Gibbon genome and the fast karyotype evolution of small apes

All contents refer to the original paper (Carbone et al. Nature. 2014 Sep 11;513(7517):195-201)

Summary and personal comments

This paper concerns a study of gibbon karyotype in the perspective of their divergent evolution from ancestral primates. Gibbons, small monkeys living in South-East Asia, differ from other primates, such as great apes and Old World monkeys, for a surprising number of chromosomal rearrangements. The authors aimed to study the mechanisms underlying such an important plasticity in gibbon genome gibbon.

1) The authors sequenced and assembled the genome of a white-cheeked gibbon female (Nomascus leucogenys), ordered in 26 chromosomes (against human reference), and analyzed gibbon-human synteny breakpoints (= rupture of synteny=physical co-localization of genetic loci on the same chromosome within gibbon and human).

Fig 2a shows Oxford plots for human (axys y) versus other primates chromosomes (axys x), expressed in terms of collinear blocks of > 10 Mb. It is evident from the graphic that, when compared to other primates, gibbons present the highest rate of chromosome rearrangements, graphically visualized as a scattered instead of a linear plot (Fig2a), in particular large-scale reshuffling (as shown in Fig 2b, right part of the graphic). Examples of synteny breakpoints, such as chromosomal inversion, are shown in Fig 2c.

2) The authors analyzed various transposable elements of different primates and found that one retrotransposon, the LAVA element, is exclusive to gibbon genome. Intragenic LAVA insertions are observed particularly in genes that are important for cell division and chromosome segregation, as shown in Table 1 of the Extended Data. Authors hypothesized that antisense insertions of LAVA elements into introns could determine an early transcription termination by polyadenilation. They provided evidence supporting their hypothesis through a gene construct involving a luciferase: LAVA insertions into luciferase gene determined an early termination of luciferase transcription, as suggested by lower enzymatic activity (Fig 3 b right).

4) Moreover, authors explored LAVA families across 4 gibbon genera in order to study gibbon lineage evolution. They identified 22 LAVA subfamilies and used a maximum likelihood method to estimate LAVA age and to locate the divergence of gibbons from great apes at 16.8 Myr ago. Furthermore, they performed a WGS of the genome of 4 gibbon genera (from 2 individuals per genera) and constructed the most probable gene trees through a UPGMA method (unweighted pair group method with arithmetic mean) from a coalescent-based analysis (ABC), as shown in Fig 4a. Fig 5 from Extended Data shows the 15 top UPGMA trees for 100 kb non-overlapping sliding windows of gibbon genome. Interestingly, the most probable bifurcating species topology suggest a strikingly rapid speciation process for all 4 gibbon genera, with a beginning of speciation placed at 5 Myr ago (Fig 4b).

5) Finally, in order to investigate the features of such an adaptive evolution, authors analyzed genomic regions which could have undergone lineage-specific modifications. They identified 240 regions with gibbon-specific accelerated substitution rates (gibARs) that were not only intragenic but also co-localized with LAVA elements. They also identified genes (TBX5, COL1A1, CHRNA1, SNX19) that might have been undergone a positive selection related to gibbon-specific traits, such as longer arms or stronger shoulder/elbow muscles compared to humans.

This paper underlines important characteristics of gibbon genomes and provides novel insights into genome plasticity mechanisms of those small apes. Nevertheless, it remains largely unclear under which circumstances gibbons had undergone such an accelerated evolution and how speciation and fixation of specific traits could have been produced so rapidly.

Carbone, L., Alan Harris, R., Gnerre, S., Veeramah, K., Lorente-Galdos, B., Huddleston, J., Meyer, T., Herrero, J., Roos, C., Aken, B., Anaclerio, F., Archidiacono, N., Baker, C., Barrell, D., Batzer, M., Beal, K., Blancher, A., Bohrson, C., Brameier, M., Campbell, M., Capozzi, O., Casola, C., Chiatante, G., Cree, A., Damert, A., de Jong, P., Dumas, L., Fernandez-Callejo, M., Flicek, P., Fuchs, N., Gut, I., Gut, M., Hahn, M., Hernandez-Rodriguez, J., Hillier, L., Hubley, R., Ianc, B., Izsvák, Z., Jablonski, N., Johnstone, L., Karimpour-Fard, A., Konkel, M., Kostka, D., Lazar, N., Lee, S., Lewis, L., Liu, Y., Locke, D., Mallick, S., Mendez, F., Muffato, M., Nazareth, L., Nevonen, K., O’Bleness, M., Ochis, C., Odom, D., Pollard, K., Quilez, J., Reich, D., Rocchi, M., Schumann, G., Searle, S., Sikela, J., Skollar, G., Smit, A., Sonmez, K., Hallers, B., Terhune, E., Thomas, G., Ullmer, B., Ventura, M., Walker, J., Wall, J., Walter, L., Ward, M., Wheelan, S., Whelan, C., White, S., Wilhelm, L., Woerner, A., Yandell, M., Zhu, B., Hammer, M., Marques-Bonet, T., Eichler, E., Fulton, L., Fronick, C., Muzny, D., Warren, W., Worley, K., Rogers, J., Wilson, R., & Gibbs, R. (2014). Gibbon genome and the fast karyotype evolution of small apes Nature, 513 (7517), 195-201 DOI: 10.1038/nature13679

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