The first gibbon genome to be sequenced provides clues about how genomes can be shuffled in short evolutionary time frames, and about how gibbons adapted and diversified in the jungles of southeast Asia. See Article p.195
The gibbon — a singing, swinging, southeast-Asian ape of the Hylobatidae family — occupies a poorly understood branch of the primate family tree. Despite being superficially similar to monkeys, gibbons share many traits with humans: pair bonding and monogamy; the lack of a tail; the ability to walk upright on legs; and a fondness for singing. Our understanding of gibbon evolution is now set to improve because they have just joined an exclusive primate club whose members include humans, chimpanzees and orangutans. On page 195 of this issue, Carbone et al.1 report that they have sequenced the genome of Asia, a white-cheeked gibbon of the Nomascus genus. Their analysis unveils unique genomic features that shed light on some of the mysteries surrounding the evolutionary history of this remarkable mammalian family.
The genomes of almost all eukaryotes (plants, fungi and animals) are organized into blocks of DNA that undergo periodic reorganization. These reshuffling events, which typically occur in small increments, can lead to the emergence of species with distinct variations in karyotype — an organism's chromosome structure and number. How reshuffling occurs, and what factors lead to the fixation of new karyotypes, is an abiding genetic mystery, but mobile DNA elements are thought to have a role in some genome rearrangements. These DNA sequences, which were discovered more than 50 years ago2, can move from one location in the genome to another, often leaving a copy of themselves behind.
By comparing Asia's genome with those of three other gibbons of the genera Hylobates, Hoolock and Symphalangus, Carbone and colleagues dated the divergence of gibbons from the great apes at roughly 17 million years ago (Fig. 1). However, they found that in a strikingly rapid series of speciation events that spanned 2 million years or less, an ancestral gibbon quickly gave rise to the four genera of extant gibbons. Coinciding with and perhaps reinforcing this rapid speciation is an unusually fluid karyotype3 — the chromosomes of different gibbon species are more structurally diverse than those of any of the great apes.
Carbone and co-workers suggest that the gibbon's extreme chromosomal diversity may be attributable to a family of mobile DNA elements that is not found in other primate lineages. These LINE-1-Alu-VNTR-Alu-like (LAVA) elements are named after the three distinct mobile elements from which they derive4. Although each of the parental elements is common to all apes, the composite is unique to the gibbon lineage, with its origin dating to the time gibbons split from the great-ape lineage.
The authors' examination of the four genomes revealed the profound impact of LAVA elements on gibbon genome dynamics. In several places, insertion of LAVA elements caused premature termination of gene transcription, which might lead to the production of proteins with altered functions. The affected genes notably include several that are involved in chromosome segregation, whereby replicated chromosomes are equally distributed to progeny during cell division. Carbone et al. propose a scenario in which LAVA insertion results in subtly altered proteins that mildly disrupt chromosome segregation and so enhance genome plasticity. However, major alterations or a loss of function of these genes would lead to sterility or death, limiting the ability of LAVA elements to generate new chromosome arrangements.
Lending credence to the subtle-alteration model, Carbone and colleagues found that the gibbon genome contained 240 short segments (most around 150 base pairs in length) in which mutations resulting in base-pair substitutions have occurred faster than expected since separation from the great-ape lineage — a hallmark of adaptive evolution. These regions mostly lie close to the genes affected by LAVA insertions. The authors speculate that the regions may have diversified specifically in gibbons to ameliorate the detrimental effects of active LAVA elements; functional elements that modulate the impact of LAVA insertions on gene transcription were created, such as enhancers (which control gene expression from a distance)4.
Such gene disruptions, coupled with population-size fluctuations across southeast Asia during the Miocene-to-Pliocene transition 2.5 million years ago, may have led to the extraordinary chromosomal diversity displayed in extant gibbons. Several other eukaryotic groups underwent rapid diversification in karyotype as they evolved5, including sunflowers, Australian grasshoppers, horses and kangaroos, and the emergence of some of these species coincided with notable activity of mobile DNA. However, proof of Carbone and colleagues' subtle-alteration model will require thorough and integrative functional and evolutionary genomic analyses — a strategy that has been of great benefit to other large-scale genomics efforts6.
Gibbons almost fly through the trees, hitting speeds of up to 56 kilometres an hour using only their arms in a pendulum motion termed brachiation7 (Fig. 2). The physiological features that allow this fluid and swift motion include long and powerful arms, permanently hooked hands, and a ball-and-socket wrist joint that enables swift changes in direction, even at high velocities. The authors found evidence that genes important to forelimb patterning and specialization in the gibbon have experienced a rapid evolution not seen in other primate lineages. Establishing a functional link between the adaptive evolution of these genes and gibbon brachiation is an exciting future direction — it could provide the first evidence that anatomical and locomotive specialization can be linked to specific changes at the genome level in primates.
Further exploration of the gibbon genome may shed light on other features we share with gibbons, such as their ability to sing like human operatic sopranos8 and their penchant for walking on two legs. Publication of Asia's genome gives us something to sing about — and to swing about.
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