Amplification Dynamics of Platy-1 Retrotransposons in the Cebidae Platyrrhine Lineage

Abstract

Platy-1 elements are Platyrrhine-specific, short interspersed elements originally discovered in the Callithrix jacchus (common marmoset) genome. To date, only the marmoset genome has been analyzed for Platy-1 repeat content. Here, we report full-length Platy-1 insertions in other New World monkey (NWM) genomes ( Saimiri boliviensis , squirrel monkey; Cebus imitator , capuchin monkey; and Aotus nancymaae , owl monkey) and analyze the amplification dynamics of lineage-specific Platy-1 insertions. A relatively small number of full-length and lineage-specific Platy-1 elements were found in the squirrel, capuchin, and owl monkey genomes compared with the marmoset genome. In addition, only a few older Platy-1 subfamilies were recovered in this study, with no Platy-1 subfamilies younger than Platy-1-6. By contrast, 62 Platy-1 subfamilies were discovered in the marmoset genome. All of the lineage-specific insertions found in the squirrel and capuchin monkeys were fixed present. However, ∼15% of the lineage-specific Platy-1 loci in Aotus were polymorphic for insertion presence/absence. In addition, two new Platy-1 subfamilies were identified in the owl monkey genome with low nucleotide divergences compared with their respective consensus sequences, suggesting minimal ongoing retrotransposition in the Aotus genus and no current activity in the Saimiri , Cebus , and Sapajus genera. These comparative analyses highlight the finding that the high number of Platy-1 elements discovered in the marmoset genome is an exception among NWM analyzed thus far, rather than the rule. Future studies are needed to expand upon our knowledge of Platy-1 amplification in other NWM genomes.

Cebidae Alu Element Alignments and a Complex Non-Human Primate Radiation

“…Rapid diversification and large ancestral population size among cebid taxa have made determining the exact phylogeny a difficult task that has required innovative methods to be applied, which have yet to give confident results. A platyrrhine specific SINE element called Platy-1 is reported to have little activity in Aotus , virtually no current mobilization in squirrel monkey and capuchins [ 26 ], while marmoset exhibits extensive expansion of Platy-1 elements [ 27 ]. This could mean that a branch including Aotus , that later led to squirrel monkey and capuchins, diverged first, followed by the Callitrichinae branch that led to marmosets and tamarins and that the Platy-1 expansion took place after this split.…”

Extensive Independent Amplification of Platy-1 Retroposons in Tamarins, Genus Saguinus

“…The scaffold level genome assembly for S. imperator [SagImp_v1] (GCA_004024885.1 _SagImp_v1_BIUU), the chromosome-level genome assembly for S. midas [ASM2_v1] (GCA_021498475.1_ASM2149847v1), and a more recent genome assembly for C. jacchus [calJac4] (GCA_009663435.2_Callithrix_jacchus_cj1700_1.1 [calJac4] were obtained from the National Center for Biotechnology Information. Each genome was subjected to Repeat-Masker [8] (RepeatMasker-Open-4.0; accessed on 14 June 2023) analysis using a custom library consisting of the 62 original Platy-1 subfamilies reported in [1], the two Aotus derived subfamilies previously reported in [5], as well as all current Alu subfamily consensus sequences obtained from RepBase [9]. This custom library is available as Supplementary File S1.…”

“…In sharp contrast, nearly all lineage-specific insertions for S. imperator (Figure 4C) and S. midas (Figure 4D) belong to the youngest subfamily, Platy-1-8c_Saguinus, with S. midas having a pronounced leftward shift to the lower percent divergence bins. Using a mutation rate of 0.006024 per base per million years (my) as described previously in [5], 2% divergence corresponds to an age estimate of 3.32 my, while 7% is ~11.62 my. However, Platy-1 elements are only ~100 bp in length, and therefore, each nucleotide corresponds to 1%, or about 1.66 my [1,5], hindering pin-point timing of the observed amplification burst.…”

“…Platy-1 elements have reportedly been nearly quiescent in the Saimiri and Cebus lineages for millions of years, whereas Platy-1 mobilization in owl monkey (Aotus) appears to have resumed with recent discernible activity leading to the discovery of two new subfamilies, Platy-1-4b_Aotus and 4b3_Aotus. However, all three genera (Saimiri, Cebus and Aotus) contain only a fraction of the number of Platy-1 elements compared to marmoset [5].…”

“…Roughly 2200 Platy-1 elements, characterized into 62 subfamilies, were ascertained from C. jacchus [calJac3] in that initial study, and their amplification dynamics ranged from a slow, mostly linear propagation during early Platy-1 evolution in all platyrrhines, to a star-like burst of younger subfamilies unique to the common marmoset [1]. As WGS became available for other platyrrhine genomes, Platy-1 elements were characterized in squirrel monkey (Saimiri boliviensis; saiBol1) (Cebidae), capuchin monkey (Cebus imitator; Cebus_imitator-1.0) (Cebidae) and owl monkey (Aotus nancymaae; Anan_1.0) (Aotidae) [5]. Platy-1 elements have reportedly been nearly quiescent in the Saimiri and Cebus lineages for millions of years, whereas Platy-1 mobilization in owl monkey (Aotus) appears to have resumed with recent discernible activity leading to the discovery of two new subfamilies, Platy-1-4b_Aotus and 4b3_Aotus.…”