Co-Opted Megasatellite DNA Drives Evolution of Secondary Night Vision in Azara's Owl Monkey

Koga, Akihiko; Tanabe, Hideyuki; Hirai, Yohei; Imai, Hiroo; Imamura, Makoto; Oishi, Takao; Stanyon, Roscoe; Hirai, Hirohisa

doi:10.1093/gbe/evx142

Cited by 13 publications

(22 citation statements)

References 30 publications

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“…In mice, constitutive heterochromatin, which can be marked by major satellite repeats (MSRs), localizes to the central region of the nucleus in rod cells (Solovei et al, 2009). The rod cells of owl monkeys, the only genus of nocturnal/cathemeral simian primates, show a spherical heterochromatin block in the central region of the nucleus, and a primary component of the heterochromatin region is the OwlRep, a megasatellite DNA that has expanded specifically in the owl monkey lineage (Koga et al, 2017;Nishihara et al, 2018). Thus, because megasatellites as a whole can be a major component of heterochromatin, lineage-specific expansion of satellite repeats might have had an impact on the nuclear architecture associated with nocturnal adaptation in this lineage.…”

Section: Repetitive Sequences and Nuclear Architecturementioning

confidence: 99%

Transposable elements as genetic accelerators of evolution: contribution to genome size, gene regulatory network rewiring and morphological innovation

Nishihara

2019

Genes Genet. Syst.

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In the current era, as a growing number of genome sequence assemblies have been reported in animals, an in-depth analysis of transposable elements (TEs) is one of the most fundamental and essential studies for evolutionary genomics. Although TEs have, in general, been regarded as non-functional junk/selfish DNA, parasitic elements or harmful mutagens, studies have revealed that TEs have had a substantial and sometimes beneficial impact on host genomes in several ways. First, TEs are themselves diverse and thus provide lineage-specific characteristics to the genomes. Second, because TEs constitute a substantial fraction of animal genomes, they are a major contributing factor to evolutionary changes in genome size and composition. Third, host organisms have co-opted many repetitive sequences as genes, cis-regulatory elements and chromatin domain boundaries, which alter gene regulatory networks and in addition are partly involved in morphological evolution, as has been well documented in mammals. Here, I review the impact of TEs on various aspects of the genome, such as genome size and diversity in animals, as well as the evolution of gene networks and genome architecture in mammals. Given that a number of TE families probably remain to be discovered in many non-model organisms, unknown TEs may have contributed to gene networks in a much wider variety of animals than considered previously.

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Section: Repetitive Sequences and Nuclear Architecturementioning

confidence: 99%

Transposable elements as genetic accelerators of evolution: contribution to genome size, gene regulatory network rewiring and morphological innovation

Nishihara

2019

Genes Genet. Syst.

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“…Each of these species has a unique lifestyle, eye morphology, and visually mediated behavior that make some aspects of their visual system unique from other primates, including humans. For instance, owl monkeys are nocturnal (Fleagle, ), and therefore have secondarily acquired retinal specializations associated with nocturnal vision (Koga et al, ). These include an increase in eye size, changes in the cellular composition of the retina (Dyer et al, ), and the loss of S cones necessary for color vision (Jacobs, ).…”

Section: Introductionmentioning

confidence: 99%

Architectonic characteristics of the visual thalamus and superior colliculus in titi monkeys

Baldwin

Krubitzer

2018

J of Comparative Neurology

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Titi monkeys are arboreal, diurnal New World monkeys whose ancestors were the first surviving branch of the New World radiation. In the current study, we use cytoarchitectonic and immunohistochemical characteristics to compare titi monkey subcortical structures associated with visual processing with those of other well-studied primates. Our goal was to appreciate features that are similar across all New World monkeys, and primates in general, versus those features that are unique to titi monkeys and other primate taxa. We examined tissue stained for Nissl substance, cytochrome oxidase (CO), acetylcholinesterase (AChE), calbindin (Cb), parvalbumin (Pv), and vesicular glutamate transporter 2 (VGLUT2) to characterize the superior colliculus, lateral geniculate nucleus, and visual pulvinar. This is the first study to characterize VGLUT2 in multiple subcortical structures of any New World monkey. Our results from tissue processed for VGLUT2, in combination with other histological stains, revealed distinct features of subcortical structures that are similar to other primates, but also some features that are slightly modified compared to other New World monkeys and other primates. These included subdivisions of the inferior pulvinar, sublamina within the stratum griseum superficiale (SGS) of the superior colliculus, and specific koniocellular layers within the lateral geniculate nucleus. Compared to other New World primates, many features of the subcortical structures that we examined in titi monkeys were most similar to those in owl monkeys and marmosets, with the lateral geniculate nucleus consisting of two main parvocellular layers and two magnocellular layers separated by interlaminar zones or koniocellular layers.

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“…OwlRep is a megasatellite DNA that was first identified in A. azarae ( Prakhongcheep, Chaiprasertsri, et al 2013 ). Its presence in the genome of A. lemurinus was revealed by chromosome FISH (fluorescence in situ hybridization) analysis ( Koga et al. 2017 ).…”

Section: Discussionmentioning

confidence: 99%

“…Transfer of this repetitive sequence to other chromosomes may have been mediated by the generation and migration of extrachromosomal circular DNA. This amplification to form the megasatellite DNA corresponds to step (5), and it is likely that the amplification was favored by natural selection because we know that the abundance of OwlRep is directly associated with adaptation to a nocturnal lifestyle ( Koga et al. 2017 ).…”

Section: Discussionmentioning

confidence: 99%

“…Thus, owl monkeys are a unique taxon for understanding adaptation to night vision because we know of no other species which has acquired nocturnality in as short a time span as the last 20 Myr. We have recently shown that the primary DNA component of the central heterochromatin block found in owl monkey rod cells is OwlRep, which is a satellite DNA present in large amounts in the owl monkey genome ( Koga et al. 2017 ).…”

Section: Introductionmentioning

confidence: 99%

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Evolutionary Origin of OwlRep, a Megasatellite DNA Associated with Adaptation of Owl Monkeys to Nocturnal Lifestyle

Nishihara

Stanyon

Kusumi

et al. 2017

Genome Biology and Evolution

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Rod cells of many nocturnal mammals have a “non-standard” nuclear architecture, which is called the inverted nuclear architecture. Heterochromatin localizes to the central region of the nucleus. This leads to an efficient light transmission to the outer segments of photoreceptors. Rod cells of diurnal mammals have the conventional nuclear architecture. Owl monkeys (genus Aotus) are the only taxon of simian primates that has a nocturnal or cathemeral lifestyle, and this adaptation is widely thought to be secondary. Their rod cells were shown to exhibit an intermediate chromatin distribution: a spherical heterochromatin block was found in the central region of the nucleus although it was less complete than that of typical nocturnal mammals. We recently demonstrated that the primary DNA component of this heterochromatin block was OwlRep, a megasatellite DNA consisting of 187-bp-long repeat units. However, the origin of OwlRep was not known. Here we show that OwlRep was derived from HSAT6, a simple repeat sequence found in the centromere regions of human chromosomes. HSAT6 occurs widely in primates, suggesting that it was already present in the last common ancestor of extant primates. Notably, Strepsirrhini and Tarsiformes apparently carry a single HSAT6 copy, whereas many species of Simiiformes contain multiple copies. Comparison of nucleotide sequences of these copies revealed the entire process of the OwlRep formation. HSAT6, with or without flanking sequences, was segmentally duplicated in New World monkeys. Then, in the owl monkey linage after its divergence from other New World monkeys, a copy of HSAT6 was tandemly amplified, eventually forming a megasatellite DNA.

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Co-Opted Megasatellite DNA Drives Evolution of Secondary Night Vision in Azara's Owl Monkey

Cited by 13 publications

References 30 publications

Transposable elements as genetic accelerators of evolution: contribution to genome size, gene regulatory network rewiring and morphological innovation

Transposable elements as genetic accelerators of evolution: contribution to genome size, gene regulatory network rewiring and morphological innovation

Architectonic characteristics of the visual thalamus and superior colliculus in titi monkeys

Evolutionary Origin of OwlRep, a Megasatellite DNA Associated with Adaptation of Owl Monkeys to Nocturnal Lifestyle

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