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

Abstract

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.

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

“…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.…”

The Heterochromatin Block That Functions as a Rod Cell Microlens in Owl Monkeys Formed within a 15-Myr Time Span

“…The three megasatellite DNAs consisted of repeat units of 185, 344, and 187 bp, and were named OwlAlp1, OwlAlp2, and OwlRep, respectively. Of these, OwlRep was unique to owl monkeys; satellite DNA similar in nucleotide sequence to OwlRep was not found in the other New World monkeys or more distantly related primates that we examined ( Koga et al 2017 ; Nishihara et al 2018 ). Using the three megasatellite DNAs as probes for different colors, we conducted a three-dimensional fluorescent in situ hybridization (3D-FISH) analysis of rod cells from A. azarae ( Koga et al 2017 ).…”

Replacement of owl monkey centromere satellite by a newly evolved variant was a recent and rapid process

“…The main DNA component of the microlens structure of owl monkeys is OwlRep, which is another megasatellite DNA that coexists with OwlAlp1 and OwlAlp2 in the owl monkey genome (Koga et al, 2017). The acquisition of the microlens structure was a complicated process involving these three megasatellite DNAs (Nishihara et al, 2018). OwlAlp2 can be thought to have originally been centromeric satellite DNA.…”