA) between humans and mice had approximately 754 functional OR genes. The number of functional OR genes increased to 1037 in the mouse lineage, whereas it declined to 388 in the human lineage. (b) The MRCA between jawed and jawless fishes had at least two functional genes, whereas the MRCA between fishes and tetrapods had at least 9 functional OR genes. Class II genes (blue circle) expanded enormously in amphibians and mammals.