Evolution of a Multiple Sex-Chromosome System by Three-Sequential Translocations among Potential Sex-Chromosomes in the Taiwanese Frog Odorrana swinhoana

Abstract

Translocation between sex-chromosomes and autosomes generates multiple sex-chromosome systems. It happens unexpectedly, and therefore, the evolutionary meaning is not clear. The current study shows a multiple sex chromosome system comprising three different chromosome pairs in a Taiwanese brown frog (Odorrana swinhoana). The male-specific three translocations created a system of six sex-chromosomes, ♂X₁Y₁X₂Y₂X₃Y₃-♀X₁X₁X₂X₂X₃X₃. It is unique in that the translocations occurred among three out of the six members of potential sex-determining chromosomes, which are known to be involved in sex-chromosome turnover in frogs, and the two out of three include orthologs of the sex-determining genes in mammals, birds and fishes. This rare case suggests sex-specific, nonrandom translocations and thus provides a new viewpoint for the evolutionary meaning of the multiple sex chromosome system.

Keywords: autosome; fusion; hexavalent; sex-chromosome turnover.

Figure 1

Somatic and meiotic chromosomes of Odorrana swinhoana. Late replication banded karyotypes in male (a) and female (b). Chromosomes 1, 3, and 7 are heteromorphic in males (indicated by arrows), whereas they are homomorphic in females. The metaphase at first meiotic division comprises one hexavalent and ten bivalent rings (c). Each of the chromosome members comprising the hexavalent is numbered in red. The presumed pathway of triangular translocations through the chromosomes 1, 3 and 7 in male (d). The translocated chromosomal parts are diagrammatically indicated in black (chromosome 1), red (chromosome 3) and yellow (chromosome 7). The three translocations are diagrammatically represented in a box at the right bottom. Telomeres are indicated by two dots. The ring with an arrowhead indicates an inversion. Bar, 10 μm.

Figure 2

Chromosome painting and diagrams showing the multiple sex-chromosomes and potential sex-chromosomes. Hybridization with probes of microdissected chromosomes 1 (green) and 3 (red) onto the 1st meiotic chromosomes and somatic chromosomes of male and female (a1–a3). Chromosome 1 probe DNA is shown in green, while chromosome 3, in red. The hybridization with hexavalent probe (red) onto the 1st meiotic chromosomes and somatic chromosomes of male and female (a4–a6). Hexavalents are boxed by the white dotted line (a1,a4). Diagrams of six sex-chromosomes in males (left) and females (right) (b): chromosomal materials of No. 1, 3 and 7 are shown in black, red and yellow, respectively. The hexavalent is diagrammatically shown in (c). Thirteen haploid complements of ranid frogs, of which six potential sex-chromosomes are colored, and their chromosome numbers are circled (upper) (d). Orthologs of three sex-determining genes that are mapped in the Japanese frog G. rugosa are shown on the left or top of chromosomes 1 and 7, respectively. The late replication banding patterns of 13 chromosome complements are perfectly conserved between Glandirana rugosa and Odorrana swinhoana, shown at the bottom.