Alu elements and the phylogeny of capuchin (Cebus and Sapajus) monkeys

Abstract

Three families of New World monkeys, the Pitheciidae, Atelidae, and Cebidae, are currently recognized. The monophyly of the Cebidae is supported unequivocally by the presence of ten unique Alu elements, which are absent from the other two families. In this paper, the five genomic regions containing these Alu elements were sequenced in specimens representing nine capuchin (Cebus, Sapajus) species in order to identify mutations that may help elucidate the taxonomy and phylogenetic relationships of the cebids. The results confirmed the presence of previously described Alu elements in the capuchins. An Alu insertion present in the Cebidae2 genomic region belonging to the AluSc subfamily was amplified and sequenced only in Sapajus. No amplified or unspecific product was obtained for all other species studied here. An AluSc insertion present in the CeSa1 region was found only in Cebus, Sapajus, and Saimiri. Cebidae4 was characterized by two insertions, an AluSz6 shared by all cebids, and a complete SINE (AluSx3) found only in the capuchins (Cebus and Sapajus). The genomic region Cebidae5 revealed two insertion events, one of the AluSx subfamily, which was shared by all cebids, and another (AluSc8), that was unique to Cebus, offering a straightforward criterion for the differentiation of the two genera, Cebus and Sapajus. The Cebidae6 region showed four distinct insertion events: a 52-bp simple repeat ((TATG) n), two very ancient repeats (MIRc) and a TcMar-Tigger shared by all New World monkeys studied so far, and an Alu insertion of the AluSx subfamily present exclusively in the cebids. The phylogenetic tree confirmed the division of the capuchins into two genera, Cebus and Sapajus, and suggested the southern species Sapajus nigritus robustus and S. cay as the earliest and second earliest offshoots in this genus, respectively. This supports a southern origin for the Sapajus radiation.

A phylogenomic perspective on the robust capuchin monkey (Sapajus) radiation: First evidence for extensive population admixture across South America

“…Our phylogenomic data provided strong support for Cebus and Sapajus as two reciprocally monophyletic clades. This is concordant with morphological evaluations of distinctiveness between robust and gracile capuchins (Elliott, 1913;Hershkovitz, 1949;Groves, 2001Groves, , 2005Silva-Júnior, 2001Lynch Alfaro et al, 2012b), and mitochondrial and Alu element data that also point to this split (Lynch Alfaro et al, 2012a;Lima et al, 2017;Martins Jr. et al, 2015;Viana et al, 2015). We recovered a late Miocene split for robust and gracile capuchins, concordant with previous molecular studies.…”

“…Subsequently, genetic research validated the separation of robust and gracile capuchins as two distinct and equally diverse clades using mitochondrial (Lynch Alfaro et al, 2012a;Lima et al, 2017) and a combination of mtDNA and nuclear (Perelman et al, 2011) markers. Two Alu elements provide strong evidence for the monophyly of robust versus gracile capuchins: Alu element S49P is present in Sapajus but not Cebus (Viana et al, 2015) and the AluSc8 insertion is found in Cebus but not Sapajus (Martins Jr. et al, 2015). A recent review justified the splitting of robust and gracile capuchins into two genera (Cebus for gracile capuchins and Sapajus for robust capuchins) based on the distinct morphology, biogeographic history, behavior, and ecology of each type (Lynch Alfaro et al, 2012b).…”

The Multiple Representations of Complex Digit Movements in Primary Motor Cortex Form the Building Blocks for Complex Grip Types in Capuchin Monkeys

“…formerly Cebus spp.) (Martins et al, 2015) of both sexes (3 males and 1 female) weighing between 1.9 and 4.6 kg. Movements evoked by LT-ICMS were digitally recorded from two separate angles (Sanyo Xacti VPC-HD2000A, 1920 ϫ 1080 resolution, 60 frames/s) and analyzed offline (see Movement analysis).…”

In search of a meaningful classification for Amazonian marmosets: Should dwarf marmosets be consideredMicocongenerics?

“…; Martins et al. ; Robinson et al., ; Young & Heard‐Booth, ; Fedigan, ). The divergence time between the Sapajus and Cebus clades was estimated at 6.2 Ma (Lynch‐Alfaro, Boubli, et al., ) and the widespread sympatry was explained by a rapid diversification during the Pliocene followed by expansion and invasion by the Atlantic Forest Sapajus of the Amazon basin, where currently species of the two genera occur in sympatry (Lynch‐Alfaro, Boubli, et al., ).…”

“…These morphological and ecological differences in robust and gracile capuchins monkeys (Lynch-Alfaro, Silva, et al, 2012) agree with the biogeographical analyses presented in Lynch-Alfaro, Boubli, et al (2012) to advocate placing species of these two groups into the genera Sapajus and Cebus, respectively. This taxonomic classification was largely adopted thereafter (Bezerra et al 2014;Martins et al 2015;Robinson et al, 2016;Young & Heard-Booth, 2016;Fedigan, 2017). The divergence time between the Sapajus and Cebus clades was estimated at 6.2 Ma (Lynch-Alfaro, Boubli, et al, 2012) and the widespread sympatry was explained by a rapid diversification during the Pliocene followed by expansion and invasion by the Atlantic Forest Sapajus of the Amazon basin, where currently species of the two genera occur in sympatry (Lynch-Alfaro, Boubli, et al, 2012).…”