Phylogenomics of species from four genera of New World monkeys by flow sorting and reciprocal chromosome painting

Abstract

Background: The taxonomic and phylogenetic relationships of New World monkeys (Platyrrhini) are difficult to distinguish on the basis of morphology and because diagnostic fossils are rare. Recently, molecular data have led to a radical revision of the traditional taxonomy and phylogeny of these primates. Here we examine new hypotheses of platyrrhine evolutionary relationships by reciprocal chromosome painting after chromosome flow sorting of species belonging to four genera of platyrrhines included in the Cebidae family: Callithrix argentata (silvered-marmoset), Cebuella pygmaea (pygmy marmoset), Callimico goeldii (Goeldi's marmoset) and Saimiri sciureus (squirrel monkey). This is the first report of reciprocal painting in marmosets.

Results: The paints made from chromosome flow sorting of the four platyrrhine monkeys provided from 42 to 45 hybridization signals on human metaphases. The reciprocal painting of monkey probes on human chromosomes revealed that 21 breakpoints are common to all four studied species. There are only three additional breakpoints. A breakpoint on human chromosome 13 was found in Callithrix argentata, Cebuella pygmaea and Callimico goeldii, but not in Saimiri sciureus. There are two additional breakpoints on human chromosome 5: one is specific to squirrel monkeys, and the other to Goeldi's marmoset.

Conclusion: The reciprocal painting results support the molecular genomic assemblage of Cebidae. We demonstrated that the five chromosome associations previously hypothesized to phylogenetically link tamarins and marmosets are homologous and represent derived chromosome rearrangements. Four of these derived homologous associations tightly nest Callimico goeldii with marmosets. One derived association 2/15 may place squirrel monkeys within the Cebidae assemblage. An apparently common breakpoint on chromosome 5q33 found in both Saimiri and Aotus nancymae could be evidence of a phylogenetic link between these species. Comparison with previous reports shows that many syntenic associations found in platyrrhines have the same breakpoints and are homologous, derived rearrangements showing that the New World monkeys are a closely related group of species. Our data support the hypothesis that the ancestral karyotype of the Platyrrhini has a diploid number of 2n = 54 and is almost identical to that found today in capuchin monkeys; congruent with a basal position of the Cebidae among platyrrhine families.

Figure 1

Four phylogenies for New World monkey genera. a) modified from Rosenberger et al 1984 [72] and b) modified from Ford 1986 [73] are based on morphological traits, while c) modified from Schneider et al., 2001 [40] and d) modified from Ray et al., 2005 [39] are based on molecular studies. See text for further details.

Figure 2

Geographic distribution of four species of Cebidae. Geographic distribution of the four species studied by flow sorting and reciprocal chromosome painting: Callithrix argentata in violet, Cebuella pygmaea in red, Callimico goeldii in green and Saimiri sciureus in yellow.

Figure 3

G-banded karyotype of four species of Cebidae. a) Callithrix argentata, b) Cebuella pygmaea, c) Callimico goeldii and d) Saimiri sciureus. The X-chromosome of Saimiri sciureus differs by a pericentric inversion or centromere shift.

Figure 4

Flow karyotypes of four species of Cebidae: a) Callithrix argentata, b) Cebuella pygmaea, c) Callimico goeldii and d) Saimiri sciureus.

Figure 5

Hybridization of Cebidae probes on human metaphases. Hybridization examples of Cebidae probes on a human metaphase: a) CAR 12 paints segments of HSA 2 and 15, b) CAR 15 paints segments of HSA 3, c) CAR 18 paints a segment of HSA 1q, d) CPY 4 paints HSA 17, 20 and a segment of HSA 13, e) CPY 8 paints HSA 8p and 18, f) CPY 10 paints HSA 1p and 10p, g) CGO 15 paints segments of HSA 9 and all of 22, h) CGO 17 paints a segment of HSA 13 and all of 17, i) CGO 22 paints a small segment of HSA 3 and all of 21, j) SSC 7 paints HSA 2q and segments of 15, k) SSC 14 paints a segment of HSA 1q and most of 19, l) SSC 15 paints HSA 8p and 18.

Figure 6

Human idiogram with hybridization assignments of Cebidae paints. Human chromosomes are numbered below: a) Callithrix argentata chromosomes numbered to the left and to the right, Cebuella pygmaea chromosomes; b) Callimico goeldii chromosomes numbered to the left and to the right, Saimiri sciureus chromosomes.

Figure 7

Human idiogram with all reciprocal chromosome painting data. Human idiogram with all reciprocal chromosome painting data integrating results from this report and the literature [50, 52, 54] Breakpoints common to all platyrrhine species and hypothesized to be present in the APLK (ancestral platyrrhine karyotypes) are shown as a black line across human chromosome. Breakpoints found in other groups of species or single species are color coded. CPY = Cebuella pygmaea, CAR = Callithrix argentata, CJA = Callithrix jacchus, CGO = Callimico goeldii, SSC = Saimiri sciureus, ANA = Aotus nancymae, CPA = Callicebus pallescens, LLA = Lagothrix lagotricha.