Open access peer-reviewed chapter

Comparative Cytogenetics Allows the Reconstruction of Human Chromosome History: The Case of Human Chromosome 13

Written By

Rita Scardino, Vanessa Milioto and Francesca Dumas

Submitted: 31 May 2018 Reviewed: 08 June 2018 Published: 05 November 2018

DOI: 10.5772/intechopen.79380

From the Edited Volume

Cytogenetics - Past, Present and Further Perspectives

Edited by Marcelo Larramendy and Sonia Soloneski

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Abstract

Comparative cytogenetics permits the identification of human chromosomal homologies and rearrangements between species, allowing the reconstruction of the history of each human chromosome. The aim of this work is to review evolutionary aspects regarding human chromosome 13. Classic and molecular cytogenetics using comparative banding, chromosome painting, and bacterial artificial chromosome (BAC) mapping can help us formulate hypotheses about chromosome ancestral forms; more recently, sequence data have been integrated as well. Although it has been previously shown to be conserved when compared to the ancestral primate chromosome, it shows a degree of rearrangements in some primate taxa; furthermore, it has been hypothesised to have a complex origin in eutherian mammals which has still not been completely clarified.

Keywords

  • FISH
  • evolution
  • mammals
  • human synteny

1. Introduction

Comparative cytogenetics has been widely applied to many mammalian species [1, 2, 3] through banding methods and, later, with fluorescence in situ hybridization (FISH) of whole chromosomes and bacterial artificial chromosome (BAC) probes; these approaches permit the definition of regions of chromosomal homology, rearrangements, and breakpoints, as well as elucidate phylogenetic relationships between taxa [4]. In addition, the comparative cytogenetic approach is particularly useful in the reconstruction of human chromosome (HSA) history. Indeed, parsimony analysis of homologies and rearrangements permits us to define ancestral chromosomal syntenies (synteny is the colocalization of two or more genetic loci) and derived ones [2]. Banding allows us to first evaluate rearrangements between species; the mapping of whole chromosomes through the chromosomal painting approach allows researchers to better define rearrangements at the molecular level, such as Robertsonian ones and breakpoints. At a finer level, the use of DNA cloned inside vectors such as yeast artificial chromosomes (YACs) or BAC, used as mapping probes, permits the evaluation of chromosomal dynamics [5, 6], defining marker orders and intrachromosome rearrangements. Moreover, the use of specific loci or repetitive probes permits the localization of specific sequences, such as repetitive ones, which are often supposed to be responsible for the plasticity of chromosomes [7, 8, 9, 10] and human genes involved in cancers [11].

More recently, the integration of cytogenetic data with sequence data has been proposed [12, 13, 14, 15, 16]. These kinds of data are available from genomic browsers and are helpful for testing previously proposed phylogenomic hypotheses and chromosomal organisation reconstructions.

In this review, we report the principal approach which has proven useful for studying human chromosome history by analysing previous cytogenetic and sequence data regarding human chromosome 13.

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2. The reconstruction of human chromosome history

At least three or four principal approaches can be used to reconstruct human synteny history. In a comparative perspective, the analysis of banding data permits the identification of chromosomal homologies. In particular, the analysis of the banding patterns obtained by the enzymatic digestion of chromosomes in metaphases using proteolysis and Giemsa solution staining permits the identification of chromosomal homologies and principal rearrangements occurring between species. Consequently, by focusing attention on a single chromosome, it is possible to track the principal evolutionary steps involving each individual human chromosome [1].

Another approach is the analysis of comparative painting data; the painting approach consists of a whole chromosome undergoing FISH on cytogenetic preparations, allowing the identification of molecular level homologies, interchromosomal rearrangements and genomic breakpoints. First, human chromosome probes are mapped onto metaphases of target species (chromosome painting [CP]) [17], then, for a better comparison, animal chromosomal probes are mapped onto human metaphases in a reciprocal hybridization (RP) [18]. Subsequently, whole animal chromosomes are mapped onto other animal metaphases in an approach known as ZOO-FISH, Z-F [19]. The analysis of these data regarding a single chromosome, consequentially, permits the tracking of each change involving the human chromosome under study.

In addition, human chromosome evolution can be studied using another kind of probe, the BAC probe, containing an insert of 50–300 Kb of the human genome. It can be mapped by FISH onto the metaphases of many species. BACs are available for each human chromosome and can be purchased from the BAC/PAC Resource Center (Chori), and some of them are commercially available for medical diagnosis. These probes are very useful in detecting small interchromosomal rearrangements which are not detectable by painting and in defining marker order along chromosomes, thus revealing inversions, new centromere evolutions (new centromeres arise without the occurrence of inversions, maintaining the marker order), and duplications [3].

Comparative cytogenetics has been applied to reconstructing most human chromosome history; these published works have mainly been done by reviewing previous painting data or by mapping BAC probes on primates (see review in [2]) and other eutherian mammals; some works have analysed only specific chromosome regions (see Table 1 for representative works).

Furthermore, alignments of sequences (SA) of many mammal species, obtainable from the NCBI, UCSC, and Ensemble genome browsers, can be integrated with molecular cytogenetic information in order to shed light on the history and peculiar features characterising each human chromosome.

2.1. The evolutionary history of HSA 13

Human chromosome 13 has been sequenced, and it has been shown to be the largest acrocentric chromosome in the human karyotype. Currently, the NCBI reports 1381 total genes, 41 novel genes, and 477 pseudogenes for a size of 114.36 MB [47]. It is among the human chromosomes with the lowest percentage of duplicated sequences [48].

The analyses of classical and molecular cytogenetics, using comparative banding and chromosome painting, have allowed researchers to formulate hypotheses about its ancestral forms. In this report, we delineate the principal steps regarding the history of human chromosome 13, tracked through the analysis of previous cytogenetics literature and sequence data. We have reported a list of species analysed by painting or sequence information, chromosome homologues to human chromosome 13, human associations with HSA 13, chromosome type if available, references and methods from which we obtained the data, such as CP, RP, Z-F, and SA (see Table 2). The principal steps in the evolution of human chromosome 13 are illustrated in a graphical reconstruction of the mammal phylogenetic tree, Figure 1; the mammal phylogenetic tree has been drawn in agreement with previous ones [16, 49], with some modifications, and was created using Mesquite v.2.75 [50]. Among mammals, three major groups are distinguishable: monotremes (Prototheria, platypus), marsupials (Metatheria, opossum), and placental mammals (eutherian), with these last two known as Theria; among placental mammals, Afrotheria, Xenarthra, and Boroautherian are recognized, with the latter comprising Laurasiatheria and Euarchontoglires (or Supraprimates) [49]. In the mammalian phylogenetic tree are shown the orthologue blocks that correspond to human chromosome 13—in yellow—in representative eutherian species for which reciprocal chromosome painting is available; for some of them also DNA sequence alignments have been previously showed, see Table 2 for reference. For each species are reported chromosome ideograms on which human synteny 13 is found, and on the left of the ideograms are reported the species’ chromosome number and on the right HSA syntenies; the black circle is the centromere. Syntenies homologues of human chromosome 13 in platypus (Monotremata) are on chromosomes 2, 10, and 20, in opossum (Metatheria) are on chromosomes 4 and 7, and in chicken (Aves) are on chromosome 1. These chromosomes are reported in box because they are representative eutherian mammal outgroups and data come just from sequence alignments. When HSA 13 synteny, in yellow, is rearranged with just few human syntenies, these are represented in different colours and are reported on the right of the ideogram (e.g., in Indri chromosome 3, synteny 13 is fused with synteny 17 in red), whereas when HSA 13, in yellow, is rearranged with many human syntenies, these are represented by white segments for logistic issue (e.g., on chicken chromosome 1). Through painting and sequence analysis in mammals, human chromosome 13 has been previously shown to be conserved, with some exceptions (Table 2, Figure 1). Indeed, the homologues to human chromosome 13 are found as single conserved chromosomes in most representative mammalian orders analysed by chromosome painting, for example in Dermoptera, Pilosa, Carnivori (cat—Felis silvestris catus ch A1), Lagomorpha (rabbit—Oryctolagus cuniculus ch 8), Perissodactyla (horse—Equus caballus ch 17), and Cetartiodactyla (cattle—Bos tauros ch 12 and pig—Sus scrofa ch 11; in pig, the synteny is metacentric due to a new centromere formation). Human synteny 13 has gone to many rearrangements such as translocation and fission in other different groups; indeed, it is associated with one or more human syntenies due to translocation, as in Tubulidentata, Afrosoricida, Eulipotyphla, Macroscelidea, Sirenia, Pholidota, Chiroptera (Table 2). For example, among Chiroptera in Greater mouse-eared bat, on Myotis myotis ch 5/6 is present human synteny 13 associated with many other human syntenies (8 lightgreen/4 bordoux/13 yellow/12 green/22 darkgreen) and among Rodentia in eastern grey squirrel, Sciurus carolinensis ch 6, human synteny 13 in yellow is associated with other human syntenies (reported in white in Figure 1). Furthermore, human synteny 13 is fragmented into two segments or into many segments and associated with other HSA syntenies, for example in Carnivori (Canis—Canis lupus familiaris ch 22, 28), in Proboscidea (elephant—Loxodonta Africana ch 16, 26), and in Rodentia species such as birch mouse (Sicista betulina ch 1, 9; in these last species, many other human syntenic associations are reported in white segments for logistic concern in Figure 1).

HSA chr.MethodsReferences
1Region study by BAC mapping
History by multidisciplinary approach
History by BAC mapping
[20]
[21]
[2]
2Region study by BAC mapping
History by BAC mapping
[22]
[2]
3Region study by BAC mapping
Review
[23, 24, 25]
[26]
4Region study by BAC mapping
History by BAC mapping
Region study by BAC mapping
[27]
[2]
[28, 29]
5Region study by BAC mapping
review
[30, 31]
[2]
6History by BAC mapping[32, 33]
7Painting
Review
Region study by BAC mapping
[34]
[35]
[36]
8Brief history by BAC mapping[2]
9Region study by BAC mapping[37]
10History by BAC mapping[37, 38]
11History by BAC mapping[39]
12Brief history by BAC mapping[2]
13History by BAC mapping[40]
14Region study by BAC mapping[41]
15Region study by BAC mapping[41, 42]
16History by BAC mapping,
Painting
[43]
[34]
17History by BAC mapping[2]
18Region study by BAC mapping,
History by BAC mapping
[44]
[2]
19Painting,
Brief history by BAC mapping
[34]
[2]
20History by BAC mapping[45]
21Region study by BAC mapping
Brief history by BAC mapping
[23]
[2]
22Brief history by BAC mapping[2]
XBrief history by BAC mapping[2]
yRegion study by BAC mapping[46]

Table 1.

List of representative works, (references and methods) analyzing each human chromosome evolution and/or marker order in particular chromosomal region.

Chromosome typeChr.Human associationReferencesMethods
Dermoptera
Galeopterus variegatusAcrocentric13[58]RP
Proboscidea
Loxodonta africanaAcrocentric
Submetacentric
16,2613, 6/13/3[59]
[12, 16]
CP
SA
Elephas maximusAcrocentric
Submetacentric
16, 2613, 6/13/3[59]CP
Tubulidentata
Orycteropus aferSubmetacentric119/16/13/2/8/4[59, 60]CP
SA
Afrosoricida
Chrysochloris asiaticaMetacentric813/18[61, 60]RP
SA
Macroscelidea
Elephantulus rupestris
Elephantulus edwardii
Submetacentric213/3/21/5[61]
[60]
CP
SA
Macroscidelis proboscidensSubmetacentric213/3/21/5[53]CP
Sirenia
Trichechus manatusMetacentric1913/3[62]CP
Eulipotyphla
Sorex araneusMetacentricbc9/5/2/13/8/7[16, 63]CP, SA
Blarinella griseldaSubmetacentric313/10/13/4/5[63]CP
Neotetracus sinensisSubmetacentric
Acrocentric
3,1013/4/20/10,
1/13/10/12/22
[63]CP
Hemiechinus auritus[64]CP
Talpa europaeaMetacentric62/13[65]CP
Cingulata
Dasypus novemcinctusSubmetacentric19[66]CP
Pilosa
Choloepus didactylusAcrocentric17[64]CP
Coniochaeta hoffmanniiAcrocentric12[66]CP
Tamandua tetradactylaMetacentric4, (2*)13/1[64, *66]CP
Bradypus torquatusAcrocentric12[67]CP
Bradypus variegatusAcrocentric17[67]CP
Carnivora
Mustela putorius[68]CP
Vulpes vulpesSubmetacentrics6,913/14, 2/8/13/3/19[69]RP
Canis lupus familiarisAcrocentrics(25*) 22, 28[*70]
[69]
[71, 72]
[16]
RP
CP
Z-F
SA
Felis silvestris catusAcrocentricA1[69]
[12, 13, 51]
CP
SA
Mephitis mephitisSubmetacentric19[73]CP
Procyon lotorMetacentric313/2[73]CP
Perissodactyla
Equus caballusAcrocentric17[74]
[13, 16]
[19]
[40]
RP
SA
Z-F
BAC
Equus asinus11[19]Z-F
Equus burchelliSubmetacentric6q13/9[19]RP
Z-F
Equus grevyi6q13/9[19]Z-F
Equus zebra hartmannae15[19]Z-F
Equus hemionus onager5q12/13/22[19]Z-F
Equus przewalskii16[19]Z-F
Diceros bicornisAcrocentric10[19]Z-F
Ceratotherium simum10[19]Z-F
Tapirus bairdii1[19]Z-F
Tapirus indicusAcrocentric18[19]Z-F
Tapirus pinchaque13[19]Z-F
Tapirus terrestris8[19]Z-F
Hemiechinus auritusSubmetacentrics5q,65/13, 2/22/12/13/12[64]CP
Pholidota
Manis javanicaSubmetacentric
Metacentric
1,9q13/5/2p, 18/13[64]
[75]
CP
CP
Manis pentadactylaSubmetacentric
Acrocentric
1q, 1713/5/2, 13[75]CP
Cetartiodactyla
Bos taurusAcrocentric12[12, 16]
[76]
SA
RP
Sus scrofaMetacentric11[12, 16]
[76]
SA
RP
Camelus dromedariusMetacentric14[76]RP
Globicephala melasMetacentric15[77]Z-F
Hippopotamus amphibiousMetacentric15[77]Z-F
Giraffa camelopardalisMetacentric1214/15/13[77]Z-F
Okapia johnstoniAcrocentric11[77]Z-F
Moschus moschiferusAcrocentric17[77]Z-F
Lagomorpha
Oryctolagus cuniculusSubmetacentric813/12[78]
[51]
RP
SA
Rodentia
Mus musculus3,5,8,14,14[13]
[79]
[16]
SA
SA
SA
Rattus norvegicus2,12,15,15,16[13]
[16]
SA
SA
Sciurus carolinensisSubmetacentric610/13[80]
[81]
RP
RP
Petaurista albiventerMetacentric1110/13[81]CP
Tamias sibiricusMetacentric1010/13[81]CP
Castor fibreSubmetacentric48/13[79]CP
Pedetes capensisSubmetacentric613/12/22[79]CP
Sicista betulinaMetacentric,
Submetacentric
1,913/4/10/11/9/10, 3/6/313/19[79]CP
Chiroptera
Eonycteris spelaeaSubmetacentricE1113/4/8/13[82]CP
Rhinolophus mehelyiAcrocentricR613/4/8/13[82]CP
Hipposideros larvatusMetacentricH113/3/21[82, 83]CP
Mormopterus planicepsMetacentricM713/18[82]CP
Myotis myotisMetacentricV5/64/8/13/12/22[82]CP
Aselliscus stoliczkanusMetacentric122/12/13/4/8/13[83]CP
Megaderma spasmaMetacentric1220/13/8b/4c[84]CP
Taphozous melanopogonSubmetacentric14c/8b/13/16b/7c/5a[84]CP
Primates
Strepsirrhini
Avahi laniger12[85]CP
Daubentonia madagascariensis8p10/13[85]CP
Eulemur fulvus12[85]CP
Hapalemur griseus griseus15[85]CP
Indri indriSubmetacentric3p13/17[85]CP
Lemur cattaAcrocentric13[85, 86]BAC
CP
Lepilemur ankaranensis14[87]CP
Lepilemur dorsalis6p[85, 87]CP
Lepilemur edwardsi6p[87]CP
Lepilemur leucopus1q ter[87]CP
Lepilemur microdon5p[87]CP
Lepilemur mittermeieri7p[87]CP
Lepilemur mustelinus8 ter[87, 85]CP
Lepilemur jamesi5q ter[87]CP
Lepilemur ruficaudatus5q prox[85, 87]CP
Lepilemur septentrionalis14[85, 87]CP
Microcebus murinusSubmetacentric13[85, 87]CP
Propithecus verreauxi6q5/13[85]CP
Otolemur crassicaudatusAcrocentric14[88]CP
Galago moholiMetacentric513/16/12[88]CP
Otolemur garnettiiSubmetacentric14[89]RP
Nycticebus coucangSubmetacentric18
17
[89, 90]RP
CP
Platyrrhini
Alouatta belzebulAcrocentric14[91]CP
Alouatta carayaAcrocentric15 (20*)[92, *93]CP
Alouatta guariba guaribaAcrocentric14[93]CP
Alouatta seniculus arctoidea16[91]CP
Alouatta seniculus macconnelliSubmetacentric4q13/19[92]CP
Alouatta seniculus sara12[91]CP
Aotus lemurinusgriseimembraAcrocentric17[93, 94]CP
Aotus nancymaaeAcrocentric19[95]CP
Ateles geoffroyi[96]CP
Ateles belzebuth hybridusAcrocentric12[97]CP
Ateles belzebuth marginatusSubmetacentric12[98]CP
Ateles paniscus paniscusMetacentric413a/13b/3c/7b/1a2[98]CP
Brachyteles arachnoidesAcrocentric20[98]CP
Callicebus donacophilus pallescensAcrocentric15[99]CP
Callicebus lugensSubmetacentric11/13–12/13[100]CP
Callicebus molochAcrocentric21[101]CP
Callicebus cupreusSubmetacentric
Acrocentric
7,173/21/13, 13/17[102]CP
Callimico goeldiiAcrocentrics19,1713/9/22, 13/17[18, 103]CP
RP
Callithrix argentataSubmetacentrics2,113/9/22, 20/17/13[18, 103]CP
RP
Callithrix jacchusSubmetacentrics1,513/9/22, 20/17/13[18, 103]CP
RP
Cebuella pygmaeaSubmetacentrics1,413/9/22,20/17/13[18, 103]CP
Saguinus oedipusSubmetacentrics1,29/13/22,20/17/13[18, 103]CP
Cebus apella (Sapajus)Acrocentric17[104, 105]CP
Z-F
Sapajus a. paraguayanusAcrocentric17[105]Z-F
Sapajus A. robustusAcrocentric17[105]Z-F
Cebus capucinusAcrocentric11[105]CP
Cebus nigrivitatusAcrocentric17[97]CP
Chiropotes israelitaAcrocentric15[95]CP
Chiropotes utahickiAcrocentric15[95]CP
Lagothrix lagotrichaSubmetacentric8[106]CP
Leontopithecus chrysomelasSubmetacentrics1,29/13/22,13/17/20[107]CP
Pithecia irrorataSubmetacentric822/13[108]CP
Cacajao calvus rubicundusAcrocentric13[108]CP
Saimiri sciureusAcrocentric16[18, 101]CP
Catarrhini
Chlorocebus aethiopsMetacentric3[109]CP
Cercopithecus erythrogasterSubmetacentric12[110]Z-F
Cercopithecus neglectusMetacentric19[111]RP
Cercopithecus stampfliiSubmetacentric13[110]Z-F
Presbytis cristataMetacentric19[112]CP
Colobus guerezaMetacentric19[113]CP
Erythrocebus patasSubmetacentric15[111]RP
Hylobates concolorMetacentrics5,91/13; 1/4/10/13[114]CP
Hylobates klossii4q3/13[115]CP
Hylobates larMetacentric4q3/13[17]CP
Hylobates moloch4q3/13[115]CP
Macaca fuscataSubmetacentric16[116]CP
Nasalis larvatusMetacentric15[117]CP
Pygathrix nemaeusSubmetacentric17[118]CP
Semnopithecus francoisiMetacentric9[119]CP
Semnopithecus phayreiMetacentric9[115]CP
Symphalangus syndactylus15[17]CP
Pongo pygmaeusAcrocentric14[17]CP
Gorilla gorillaAcrocentric14[17]CP
Pan troglodytesAcrocentric14[17]CP
Scandentia
Tupaia belangeriAcrocentric17[120]CP
Tupaia minorAcrocentric16[121]CP
Galliformes
Gallus gallus1[51, 52]SA
Monotremata
Ornithorhynchus anatinusSubmetacentric
Metacentrics
2,10,20[51]SA
Didelphimorphia
Monodelphis domesticaSubmetacentrics4,7[51, 52]SA

Table 2.

List of species analyzed by chromosomal painting (CP or reciprocal P) and/or sequence alignments (SA) and the references used. For each species is reported the human chromosome 13 homologous and eventually, if present other human associations.

Figure 1.

The mammalian phylogenetic tree showing the orthologue blocks that correspond to human chromosome 13—in yellow—in representative eutherian species for which reciprocal chromosome painting is available. For some species also DNA sequence alignments have been previously showed, see Table 2 for citation; in the tree, it is reported the ancestral synteny 13 form described by painting data analysis and in the box the eutherian ancestral chromosome 13 alternative reconstruction obtained through sequence data* [17]. The platypus (Monotremata), opossum (Metatheria) and chicken (Aves) chromosomes homologues are reported in the box to the low right; these last species are representative outgroups. Different colours represent HSA human syntenies which are reported on the right of the ideogram; white region represents parts of chromosomes covered by many different human syntenies; on the left of the ideogram are reported the species’ chromosome number of the 13 human homologues; the black circle is the centromere.

Through genome assembly analysis (alignments of sequences, SA), chromosome 13 has also been shown to be conserved in many mammals such as pigs, horses, and cats [13], very rearranged in mice (Mus musculus ch 3, 5, 8, 14) [14] and fragmented in platypus (Ornithorhynchus anatinus ch 2, 10, 20) [51]; moreover, it has also been shown to be present in the outgroups Opossum (Monodelphis domestica ch 4, 7) and chicken (Gallus gallus ch 1) [52] (Table 2, Figure 1). More recently, researchers analysing more than 19 placental mammals have hypothesised that the eutherian homologue 13 ancestor was fused with other human syntenies (HSA 4, and parts of HSA 2 and 8) [16]. This alternative reconstruction obtained through sequence data (in Figure 1 reported in the box*) see synteny 13 on EUT ch 1 associated with other HSA syntenies (2 orange/8 lightgreen/4 bordoux) according with previous sequence alignments work [17]. Part of this human associations (13/2/8/4) involving human synteny 13 is found through painting just in Greater mouse-eared bat ch 5/6, HSA syntenies 4/8/13/12/22, and for this reason, the alternative reconstruction do not find support through painting. Thus, the two reconstructions, by painting and by sequence analysis, regarding the ancestral synteny 13 in eutherian are not in agreement. Better analysis is needed in order to clarify this complex origin. The main issue to be considered to shed light on this issue is the use of appropriate outgroups in the reconstruction of the ancestral eutherian chromosome forms and the incomplete set of taxa analysed. Indeed, the lack of comparative chromosome painting between eutherians and other mammals, such as monotreme and marsupials, and on the other hand the lack of data on many genomes do not permit an exact reconstruction [16, 53].

Human chromosome 13 has also been analysed by mapping BAC probes onto representative Mammalian orders [40]; this work has especially focused attention on the history of this chromosome, with particular focus on intrachromosomal rearrangements and the potential relationships between evolutionarily new centromeres (ENCs) and neocentromeres occurring in clinical cases. Indeed, it has been hypothesised that neocentromere formation, a typical event in many tumours, could occur in correspondence to ENC position arising during evolution [54]. BAC mapping has permitted the study of small intrachromosomal rearrangements along the human 13 homologues and the identification of the occurrence of new evolutionary centromeres. Among mammals, evolutionary centromere repositioning on HSA 13 homologues have been shown in pigs and many primates such as for example on Lagothrix lagotricha chromosome 8 [40]; furthermore, a small inversion is common in nonprimate mammals [3, 40].

Although human chromosome 13 has been previously shown to be conserved, when compared to ancestral primate chromosomes, it shows some degree of rearrangements in certain primate taxa. Conflicting interpretations of classical banding data on human and great ape chromosome 13 have been published [1, 55, 56]. Among Hominoids, humans, chimpanzees, and orangutans share the same acrocentric form from which the gorillas’ differs by only a small paracentric inversion [57]. Among Strepsirrhini, it is a single conserved chromosome as seen for example in grey mouse lemur (Microcebus murinus ch 13); however, in this species, synteny 13 is metacentric presumably due to an inversion or alternatively for the occurrence of a new centromere. Synteny 13 has gone to different rearrangements in other species such as, for example, in indri (Indri indri ch 3), where it is fused with synteny 17 in red (Figure 1).

Among Catarrhines (Old World monkeys), the HSA 13 homologues differ in the presence of new centromeres, for example Vervet monkey (Chlorocebus aethiops); the Chlorocebus chromosome 3 are, indeed, metacentric if compared with the acrocentric human form (Figure 1).

Even if human chromosome 13 is presumably conserved in the ancestors of platyrrhines, HSA 13 homologue has gone into many rearrangements in New World monkeys; indeed, synteny 13 has gone to fission and subsequent translocation with other HSA syntenies in Common marmosets (Callithrix jacchus), resulting in chromosome 1 and 5 (covered, respectively, by HSA 13 yellow/9 blue/22 darkgreen and 13 yellow/17 red/20 lightgreen), and in Titi monkeys (Callicebus cupreus) resulting in ch 7 and 17 (covered, respectively, by HSA 3 fuxia/21 lightblue/13 yellow and 13 yellow/17 red; Figure 1). Furthermore, some intrachromosomal rearrangements, such as inversions and new centromeres, have been shown by BAC in other Platyrrhini [40].

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3. Conclusion

Classic cytogenetics, using banding, and molecular cytogenetics, using painting or other mapping probes such as BAC, are useful methods for reconstructing human chromosome history in a comparative approach with mammals. Although human chromosome 13 has previously been shown to be conserved in mammals, it is less conserved then previously claimed; indeed, some interchromosomal rearrangements have been demonstrated through painting, and intrachromosomal rearrangements have been shown by BAC mapping in various taxa; for this reason, further analysis is needed. Furthermore, the ancestral eutherian form has yet to be elucidated, as contrasting results continue to be shown through painting and sequence data comparison.

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Acknowledgments

Thanks to the “Fondazione Intesa San Paolo Onlus” which supported this work by funding the project “Evoluzione genomica in Primates” (2016-NAZ-0012, CUP, B72F16000130005) of F.D.

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Conflict of interest

We have no conflicts of interest.

References

  1. 1. Dutrillaux B. Chromosomal evolution in primates: Tentative phylogeny from Microcebus murinus (Prosimian) to man. Human Genetics. 1979;48:251-314
  2. 2. Stanyon R, Rocchi M, Capozzi O, Roberto R, Misceo D, Ventura M, et al. Primate chromosome evolution: Ancestral karyotypes, marker order and neocentromeres. Chromosome Research. 2008:17-39
  3. 3. Rocchi M, Archidiacono N, Schempp W, Capozzi O, Stanyon R. Centromere repositioning in mammals. Heredity. 2012;108(1):59-67
  4. 4. Dumas F, Mazzoleni S. Neotropical primate evolution and phylogenetic reconstruction using chromosomal data. The Italian Journal of Zoology. 2017;84(1):1-18
  5. 5. Sineo L, Dumas F, Vitturi R, Picone B, Privitera O, Stanyon R. Williams-Beuren mapping in Callithrix argentata, Callicebus cupreus and Alouatta caraya indicates different patterns of chromosomal rearrangements in neotropical primates. Journal of Zoological Systematics and Evolutionary Research. 2007;45(4):366-371
  6. 6. Picone B, Dumas F, Stanyon R, Lannino A, Bigoni F, Privitera O, et al. Exploring evolution in Ceboidea (Platyrrhini, primates) by Williams-Beuren probe (HSA 7q11.23) chromosome mapping. Folia Primatologica. 2008;79(5):417-427
  7. 7. Dumas F, Sineo L, Ishida T. Taxonomic identification of Aotus (Platyrrhinae) through cytogenetics | Identificazione tassonomica di Aotus (Platyrrhinae) mediante la citogenetica. Journal of Biological Research. 2015;88(1):65-66
  8. 8. Dumas F, Cuttaia H, Sineo L. Chromosomal distribution of interstitial telomeric sequences in nine neotropical primates (Platyrrhini): Possible implications in evolution and phylogeny. Journal of Zoological Systematics and Evolutionary Research. 2016;54(3):226-236
  9. 9. Mazzoleni S, Schillaci O, Sineo L, Dumas F. Distribution of interstitial telomeric sequences in primates and the pygmy tree shrew (Scandentia). Cytogenetic and Genome Research. 2017;151(3):141-150
  10. 10. Mazzoleni S, Rovatsos M, Schillaci O, Dumas F. Cytogenetics evolutionary insight on localization of 18S, 28S rDNA genes on homologous chromosomes in Primates genomes. Comparative Cytogenetics. 2018;12(1):27-40
  11. 11. Hruba M, Dvorak P, Weberova L, Subrt I, Hruba M, Dvorak P, et al. Independent coexistence of clones with 13q14 deletion at reciprocal translocation breakpoint and 13q14 interstitial deletion in chronic lymphocytic leukemia. Leukemia & Lymphoma. 2012;53(10):2054-2062
  12. 12. Froenicke L. Origins of primate chromosomes—As delineated by Zoo-FISH and alignments of human and mouse draft genome sequences. Cytogenetic and Genome Research. 2005;108:122-138
  13. 13. Murphy WJ, Larkin DM, Der WAE, Bourque G, Tesler G, Auvil L, et al. Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science. 2005;309(5734):613-617
  14. 14. Ma J, Zhang L, Suh BB, Raney BJ, Burhans RC, Kent WJ, et al. Reconstructing contiguous regions of an ancestral genome. Genome Research. 2006;16(12):1557-1565
  15. 15. Robinson TJ, Ruiz-herrera A, Froenicke L. Dissecting the mammalian genome—New insights into chromosomal evolution. Trends in Genetics. 2006;22(6):297-301
  16. 16. Kim J, Farré M, Auvil L, Capitanu B, Larkin DM, Ma J, et al. Reconstruction and evolutionary history of eutherian chromosomes. PNAS. 2017;114(27):E5379-E5388
  17. 17. Jauch A, Wienberg4 J, Stanyon R, Arnoldt N, Tofanelli S, Ishidaii T, et al. Reconstruction of genomic rearrangements in great apes and gibbons by chromosome painting. PNAS. 1992;89:8611-8615
  18. 18. Dumas F, Stanyon R, Sineo L, Stone G, Bigoni F. Phylogenomics of species from four genera of New World monkeys by flow sorting and reciprocal chromosome painting. BMC Evolutionary Biology. 2007;7(Suppl 2):S11
  19. 19. Trifonov VA, Stanyon R, Nesterenko AI, Fu B, Perelman PL, O’Brien PCM, et al. Multidirectional cross-species painting illuminates the history of karyotypic evolution in Perissodactyla. Chromosome Research. 2008;16(1):89-107
  20. 20. Weise A, Starke H, Mrasek K, Claussen U, Liehr T. New insights into the evolution of chromosome 1. Cytogenetic and Genome Research. 2005;108:217-222
  21. 21. Murphy WJ, Froenicke L, O’Brien SJ, Stanyon R. The origin of human chromosome 1 and its homologs in placental mammals. Genome Research. 2003;13(8):1880-1888
  22. 22. Fan Y, Linardopoulou E, Friedman C, Williams E, Trask BJ. Genomic structure and evolution of the ancestral chromosome fusion site in 2q13-2q14.1 and paralogous regions on other human chromosomes. Genome Research. 2002;12(11):1651-1662
  23. 23. Müller S, Stanyon R, Finelli P, Archidiacono N, Wienberg J. Molecular cytogenetic dissection of human chromosomes 3 and 21 evolution. PNAS. 2000;97(1):206-211
  24. 24. Tsend-Ayush E, Grützner F, Yue Y, Grossmann B, Hänsel U, Sudbrak R, et al. Plasticity of human chromosome 3 during primate evolution. Genomics. 2004;83(2):193-202
  25. 25. Yue Y, Grossmann B, Tsend-ayush E, Grützner F, Yang F, Haaf T. Genomic structure and paralogous regions of the inversion breakpoint occurring between human chromosome 3p12.3 and orangutan chromosome. Cytogenetic and Genome Research. 2005;108(1-3):98-105
  26. 26. Ruiz-Herrera A, Robinson TJ. Evolutionary plasticity and cancer breakpoints in human chromosome 3. BioEssays. 2008;30(11-12):1126-1137
  27. 27. Marzella R, Viggiano L, Miolla V, Storlazzi CT, Ricco A, Gentile E, et al. Molecular cytogenetic resources for chromosome 4 and comparative analysis of phylogenetic chromosome IV in great apes. Genomics. 2000;63(3):307-313
  28. 28. Dumas F, Sineo L. Chromosomal dynamics in platyrrhinae by mapping BACs probes. Journal of Biological Research. 2012;LXXXV:299-301
  29. 29. Dumas F, Sineo L. The evolution of human synteny 4 by mapping sub-chromosomal specific probes in Primates. Caryologia. 2014;67(4):281-291
  30. 30. Marzella R, Viggiano L, Ricco AS, Tanzariello A, Fratello A, Archidiacono N, et al. A panel of radiation hybrids and YAC clones specific for human chromosome. Cytogenetics and Cell Genetics. 1997;77(3-4):232-237
  31. 31. Szamalek JM, Goidts V, Chuzhanova N, Hameister H, Cooper DN, Keherer-Sawatzki H. Molecular characterization of the pericentric inversion that distinguishes human chromosome 5 from the homologous chimpanzee chromosome. Human Genetics. 2005;117(2-3):168-176
  32. 32. Capozzi O, Purgato S, Addabbo PD, Archidiacono N, Battaglia P, Spada F, et al. Evolutionary descent of a human chromosome 6 neocentromere: A jump back to 17 million years ago. Genome Research. 2009;19(5):778-784
  33. 33. Eder V, Ventura M, Ianigro M, Teti M, Rocchi M, Archidiacono N. Chromosome 6 phylogeny in primates and centromere repositioning. Molecular Biology and Evolution. 2003;20(9):1506-1512
  34. 34. Richard F, Lombard M, Dutrillaux B. Phylogenetic origin of human chromosomes 7, 16, and 19 and their homologs in placental mammals. Genome Research. 2000;10(5):644-651
  35. 35. Müller S, Finelli P, Neusser M, Wienberg J. The evolutionary history of human chromosome 7. Genomics. 2004;84:458-467
  36. 36. Dumas F, Sineo L. Chromosomal dynamics in Cercopithecini studied by Williams-Beuren probe mapping. Caryologia. 2010;63(4):435-442
  37. 37. Montefalcone G, Tempesta S, Rocchi M, Archidiacono N. Centromere repositioning. Genome Research. 1999;9(12):1184-1188
  38. 38. Carbone L, Ventura M, Tempesta S. Evolutionary history of chromosome 10 in primates. Chromosoma. 2002:267-272
  39. 39. Cardone MF, Lomiento M, Teti MG, Misceo D, Roberto R, Capozzi O, et al. Evolutionary history of chromosome 11 featuring four distinct centromere repositioning events in Catarrhini. Genomics. 2007;90(1):35-43
  40. 40. Cardone MF, Alonso A, Pazienza M, Ventura M, Montemurro G, Carbone L, et al. Independent centromere formation in a capricious, gene-free domain of chromosome 13q21 in Old World monkeys and pigs. Genome Biology. 2006;7(10):R91
  41. 41. Ventura M, Mudge JM, Palumbo V, Burn S, Blennow E, Pierluigi M, Giorda R, et al. Neocentromeres in 15q24Y26 map to duplicons which flanked an ancestral centromere in 15q25. Genome Research. 2003;13(9):2059-2068
  42. 42. Locke DP, Jiang Z, Pertz LM, Misceo D, Archidiacono N, Eichler EE. Molecular evolution of the human chromosome 15 pericentromeric region. Genome Biology. 2005;108:73-82
  43. 43. Misceo D, Ventura M, Eder V, Rocchi M, Archidiacono N. Human chromosome 16 conservation in primates. Chromosome Research. 2003;11(4):323-326
  44. 44. Goits V, Szamalek JM, Hameister H, Kehrer-Sawatzki H. Segmental duplication associated with the human-specific inversion of chromosome 18: A further example of the impact of segmental duplications on karyotype and genome evolution in primates. Human Genetics. 2004:116-122
  45. 45. Misceo D, Cardone MF, Carbone L, D’Addabbo P, de Jong PJ, Rocchi M, et al. Evolutionary history of chromosome 20. Molecular Biology and Evolution. 2005;22(2):360-366
  46. 46. Wimmer R, Kirsch S, Rappold GA, Schempp W. The evolution of the azoospermia factor region AZFa in higher primates. Cytogenetic and Genome Research. 2005;108:211-216
  47. 47. Dunham A, Matthews LH, Burton J, Ashurst JL, Howe KL, Ashcroft KJ, et al. The DNA sequence and analysis of human chromosome 13. Nature. 2004;428:522-528
  48. 48. Bailey JA, Gu Z, Clark RA, Reinert K, Samonte RV, Schwartz S, et al. Recent segmental duplications in the human genome. Science. 2002;297:1003-1007
  49. 49. Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O’Brien SJ. Molecular phylogenetics and the origins of placental mammals. Nature. 2001;409(6820):614-618
  50. 50. Maddison WP, Maddison DRV. Mesquite: A modular system for evolutionary analysis. 2008;11:1103-1118. http.//mesquiteproject
  51. 51. Graphodatsky A, Ferguson-Smith MA, Stanyon R. A short introduction to cytogenetic studies in mammals with reference to the present volume. Cytogenetic and Genome Research. 2012;137(2-4):83-96
  52. 52. Robinson TJ, Ruiz-herrera A. Defining the ancestral eutherian karyotype: A cladistic interpretation of chromosome painting and genome sequence assembly data. Chromosome Research. 2008;16:1133-1141
  53. 53. Svartman M, Stone G, Page JE, Stanyon R. A chromosome painting test of the basal Eutherian karyotype. Chromosome Research. 2004;12:45-53
  54. 54. Alonso A, Mahmood R, Li S, Cheung F, Yoda K, Warburton PE. Genomic microarray analysis reveals distinct locations for the CENP-A binding domains in three human chromosome 13q32 neocentromeres. Human Molecular Genetics. 2003;12(20):2711-2721
  55. 55. Clemente IC, Ponsa M, Garcia M, Egozcue J. Evolution of the Simiiformes and the phylogeny of human chromosomes. Human Genetics. 1990;84:493-506
  56. 56. Yunis JJ, Prakash O. The origin of man: A chromosomal pictorial legacy. Science. 1982;215(4539):1525-1530
  57. 57. Muller S, Wienberg J. “Bar-coding” primate chromosomes: molecular cytogenetic screening for the ancestral hominoid karyotype. 2001;109:85-94
  58. 58. Nie W, Fu B, O’Brien PCM, Wang J, Su W, Tanomtong A, et al. Flying lemurs—The “flying tree shrews”? Molecular cytogenetic evidence for a Scandentia-Dermoptera sister clade. BMC Biology. 2008;6:18
  59. 59. Yang F, Alkalaeva EZ, Perelman PL, Pardini AT, Harrison WR, O'Brien PCM, et al. Reciprocal chromosome painting among human, aardvark, and elephant (superorder Afrotheria) reveals the likely eutherian ancestral karyotype. PNAS. 2003;100:1062-1066
  60. 60. Ruiz-Herrera A, Robinson TJ. Chromosomal instability in Afrotheria: Fragile sites, evolutionary breakpoints and phylogenetic inference from genome sequence assemblies. BMC Evolutionary Biology. 2007;7:199
  61. 61. Robinson TJ, Fu B, Ferguson-Smith MA, Yang F. Cross-species chromosome painting in the golden mole and elephant-shrew: Support for the mammalian clades Afrotheria and Afroinsectiphillia but not Afroinsectivora. The Royal Society. 2004;271:1477-1484
  62. 62. Kellogg ME, Burkett S, Dennis TR, Stone G, Gray BA, McGuire PM, et al. Chromosome painting in the manatee supports Afrotheria and Paenungulata. BMC Evolutionary Biology. 2007;7:6
  63. 63. Ye J, Biltueva L, Huang L, Nie W, Wang J, Jing M, et al. Cross-species chromosome painting unveils cytogenetic signatures for the Eulipotyphla and evidence for the polyphyly of Insectivora. Chromosome Research. 2006;14(2):151-159
  64. 64. Yang F, Graphodatsky AS, Li T, Fu B, Dobigny G, Wang J, et al. Comparative genome maps of the pangolin, hedgehog, sloth, anteater and human revealed by cross-species chromosome painting: Further insight into the ancestral karyotype and genome evolution of eutherian mammals. Chromosome Research. 2006;14:283-296
  65. 65. Volleth M, Müller S. Zoo-FISH in the European mole (Talpa europaea) detects all ancestral Boreo-Eutherian human homologous chromosome associations. Cytogenetic and Genome Research. 2006;115:154-157
  66. 66. Svartman M, Stone G, Stanyon R. The ancestral Eutherian karyotype is present in Xenarthra. PLoS Genetics. 2006;2(7):1006-1011
  67. 67. Azevedo NF, Svartman M, Manchester A, de Moraes-Barros N, Stanyon R, Vianna-Morgante AM. Chromosome painting in three-toed sloths: A cytogenetic signature and ancestral karyotype for Xenarthra. BMC Evolutionary Biology. 2012;15-21:12-36
  68. 68. Cavagna P, Menotti A, Stanyon R. Genomic homology of the domestic ferret with cats and humans. Mammalian Genome. 2000;11:866-870
  69. 69. Yang F, O’Brien PCM, Milne BS, Graphodatsky AS, Solanky N, Trifonov V, et al. A complete comparative chromosome map for the dog, red fox, and human and its integration with canine genetic maps. Genomics. 1999;62:189-202
  70. 70. Breen M, Thomas R, Binns MM, Carter NP, Langford CF. Reciprocal chromosome painting reveals detailed regions of conserved synteny between the karyotypes of the domestic dog (Canis familiaris) and human. Genomics. 1999;61(2):145-155
  71. 71. Yang F, Graphodatsky AS, O’Brien PCM, Colabella A, Solanky N, Squire M, et al. Reciprocal chromosome painting illuminates the history of genome evolution of the domestic cat, dog and human. Chromosome Research. 2000;8:393-404
  72. 72. Graphodatsky AS, Perelman PL, Sokolovskaya NV, Beklemisheva VR, Serdukova NA, Dobigny G, et al. Phylogenomics of the dog and fox family (Canidae, Carnivora) revealed by chromosome painting. Chromosome Research. 2008;16(1):129-143
  73. 73. Perelman PL, Graphodatsky AS, Dragoo JW, Serdyukova NA, Stone G, Cavagna P, et al. Chromosome painting shows that skunks (Mephitidae, Carnivora) have highly rearranged karyotypes. Chromosome Research. 2008;16(8):1215-1231
  74. 74. Yang F, Fu B, O’Brien PCM, Nie W, Ryder OA, Ferguson Smith MA. Refined genome-wide comparative map of the domestic horse, donkey and human based on cross-species chromosome painting: Insight into the occasional fertility of mules. Chromosome Research. 2004;12:65-76
  75. 75. Nie W, Wang J, Su W, Wang Y, Yang F. Chromosomal rearrangements underlying karyotype differences between Chinese pangolin (Manis pentadactyla) and Malayan pangolin (Manis javanica) revealed by chromosome painting. Chromosome Research. 2009;17:321-329
  76. 76. Balmus G, Trifonov VA, Biltueva LS, O’Brien PCM, Alkalaeva ES, Fu B, et al. Cross species painting among camel, cattle, pig and human: Further insights into the putative Cetartiodactyla ancestral karyotype. Chromosome Research. 2007;15:499-514
  77. 77. Kulemzina AI, Trifonov VA, Perelman PL, Rubtsova NV, Volobuev V, Ferguson-Smith MA, et al. Cross-species chromosome painting in Cetartiodactyla: Reconstructing the karyotype evolution in key phylogenetic lineages. Chromosome Research. 2009;17(3):419-436
  78. 78. Korstanje R, O’Brien PCM, Yang F, Rens W, Bosma AA, van Lith HA, et al. Complete homology maps of the rabbit (Oryctolagus cuniculus) and human by reciprocal chromosomal painting. Cytogenetics and Cell Genetics. 1999;83:317-322
  79. 79. Graphodatsky AS, Yang F, Dobigny G, Romanenko SA, Biltueva LS, Perelman PL, et al. Tracking genome organization in rodents by Zoo-FISH. Chromosome Research. 2008;16(2):261-274
  80. 80. Stanyon R, Stone G, Garcia M, Froenicke L. Reciprocal chromosome painting shows that squirrels, unlike murid rodents, have a highly conserved genome organization. Genomics. 2003;82(2):245-249
  81. 81. Li T, O’Brien PCM, Biltueva L, Fu B, Wang J, Nie W, et al. Evolution of genome organizations of squirrels (Sciuridae) revealed by cross-species chromosome painting. Chromosome Research. 2004;12(4):317-335
  82. 82. Volleth M, Heller KG, Pfeiffer RA, Hameister H. A comparative ZOO-FISH analysis in bats elucidates the phylogenetic relationships between Megachiroptera and five microchiropteran families. Chromosome Research. 2002;10(6):477-497
  83. 83. Mao X, Nie W, Wang J, Su W, Ao L, Feng Q, et al. Karyotype evolution in Rhinolophus bats (Rhinolophidae, Chiroptera) illuminated by cross-species chromosome painting and G-banding comparison. Chromosome Research. 2007;15(7):835-847
  84. 84. Mao X, Nie W, Wang J, Su W, Feng Q, Wang Y, et al. Comparative cytogenetics of bats (Chiroptera): The prevalence of Robertsonian translocations limits the power of chromosomal characters in resolving interfamily phylogenetic relationships. Chromosome Research. 2008;16(1):155-170
  85. 85. Warter S, Hauwy M, Dutrillaux B, Rumpler Y. Application of molecular cytogenetics for chromosomal evolution of the Lemuriformes (Prosimians). Cytogenetic and Genome Research. 2005;108(1-3):197-203
  86. 86. Cardone MF, Ventura M, Tempesta S, Rocchi M, Archidiacono N. Analysis of chromosome conservation in Lemur catta studied by chromosome paints and BAC/PAC probes. Chromosoma. 2002;111(5):348-356
  87. 87. Rumpler Y, Warter S, Hauwy M, Fausser JL, Roos C, Zinner D. Comparing chromosomal and mitochondrial phylogenies of sportive lemurs (Genus Lepilemur, Primates). Chromosome Research. 2008;16(8):1143-1158
  88. 88. Stanyon R, Koehler U, Consigliere S. Chromosome painting reveals that galagos have highly derived karyotypes. American Journal of Physical Anthropology. 2002;117(4):319-326
  89. 89. Stanyon R, Dumas F, Stone G, Bigoni F. Multidirectional chromosome painting reveals a remarkable syntenic homology between the greater galagos and the slow loris. American Journal of Primatology. 2006;68:349-359
  90. 90. Nie W, O’Brien PCM, Fu B, Wang J, Su W, Ferguson-Smith MA, et al. Chromosome painting between human and lorisiform prosimians: Evidence for the HSA 7/16 synteny in the primate ancestral karyotype. American Journal of Physical Anthropology. 2006;129(2):250-259
  91. 91. Consigliere S, Stanyon R, Koehler U, Arnold N, Wienberg J. In situ hybridization (FISH) maps chromosomal homologies between Alouatta belzebul (Platyrrhini, Cebidae) and other primates and reveals extensive interchromosomal rearrangements between howler monkey genomes. American Journal of Primatology. 1998;46(2):119-133
  92. 92. De Oliveira EHC, Neusser M, Figueiredo WB, Nagamachi C, Pieczarka JC, Sbalqueiro IJ, et al. The phylogeny of howler monkeys (Alouatta, Platyrrhini): Reconstruction by multicolor cross-species chromosome painting. Chromosome Research. 2002;10(8):669-683
  93. 93. Ruiz-Herrera A, Garcia F, Aguilera M, Garcia M, Fontanals MP. Comparative chromosome painting in Aotus reveals a highly derived evolution. American Journal of Primatology. 2005;65(1):73-85
  94. 94. Stanyon R, Garofalo F, Steinberg ER, Capozzi O, Di Marco S, Nieves M, et al. Chromosome Painting in two genera of South American monkeys: Species identification, conservation, and management. Cytogenetic and Genome Research. 2011:1-11
  95. 95. Stanyon R, Bigoni F, Slaby T, Müller S, Stone G, Bonvicino CR, et al. Multi-directional chromosome painting maps homologies between species belonging to three genera of New World monkeys and humans. Chromosoma. 2004;113(6):305-315
  96. 96. Morescalchi MA, Schempp W, Wienberg J, Stanyon R. Mapping chromosomal homology between humans and the black-handed spider monkey by fluorescence in situ hybridization. Chromosome Research. 1997;5(8):527-536
  97. 97. García F, Ruiz-Herrera A, Egozcue J, Ponsà M, Garcia M. Chromosomal homologies between Cebus and Ateles (Primates) based on ZOO-FISH and g-banding comparisons. American Journal of Primatology. 2002;57(4):177-188
  98. 98. De Oliveira EHC, Neusser M, Pieczarka JC, Nagamachi C, Sbalqueiro IJ, Müller S. Phylogenetic inferences of Atelinae (Platyrrhini) based on multi-directional chromosome painting in Brachyteles arachnoides, Ateles paniscus paniscus and Ateles b. marginatus. Cytogenetic and Genome Research. 2005;108(1-3):183-190
  99. 99. Barros RMS, Nagamachi CY, Pieczarka JC, Rodrigues LRR, Neusser M, de Oliveira EH, et al. Chromosomal studies in Callicebus donacophilus pallescens, with classic and molecular cytogenetic approaches: Multicolour FISH using human and Saguinus oedipus painting probes. Chromosome Research. 2003;11(4):327-334
  100. 100. Stanyon R, Bonvicino CR, Svartman M, Seuánez HN. Chromosome painting in Callicebus lugens, the species with the diploid number (2n = 16) known in primates. Chromosome Research. 2003;112(4):201-206
  101. 101. Stanyon R, Consigliere S, Müller S, Morescalchi A, Neusser M, Wienberg J. Fluorescence in situ hybridization (FISH) maps chromosomal homologies between the dusky titi and squirrel monkey. American Journal of Primatology. 2000;50(2):95-107
  102. 102. Dumas F, Bigoni F, Stone G, Sineo L, Stanyon R. Mapping genomic rearrangements in titi monkeys by chromosome flow sorting and multidirectional in-situ hybridization. Chromosome Research. 2005:85-96
  103. 103. Neusser M, Stanyon R, Bigoni F, Wienberg J, Müller S. Molecular cytotaxonomy of New World monkeys (Platyrrhini)—Comparative analysis of five species by multi-color chromosome painting gives evidence for a classification of Callimico goeldii within the family of Callitrichidae. Cytogenetics and Cell Genetics. 2001;94:206-215
  104. 104. García F, Nogués C, Ponsà M, Ruiz-Herrera A, Egozcue J, Garcia Caldés M. Chromosomal homologies between humans and Cebus apella (Primates) revealed by ZOO-FISH. Mammalian Genome. 2000;11:399-401
  105. 105. Richard F, Lombard M, Dutrillaux B. ZOO-FISH suggests a complete homology between human and capuchin monkey (Platyrrhini) euchromatin. Chromosome Research. 1996;36:417-423
  106. 106. Stanyon R, Consigliere S, Bigoni F, Ferguson-Smith M, O’Brien PCM, Wienberg J. Reciprocal chromosome painting between a New World primate, the woolly monkey, and humans. Chromosome Research. 2001;9(2):97-106
  107. 107. Gerbault-Serreau M, Bonnet-Garnier A, Richard F, Dutrillaux B. Chromosome painting comparison of Leontopithecus chrysomelas (Callitrichine, Platyrrhini) with man and its phylogenetic position. Chromosome Research. 2004;12(7):691-701
  108. 108. Finotelo LFM, Amaral PJS, Pieczarka JC, de Oliveira EHC, Pissinati A, Neusser M, Müller S, Nagamachi CY. Chromosome phylogeny of the subfamily Pitheciinae (Platyrrhini, Primates) by classic cytogenetics and chromosome painting. BMC Evolutionary Biology. 2010;10:189
  109. 109. Finelli P, Stanyon R, Plesker R, Ferguson-Smith MA, O’Brien PCM, Wienberg J. Reciprocal chromosome painting shows that the great difference in diploid number between human and African green monkey is mostly due to non-Robertsonian fissions. Mammalian Genome. 1999;10(7):713-718
  110. 110. Moulin S, Gerbault-Seureau M, Dutrillaux B, Richard FA. Phylogenomics of African guenons. Chromosome Research. 2008;16:783-799
  111. 111. Stanyon R, Bruening R, Stone G, Shearin A, Bigoni F. Reciprocal painting between humans, De Brazza’s and patas monkeys reveals a major bifurcation in the Cercopithecini phylogenetic tree. Cytogenetic and Genome Research. 2005;108(1-3):175-182
  112. 112. Bigoni F, Koehler U, Stanyon R, Ishida T, Wienberg J. Fluorescence in situ hybridization establishes homology between human and silvered leaf monkey chromosomes, reveals reciprocal translocations bewtween chromosomes homologous to human Y/5, 1/9, and 6/16, and delineates an X1X2Y1Y2/X1X1X2X2 sex-chromosome system. American Journal of Physical Anthropology. 1997a;23:315-327
  113. 113. Bigoni F, Stanyon R, Koehler U, Morescalchi AM, Wienberg J. Mapping homology between human and black and white colobine monkey chromosomes by fluorescent in situ hybridization. American Journal of Primatology. 1997b;42(4):289-298
  114. 114. Koehler U, Bigoni F, Wienberg J, Stanyon R. Genomic reorganization in the concolor gibbon (Hylobates concolor) revealed by chromosome painting. American Journal of Physical Anthropology. 1995;292:287-292
  115. 115. Müller S, Hollatz M, Wienberg J. Chromosomal phylogeny and evolution of gibbons (Hylobatidae). Human Genetics. 2003;113(6):493-501
  116. 116. Wienberg J, Stanyon R, Jauch A, Cremer T. Homologies in human and Macaca fuscata chromosomes revealed by in situ suppression hybridization with human chromosome specific DNA libraries. Chromosoma. 1992;101:265-270
  117. 117. Bigoni F, Stanyon R, Wimmer R, Schempp W. Chromosome painting shows that the proboscis monkey (Nasalis larvatus) has a derived karyotype and is phylogenetically nested within Asian colobines. American Journal of Primatology. 2003;60(3):85-93
  118. 118. Bigoni F, Houck ML, Ryder OA, Wienberg J, Stanyon R. Chromosome painting shows that Pygathrix nemaeus has the most basal karyotype among Asian colobinae. International Journal of Primatology. 2004;25(3):679-688
  119. 119. Nie W, Liu R, Chen Y, Wang J, Yang F. Mapping chromosomal homologies between humans and two langurs (Semnopithecus francoisi and S. phayrei) by chromosome painting. Chromosome Research. 1998;6(6):447-453
  120. 120. Müller S, Stanyon R, O’Brien PCM, Ferguson-Smith MA, Plesker R, Wienberg J. Defining the ancestral karyotype of all primates by multidirectional chromosome painting between tree shrews, lemurs and humans. Chromosoma. 1999;108(6):393-400
  121. 121. Dumas F, Houck ML, Bigoni F, Perelman P, Romanenko SA, Stanyon R. Chromosome painting of the pygmy tree shrew shows that no derived cytogenetic traits link primates and scandentia. Cytogenetic and Genome Research. 2012;136(3):175-179

Written By

Rita Scardino, Vanessa Milioto and Francesca Dumas

Submitted: 31 May 2018 Reviewed: 08 June 2018 Published: 05 November 2018