Cytotaxonomy and geographical distribution of the Papinae

Cytotaxonomy and Geo+raphical Distribution of the Papmae

Jan Schmager Dgartment of Anthropology, Jag&mian Um’vcrsity, ul. Kzupnicra 50, Krakow, Poland Received 28 January

1972

The comparative analysis of the metrical data concerning the chromosomes of 12 species Macaca, 5 species Pa@, Thcropithsus g&da and 4 species of genus Cercocebus has been made. Some connections between the structure of the karyotypes and geographical distribution were observed, especially in genus Macaca.

1. Introdllction The various species of the genus Mama, Papio, Thercopithecus and Cercocebus have been grouped by Chiarelli (1962) in a single subfamily called Papinae. They are distributed in almost all of Africa and tropical and subtropical Asia, with the exception of Macaca sylvana, which inhabits Gibraltar. The Macaques are latitudinally the most widespread, with geographic distribution ranging from the Japanese islands to Gibraltar, and the most heterogenous for habitat and ecology. Some species are well differentiated and inhabit distinct isolated territories. For others, however, there are still some doubts as to their definition, having natural hybrids when populations of different presumed species are overlapping. Napier & Napier (1967) recognize 12 species of Macaques and this is considered the most recent taxonomic point of view. The baboons are distributed in almost all Africa and in the extreme western point of the Arabian peninsula. They occupy a well-defined “habitat” and ecology (Tappen, 1960: Osman Hill, 1967; Napier & Napier, 1967). Only in a few cases does an overlap of two species exist in the same geographical area without giving origin to group hybridization. An overlap in geographical distribution occurs, for example, for Papio leucophaeus and P. sphinx. However, the diverse ecological niches and the probable ethological barriers seem to limit any possible contact between these two species. Genetic discontinuity among the various Papio species is maintained by several ethological characteristics, almost always related to sexual choice (Kummer, 1968). The various species attributed to the genus Papio are recognizable on the basis of welldefined morphological differences and Osman Hill (1967) lists six different species in this genus. If one adds P. sphinx and P. leucophaeus (which Hill ascribes to the genus Mandrillus, but which are more commonly attributed to the genus Papio (Fiedler, 1956)) and eventually the Thercopithecus gelada (which Chiarelli, 1962, considers very similar to the Papio), we have a compact stock of species. The Cercocebus inhabit the forest of Central Africa and the geographic boundary of each species is still undefined, as are some aspects of the species’ taxonomy. This complex of species of Old World Primates seems to be an appropriate group on which to undertake a study on the connection between karyotype structure and geographical distribution. Journal of Human Evolution (1972)

1, 477485.

478

J.

SCHMAGER

2. Materials

and Methods

The present investigation was carried out on the basis of the morphometric data elaborated by Chiarelli in 1962 for the karyotypes of the different species of Macaca, Pa/Go, Thercopithecus and Cercocebus and on other data available in the Institute of Anthropology of the University of Turin or obtained from the literature. As is well known, the diploid number of chromosomes in all of this group is 42 and the chromosomes can be separated into four groups from a morphological point of view: (a) submetacentric, (b) metracentric, (c) a pair of chromosomes marked with a large achromatic region and (d) the sex chromosomes. For all the above genera, it is possible to classify 13 chromosome pairs in the first group, six in the second, and one in the third and the fourth. The X chromosomes appear to vary in size and centromere position in the different species. The Y chromosome is small and only rarely is it possible to distinguish the position of the centromere in it. On the basis of measurements, each chromosome was characterized by two indices: (1) relative length (R.A.C.L.)

=

length of each chromosome x 100 total length of the hapl. fem. karyotype >

length of long arm

(2) arm ratio (L/S) =

length of short arm > *

The mean values of both indices have been established for each chromosome of each species (excluding the arm ratio for the Y chromosome) and they are tabulated in Tables 1, 2 and 3. Table

1

Chmmosome number

3 4 5 6 7 8 9 IO 11 12 13 14 15 16 17 18 19 20 X Y

Numerical valuw of the caluhted gmupsilelongingtothe~uanlf7caca

M. &ana R.A.C.L. L/S 7.9 6.7 6.1 5.9 5.7 5.1 5.0 5.0 4.7 4.3 3.8 3.9 3.3 5.6 4.4 3.3 2.8 2.4 2-O 4.0 7.1 0.8

;:; 1.8 2.6 1.7 2.3 ;:: 2.4 33:: 2.3 I.7 I.2 1.3 1.0 1.1 1.7 1.0 1.9 2.2 -

M. jiucata R.A.C.L. 7.3 6.6 5.8 5.7 5.5 5.1 4.8 4.8 4.5 4.5 4.0 3.5 2.7 6.1 3.9 3.2 4:: 2.1 4.5 9.4 0.8

L/S ;:; 2.0 2.6 1.9 1.7 2.8 2.9 2.0 2.3 2,5 2.5 1.6 1.3 1.4 1.2 I.1 1.2 I.2 1.6 1.8 -

indim

M. mulatta, M. assamensis, M. nemertrina, M. radkta, M. @.&asa, M. &nus, M. irus M. sin&a R.A.C.L. L/S R.A.C.L. L/S 7.8 6.7 6.2 6.0 5.9 5.6 5.0 4.6 4.6 4.3 4.0 3.7 3.0 6-O 4.4 3.5 2.9 2.7 2.4 4.4 5.4 0.9

. ;.y 1.9 2.3 2.1 1.7 2.3 2.3 2.0 2.4 2.5 2.4 1.9 1.1 I.1 1.0 1.1 1.4 1.2 1.6 2.1 -

7.4 6.4 6.1 5.6 5.7 5.3 4.8 4.7 4.5 4.3 4.3 3.8 2.9 6.1 3.8 3.4 1:; 2.6 4.3 7.4 1.0

* ;.; 2.3 1.9 2.0 1.6 2.2 2.6 2.1 2.2 2.3 2.0 1.6 1.2 1.1 1.2 I.0 I.0 I.1 1.5 1.3 -

for spedem ad

M. niger, M. maura R.A.C.L. L/S 7.7 6.5

* ;.“o

5.9 5.5 4.9 4.8 4-4 4.4 3.8 3.5 3.1 6.0 4.3 3.4 2.9 2.8 2.4 4.0 6.7 0.8

2.2 1.8 * :.i 2.1 2.6 2.4 2.1 1.8 1.2 1.0 1.0 I.0 1.0 I.0 1.3 2.0 -

CYTOTAXONOW

Chromosome number 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 X Y

Table

3

AND OEOOR’iPHICAL

P. sphinr L/S R.A.C.L. 7.5 7.0 6.4 6.5 6.6 6-O 5.2 4.7 4.3 4.1 4.0 3.8 3.3 6.2 4.4 3.0 2.8 2.6 2.1 4.5 3-6 0.8

Namerid beloryty

P. hamadpas R.A.C.L. L/S

1.4 1.9 l-8 1.6 2.8 2.2 1.7 1.6 2.5 2.8 2.9 2.6 2.0 1.1 1.2 1.0 1.1 I.2 1.4 1.5 1.7 -

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 X Y

R.A.C.L. 7.9 6.5 6.1 6.1 5.4 5.2 4.9 4.7 4.6 4.2 4.2 3.8 3.6 6.3 4.7 3.4 3.2 3.0 2.7 4.7 6.0 1.0

1.5 2.3 2.2 2.8 2.1 1.8 2.1 1.9 2.5 2.9 1.4 2.8 2.8 I.1 1.1 1.1 1.1 1.2 1.1 1.6 I.1 -

P.lcucophacus, P. lynoce$vlalus, P. papio R.A.C.L. L/S 7.4 6.5 6.3 6.0 5.6 5.1 4.8 4.6 4.5 4.2 4.0 3.6 3.5 6.1 4.7 3.3 3.0 2.7 2.4 4.8 5‘5 0.9

L/S 1.6 1.6 2.3 2.1 1.7 1.2 1.9 2.1 1.6 2.1 2.1 1.3 1.8 1.1 1.0 1.0 1.0 1.0 1.1 1.6 1.7

C. atbigena, C. galcritus, c. torquatus R.A.C.L. L/S 7.9 6.6 6.1 6.0 5.4 5.4 5.2 4.9 4.6 4.4 4.0 3.7 3.2 5.9 4.6 3.5 ;:; 2.6 4.6 5.1 0.9

I.6 1.9 1.9 2.1 1.6 I.7 2.0 2.0 1.7 2.2 2.4 1.8 1.6 1.1 1.1 1.0 1.1 I*2 I.1 1.5 1.7 -

479

T. galada R.A.C.L. L/S

1.6 1.9 I.6 1.9 2.2 2.2 2.6 I.8 2.3 2.3 3.0 2.8 2.1 1.1 1.2 1.1 I.1 1.3 1.1 1.4 1.5 -

v&es of the calculated idiccs to gelmE cveoccbvs

C. aterrimus Chromosome number

7.8 6.7 6.4 6.3 6.0 5.3 5.1 4.7 4.9 4.4 3.6 3.8 3.8 6.1 4.3 3.4 2.8 2.8 2,3 4.5 5.1 0.8

DISTRIBUTION

for speck

7.4 6.9 6.6 6.0 5.9 5-8 5.0 4.7 4.6 4.1 3.8 3.9 2.7 5.9 4.7 3.5 3.1 2.8 2.5 4.2 4.7 0.9

1.5 2.0 1.9 2.3 1.8 1.8 1.8 2.2 2.1 3.2 3.0 3.2 1.7 1.0 1.0 1.1 1.3 I.1 1.2 1.6 l-8 -

and group

480

Table

J.

4

SCHMAGER

Ndd~dtlu? ingame

Names of species compared

Chromosomes different in

. size (pair number)

M. Jylvana with M. fmcata M. sylvana with M. mulatta, M. assamensis, M. nemestrina, M. irus, M. spcciasa M. sylvana with M. radiata, M. sylenus, M. sinica M. sylvana with M. niger, M. maura

M. fucata with M. mulatta, M. assamensis, M. nemestrina, M. irus, M. speciasa M. fucata with M. radiata, M. sylemss, M. sinica M. fusGata with M. niger, M. maura M. mulatta, M. assamensis, M. nemestrina, M. irus, M. speciosa with M. radiata, M. sylenus, M. sinica M. mulatta, M. assamcnsis, M. nemestrina, M. irus, M. specivsa with M. niger, M. maura M. radiata, M. sylena, M. sinica with M. niger, M. maura

compradve

position of centromere (pair number)

5

7

(12, 13, 14, 15,ZO)

5orpbo5etrialanaly1sSs

Macaca

(6, 7,8,9,

IO, 11, 18)

4 size and position of centromere (pair number)

Total number of different chromosomes

1, x

13, x

(‘1 1

5

4, X (8, 14, 19,20)

(1,5,9,10,

4

11)

(6)

3

5, X

(13, 14, 15, 19)

(3,496,

(12, 14, 19)

(1, 4,6,

2

10, 11,20) 3

4, X (L3,5,6)

12, x

(1, 11,16)

G

3, X

11, x

(5, 18) -

7, X

X

4, X

2

12,x

(7,8,15)

1

3 (4, 7, 12)

(19)

4

6, X (1,3,5,6,

10,20)

10, x

13,201

(4,7,6,

12)

1,X

2

(4)

(3, 12)

1, X

1

(20)

(7)

3

2

(4, 11515)

(7, 10)

(15,W

-

3, X

-

2, X

X

5, X

CYTOTAXONOMY

AND

GEOGRAPHICAL

DISTRIBUTION

481

In order to individuate the differences or the similarities in size and position of centromere in corresponding chromosomes belonging to different species a comparative analysis of the value of the R.A.C.L. and L/S indices has been made. When the difference between indices of corresponding chromosomes was higher than 0.4 relative units, the chromosomes were considered as different. In the analysis the different chromosomes were divided into three categories: (1) chromosomes different in relative length; (2) chromosomes different in arm ratio; (3) chromosomes different in relative length and arm ratio. The total number of different chromosomes between two species was calculated adding up to the partial results obtained from each category. In this way the karyotype of each species was compared with the karyotype of all the other species. The species belonging to the same genus with similar geographical distribution and similar karyotype were and L/S considered as a unity group; for each group the main values of R.A.C.L. indices were defined. The results of such an analysis were later on plotted in graphs in which the distances between species or groups of species are in direct relation to the amount of differences found in the chromosomes. 3. Results Macaca Five groups of species in this genus have been defined for having similar karyotype: (a) M. radiata, M. sylenus and M. sinica; (b) M. mulatta, M. assammsis, M. speciosa, M. nemestrinaand M. iru.s; (c) M. niger and M. maura; (d) M. fucata; (e) M. sylvana. The results of this analysis for this group of species are presented in Table 4, while Figure 1 presents the plotted data. Figure 1. Graphs of the connection between the karyotypes of species or groups belonging to genus Macaca. (M. sylv. = Macaca syltrana, M. i&c. = Mataca fuscatu, M. rad. = Macaca radiata, M. syl. = Macaca sylenus, M. sin. = Macaca sinica, M. mul. = Macaca mtdatta, M. ass. = Macaca ass-is, M. nem. = Macaca nemesttia, M. ir. = Macaca irus, M. sp. = Macaca speciasa, M. nig. = Macaca niger, M. maw. = Macaca maura)

M. maw.

48’2

J.

SCHMAGER

Papio and Thercopithecus Among the species studied P. leucofl~, P. qzocephalus and P. papio do not show differences in the structure of the karyotype. For this reason they have been considered as one group. P. sphinx, P. hamadryas and T~rco/.n’thmu g&da instead were considered separately for having differences in their karyotype. The results of such a comparative analysis are shown in Table 5 and Figure 2. Tpble 5

morphmnctri cddy&

Numerfcal valueat of the compudve in genera Pa.& and Theropithccns Chromosomes different in

size (pair number)

position of centromere (pair number)

1 size and position of centromexe (pair nmber)

Total numbQ of different chromosom*l

sphinx

2

4

4, x

10, x

with P. hamadtyas

(9916)

Names of species comparated P.

P. sphinx with P. kucophaeus, P. cynocephalus, P. papio P. hama&as with P. leucophaeus, P. cynacephalus, P. papio T. gelada with P. sphinx T. gciada with P. hamadryas T. gelada with P. kucophaeus, P. cynacsphallu, P. papio

Table

6

Names of speck3 comparated C. akm*mu.r with C. albigena, C. gale&w, c. torqtIahcr

/

(5,6,

(2,3,4,7)

11, 13)

3, x

1

2

(2,496)

(10)

(597)

4

7

1,x

(1,5,9,

(2,3,4,6,7,

15)

10, 13)

(13, 16, 19)

2 10; 12)

(6,8,9,

1, x 12, 15)

(4,9,11,

(196)

(4,5,7,8,

(2520)

Nmraerical aldyd8fn

2

valaes of the compurdve genus Cffh

size (pair n-b@ 5 (7,9,

15, 16,ZO)

10, x

(6313)

10,121

morphometrical

Chromosomes different in

.

6, X

(13)

6

2, x

10, x

(4,5)

5

2

12, x

(11)

5

3, x

6, X

position of centromere (pair number)

size and position of centromere (pair number)

Total number of different chrom-mes

3

2, x

10,x

(5,&W

(6,13)

CYTOTAXONOMY Figure 2. Graphs of the connection between the karyotypes of species and group belonging to genus Papio and Thcr~ithscus. (P. sph. = Pa@ sphinx, P. ham. = Papio hamadryas, P. leuc. = Papio leuco#aaeus, P. cyn. = Papio cynoccphalus, P. pap. = Pa@ papio, T. gel. = Thnopithecus gelada.

Figure 3. Graphs of the connection between the karyotypes of species and group belonging to genus Cercocebus. ater. = Cercocebus aterrimus, cc. C. alb. = Cercocebus albigena, C. gal. = Cercocebusgaleritus, C. tor. = Cercocebus kwquatur) .

AND

GEOGRAPHICAL.

DISTRIBUTION

483

P. sph.

C cter.

C. alb. C. gal. C. tor.

Cercocebus The karyotype of C. aterrimus resulted very differently from the other Cercocebusspecies, which instead do not show any significant difference. The result of the analysis is presented in Table 6 and Figure 3. 4. Discussion The results of this comparative analysis on the karyotypes of Mama, Papio, Thmofiithecus and Cercocebusseem to indicate a relation between the structure of the karyotype and the geographical distribution of the species. These relations are especially clear for the genus Macaca, but are also evident for the genus Pap*o. For the genus Macaca the differences of the karyotypes seem to follow longitudinally and latitudinally the geographic distribution of the different species. The graph of Figure 1 in fact perfectly overlaps the distribution of the different species. If we accept central Asia as the possible centre of evolutionary expansion of the genus, the ancestors of Mama seem to move and differentiate in three directions: the first and probably the earliest towards the west, the other two toward the north and south separately. Probably Mama sylvanaoriginates from the group migrated toward the west; M. fuscata from the group migrated towards the north and the group of the Celebes macacas (M. niger and M. maura) originate from the group migrated towards the south. This last observation, by the way, is in agreement with the hypothesis of Fooden (1969) which claimed that the celebesian macacas derive from M. netmstrina group. The long time of separation and the lack of contacts are the primary reasons of their differences in the karyotypes. On the other hand, the species living in continental habitats and more proximal from a geographic point of view have the karyotypes with low number of different chromosomes. The differences among the karyotypes of Papio hamadryas,P. sjhinx, Therco#ecus gel& and the karyotypes of Papio leucophaeus,P. cynoce~ha1u-s and P. papio are significant. It

484

J. SCHMAGER

Table 7

Numerical values of comparative moxphometricel analysis in most representative groups from genera studied (Macaca, Papio and Cercocebus) Chromosomes different in

Names of species comparated M. mulatta, M. assamensis, M. nemestrina, M. irur, M. speciosa with C. albigena, C. gale&s, C. torquatus M. mulatta, M. assamensis, M. nemestrina, M. iras, M. speciosa with P. leuc@haeus, P. cynocephalus, P. papi0 C. albigena, C. gale&us, C. torquatus with P. leucophaeus, P. CyMcephalus, P. papio

position of centromere (pair number)

. size and position of centromere (pair number)

Total number of different chromosomes

1,x

1

3, x

(17)

(12)

(5)

3

4, x

1

. size (pair number)

1

(1, 13920)

(49% 11, 12)

6

2, x (1,171

(5,6,9,

11, 12, 13)

8, X

(6)

1

9, x

(7)

seems probable that the differentiation of the different species of the genus Papio from an hypothetical center developed in various directions and probably had an adaptive character. Unfortunately, the karyological data for the key species of P. ursinus and P. anubis are not available at the moment. In any case, the present data seems to fit quite well with the taxonomic differences existing in this group of species. Three of the four species of Cercocebusexamined (C. albigena, C. gale&us and C. torquatus) Figure 4. Graphs of the connection between the karyotypes of more representative groups of species belonging to genera Macaca, Pa+ and Cercocebus. (M. mul. = Macaca mulatta, M. ass. = Macaca assamen&, M. nem. = Macaca nemestrka, M. ir. = Macaca iru.r, M. sp. = Macaca spaciosa, P. lcuc. = Papio leucoP. cyn. = Papi0 cynocc$!Zi P. pap. = Pafnk pa*, C. alb. = Cercocebusalbigena, C.gaL = Cercocebusgale&s, C. tor. = Cercocebus torquatus).

M. mul.

CYTOTAXONOMY

AND

GEOGRAPHICAL

DISTRIBUTION

485

have their karyotypes highly similar. The karyotype of C. aterimus appear to be quite different from them. Other data on morphology and ecology however seem to support such a diversification. In an attempt to have a synthetic relation among the three main groups of species a comparative analysis has been done for the most representative group of species (Table 7 and Figure 4). From such an analysis, it appears clear that the genera Macaca and Cercocebus are more strictly related between themselves than with Papio and this observation seems to be in agreement with the degree of specialization existing among them, the Macaca being in some way less specialized and more aboreal than baboons. The above results seem to prove a direct relation between geographical distribution or ecological adaptation and differentiation of the karyotypes in related species. This paper was written under the guidance of Professor A. B. Chiarelli during a period of four months spent at the Institute of Anthropology, University of Turin in a scholarship exchange programme with the Polish Ministry of Education. References Chiarelli, B. (1962). Comparative morphometric analysis of Primate chromosomes II. The chromosomes of the genera Macaca, Pa@, Theropithccus and Cercocebus. Caryologia 15,401-420. Chiarelli, B. (1966). Dati cariologici ed ibridologici per una revisione a livello sopragenerico della tassonomia delle scimie del vecchio mondo. Archirio per I’antr@ologia e l’ctnologia 46,105-109. Chiarelli, B. (1971). Comparative cytogenetics in Primates and its relationship with human genetics. In Com@rative Genetics in Monkeys, A@ and Man. New York, London: Academic Press. Chiarelli, B. (1972). Taxonomic Atlas of Living Primates. London: Academic Press. Fiedler, W. (1956). Ubersicht uber das System der Primates. In (H. Hofer, A. H. Schultz, D. Starck, Eds), Primatologiu. Base], New York: Karger. Fooden, J. (1969). Taxonomy and evolution of the Monkeys of Celebes. Bibl. Primatof. 10. Hill, W. C. Osman (1967). Taxonomy of the Baboon. In (H. Vagtborg, Ed.), The Baboon in Medical Research Vol. 11, pp. 3-l 1. Austin, London: University of Texas Press. Kummer, H. (1968). Social Organization of Hamadvas Baboons; a Field Study. Basel, New York: Karger. Napier, J. R. & Napier P. H. (1967). A Handbook of Lioing Primates. New York, London: Academic Press. Tappcn, N. C. (1960). Problems of distribution and adaption of the African monkeys. Current Anthrolropolo@ 1,91-120.