Rapid emergence of independent \u201cchromosomal lineages\u201d in silvered-leaf monkey triggered by Y/autosome translocation

Oronzo Capozzi,Oronzo Capozzi,Nicoletta Archidiacono,Nicoletta Archidiacono,Svetlana A Romanenko,Svetlana A Romanenko,Svetlana A Romanenko,Roscoe Stanyon,Takafumi Ishida,Mariano Rocchi,Mariano Rocchi

doi:10.1038/s41598-018-21509-4

Abstract

Sex/autosome translocations are rare events. The only known example in catarrhines is in the silvered-leaf monkey. Here the Y chromosome was reciprocally translocated with chromosome 1. The rearrangement produced an X1X2Y1Y2 sex chromosome system. At least three chromosomal variants of the intact chromosome 1 are known to exist. We characterized in high resolution the translocation products (Y1 and Y2) and the polymorphic forms of the intact chromosome 1 with a panel of more than 150 human BAC clones. We showed that the translocation products were extremely rearranged, in contrast to the high level of marker order conservation of the other silvered-leaf monkey chromosomes. Surprisingly, each translocation product appeared to form independent “chromosome lineages”; each having a myriad of distinct rearrangements. We reconstructed the evolutionary history of the translocation products by comparing the homologous chromosomes of two other colobine species: the African mantled guereza and the Indian langur. The results showed a massive reuse of breakpoints: only 12, out of the 40 breaks occurred in domains never reused in other rearrangements, while, strikingly, some domains were used up to four times. Such frequent breakpoint reuse if proved to be a general phenomenon has profound implications for mechanisms of chromosome evolution.

Highlights

In catarrhine primates (Old World monkeys, apes and humans) only one species is known to have a sex/autosome translocation
TCR chromosome 1 (TCR1) and the t(1;Y) reciprocally translocated chromosomes Y1 and Y2 were investigated by FISH using a panel of up to 70 human end-sequenced BAC clones evenly distributed along human chromosomes 5 and Y, chosen from the UCSC BAC track, hg[19] release, to which all the present sequence data are referred
The FISH experiments showed that the two TCR1 homologs of the female differed

Summary

Introduction

In catarrhine primates (Old World monkeys, apes and humans) only one species is known to have a sex/autosome translocation. This very rare exception involves chromosome Y and chromosome 1 in the silvered-leaf monkey, Trachypithecus cristatus (TCR, formerly Presbytis cristatus), a Southeast Asian colobine monkey. Bigoni et al.[6] investigated this translocation using molecular cytogenetics techniques They mapped the homology between all human chromosomes and those of the silvered-leaf monkey with chromosome paints and showed that the Y chromosome was reciprocally translocated with TCR chromosome 1 (TCR1; entirely homologous to human chromosome 5, HSA5). In 28 out of the 40 breakpoints, one or both margins were reused up to four times in other rearrangements

Methods

Results

Conclusion