'How would you calibrate a molecular clock for the phylogeny of Hylobatidae and Hominidae, and what would the results be? What does the fossil record have to say about

it?'

By: Roya Shariati The Australian National University (ANU)

phylogenetic relationships among these four major groups are still unknown. Most previous studies have been based on morphology, vocalization, electrophoretic protein evidence, and karotyping and have differed in their conclusions (Bruce and Ayala, 1979; Creel and Preuschoft, 1984; Geissmann, 1993, 2001; Groves, 1972; Haimoff et al., 1982; Liu et al., 1987; Shafer, 1986).

Although the monophyly of the gibbons (family Hylobatidae) is widely accepted, this is not the case for the taxonomy adopted within the family

.In early studies on gibbon systematics, the Hylobatidae were grouped into two distinct genera, including the siamang (Symphalangus)

on the one hand and all the remaining gibbons (Hylobates) on the other (e.g., Napier and Napier, 1967; Schultz, 1933; Simonetta, 1957). When gibbons were studied in more detail,

however, it became clear that four, not two, major hylobatid divisions needed to be recognized.

These groups are generally accepted now as four distinct subgenera (i.e., Symphalangus, Nomascus, Bunopithecus, and Hylobates)

Therefore determined the DNA sequence of the complete mitochondrial control region and adjacent phenylalanine- tRNA (Phe-tRNA) of the four gibbon subgenera with the intention of :

1-resolving the evolutionary relationships between the subgenera and

2-comparing the distances between them with those between the great ape genera Homo and Pan. (Garza and Woodruff, 1992; Hall et al., 1998; Hayashi et al., 1995; Zehr, 1999; Zhang, 1997).

Even the use of molecular techniques based mainly on mitochondrial DNA sequences was not able to resolve the evolutionary relationships among the gibbon subgenera Furthermore,

Most molecular studies did not include the subgenus Bunopithecus and therefore presented an incomplete view on gibbon evolution.

The mitochondrial control region is known to evolve faster than other parts of mtDNA and may therefore be more suited to resolve a radiation which evolved over a short time span than sequences used in previous studies (Garza and Woodruff, 1992; Hall et al., 1998)

A New Generic Name for the Hoolock Gibbon (Hylobatidae)Alan Mootnick1 and Colin Groves

The generic nomen Bunopithecus is not applicable to hoolock gibbons. Groves (1968),

The concolor gibbons (formerly regarded simply as a species of Hylobates: H. concolor) were at least as different from Hylobates and Symphalangus as they were from each other.

Each subgenus has a distinctive karyotype. The type of Bunopithecus sericu s is outside the range of modern Hylobatidae in its

dental characters. The anterior fovea is much larger and less sharply demarcated in general, but with

a larger mesial crest; the entoconid is reduced; the hypoconulid is very large the wide central basin so characteristic of modern gibbons is undeveloped and

encroached on by the surrounding cusps and grooves (Groves 2004), .

Five gibbon species representing the four major groups within the Hylobatidae clade, Hylobates, Hoolock (Bunopithecus),Symphalangus, and Nomascus, were studied. All study animals or their parents were identified by us using fur coloration and vocal characteristicsas described in Geissmann (1995).

OntogenyGibbons produce single offspring; twins are

very rare (Dal Pra & Geissmann, 1994; Dielentheis et al., 1991; Geissmann, 1989).

Gibbon birth weights (mean ± standard deviations) are 406±55 g (n=7)

for the genus Hylobates, 487±87 g (n=3)

for Nomascus, and 551±88 g for Symphalangus (Geissmann & Orgeldinger, 1995).

The differences in birth weights between the genera parallel those observed in adult body weights.

No birth weights are available for Hoolock but, to judge by adult body weights, those can be expected be similar to the birth weights of Nomascus. Gestation length in all gibbons appears to be around 7 months (Geissmann, 1991), but no data are available for Hoolock. 

Genetic Variances

Evolutionary shaping of the human α2- α1-globin duplication units by retroposition of Alu family repeats and

by simple DNA deletion events. The proposed scheme of evolution has been deduced from sequence comparison of the duplication units between human and gibbon.

The ancestral unit consisted of blocks X, I, IV, II, Y, and Z.

The evolutionary origin of block III is uncertain at the present time.

It could belong to the ancestral unit, but was deleted from the α2-, but not α1-, globin unit. Alternatively, it could have been inserted into the α1-globin unit after the duplication event.

Like other hominoids, gibbons exhibit relatively long pre-adult developmental phases

After tandem duplication, independent retroposition of different Alu family repeats into the adult α-globin locus occurred.

Of the four depicted repeats, Alu1, Alu2, and Alu3 were inserted in the human/gibbon ancestor, with the insertion timing of Alu3 as early as prior to the separation of gibbon/human from the Old World monkeys (9, 14).

 Alu4 is present in the gibbon lineage, prior to or after the human/gibbon

divergence is unknown, since the DNA region containing its

insertion site has been deleted from the human genome.

DNA was extracted from periphereal blood lymphocytes and hair samples (H. hoolock) by the standard methods outlined in Sambrook et al. (1989) and Walsh et al. (1991), respectively. The complete mitochondrial control region and adjacent Phe-tRNA from one individual each of H. (Bunopithecus) hoolock, H. (Nomascus) leucogenys leucogenys, H. (Nomascus) gabriellae, and H. (Symphalangus) syndactylus and two individuals of H. (Hylobates) lar were PCR-amplified (Saiki et al., 1988) with the oligonucleotide primers L16007(59CCCAAAGCTAAAATTCTAA-39) and H00651 (59-TAACTGCAGAAGGCTAGGACCAAACCT- 39) According to Kocher et al. (1989), with H and L designating the heavy- and light-strand sequences of the mitochondrial genome and the numbers indicating the 39 end of the primers according to the human reference sequence (Anderson et al., 1981).

homo/1-954 CCTGAGTTGTAAAAAACTCCAGTTGACAC..AAAATAGACTACGAAAGTGGCTTTAACAT

gorilla/1-949 CCTGAGTTGTAAAAAACTCCAGCTGATAT..AAAATAAACTACGAAAGTGGCTTTAATAT

chimp/1-949 CCTGAGTTGTAAAAAACTCCAGCTGATAC..AAAATAAACTACGAAAGTGGCTTTAACAC

bonono/1-950 CCTGAGTTGTAAAAAACTCCAGCTGATAC..AAAATAAACTACGAAAGTGGCTTTAACAC

pongo/1-953 CCTGAGTTGTAGAAAACTTAAGTTAATAC..AAAATAAACTACGAAAGTGGCTTTAATAT

gibbon/1-951 TCCAAGTCGTAAAAAACTCTGGCTGCTAT..AAAATAAACTACGAAAGTGGCTTTAACAC

macaque/1-946 TCTAAACTGT..AAAACCCTAGCTGATGT..AAAATAAACTACGAAAGTGGCTTTAAAGC

monkey/1-958 ACTAAGTTGTGGAAAACTCCAGTTATAGT..GAAATACCCTACGAAAGTGGCTTTAATAT

Considering the fast pace of sequence evolution pertaining to the mitochondrial control region,

Only great ape sequences were taken into account for the sequence comparisons and phylogenetic analyses. The gorilla (Gorilla gorilla, NC001645) and orang-utan (Pongo pygmaeus, NC001646) (Horai et al., 1995)

Sequences were excluded from the analyses since both of the sequences exhibit a major deletion in the mitochondrial control region.

Thus, the herein determined sequences were compared with the homologous sequences obtained from human (Homo sapiens, NC001807) (Anderson et al., 1981), pygmy chimpanzee (Pan paniscus, NC001644) (Horai et al., 1995), and common chimpanzee (Pan troglodytes, X93335) (Arnason et al., 1996).

Phylogenetic Analyses

The expected monophylies of both the Homo–Pan and the gibbon clades are supported by bootstrap values of 100%.

The Hylobatidae, Nomascus is the most basal group, followed by Symphalangus, whereas Bunopithecus and Hylobates were the last to diverge.

Nomascus as the deepest split is supported by high bootstrap values in all three tree reconstruction methods used.

Results about the relationships among Bunopithecus, Hylobates, and Symphalangus are contradictive; whereas maximum likelihood and neighbor-joining link Bunopithecus and Hylobates, maximum-parsimony groups Bunopithecus with Symphalangus.

Pure observed sequence distances and not taking different generation times into account,

It is obvious that the distances among the four gibbon subgenera are in the same range as those between Homo and Pan, or even higher.

The uncorrected average distances are 10.3% between Hylobates and Bunopithecus, 10.6% between Symphalangus and the Bunopithecus–Hylobates clade, and 12.8% between Nomascus and the other three subgenera.

In contrast, the distance between Homo and Pan is only 9.6%. Based on these findings, it would be justified to elevate all four gibbon subgenera to genus rank.

The data depict evolutionary relationships among the gibbon genera that are supported by high bootstrap values.

However, more extensive stretches of mitochondrial and nuclear DNA may need to be sequenced to definitively establish the branching order of the four gibbon clades.

Times of catarrhine divergences in million years before present

The monophyly of the hylobatids and their basal position within the phylogeny of living Hominoidea are well established top Figure.

The monophyly of the group consisting of the African apes (genera Pan and Gorilla) and humans (Homo), but excluding the Asian orang-utans (Pongo), is also well supported.

The term "great apes" does not represent a systematic unit. It is often used to represent a group consisting of the African apes and the orang-utans, but excluding humans. These apes have traditionally been united in the family "Pongidae".

This grouping is based on similarity.Humans are more closely related to some of its members (i.e. the African apes) than to its other members (i.e. the Asian orang-utans), the great apes do not represent a monophyletic group.

In 1967 molecular differences among the hominoids were transferred to divergence times by Sarich and Wilson,

‘‘.If man and Old World monkeys last shared a common ancestor 30 million years ago, then man and African apes shared a common ancestor 5 million years ago (Sarich and Wilson).

The original arguments for recent hominoid divergences have been supported in other studies applying local primate calibration points: the split between Platyrrhini (New World monkeys) and Catarrhini (Old World monkeys, great apes, and Homo) set at 35–40 MYBP (Goodman et al. 1998), the split between Cercopithecoidea and Hominoidea set at 30 MYBP or 25 MYBP (Porter et al. 1997),

and that between Pongo and the lineage leading to Gorilla/Pan/Homo set at 14–17 MYBP (Sibley and Ahlquist 1987; Adachi and Hasegawa1995.

Characteristics

Family Hylobatidae

Genus: Hylobates Small or dwarf gibbons, lar group

Genus: Hoolock Hoolocks

Genus: Nomascus Crested gibbons, concolor group

Genus: Symphalangus Siamangs

Family Hominidae

Genus: Homo Humans

Genus: Gorilla Gorillas

Genus: Pan Chimpanzees

Genus: Pongo Orangutans

1. The Hominoidea share several primitive characteristics of catarrhine primates with their sister group, the Cercopithecoidea ("Old World monkeys"), including:

2. As in all catarrhine primates, the ektotympanic ring is drawn out to form an external bony auditory meatus.

3. The bony palate and the nasal apertures are relatively broad relativ broad.

4. The dental formula in hominoids is the same as in all other catarrhine primates: 2.1.2.3 / 2.1.2.3.

Photograph of buff cheeked gibbon courtesy of Alan R. Thomson,

copyright The Royal Zoological Society of Scotland.

1. Skull of Hylobates hoolock, white-browed or hoolock gibbon, from South East Asia – Bangladesh, Burma, Assam.

2. Skull of Pongo pygmaeus, the Bornean orang-utan.

3. Skulls of male and female Gorilla gorilla, the Western gorilla, from Equatorial Africa.

4. Skull of Pan troglodytes, the common chimpanzee, from West and Central Africa.

5. Skulls of Homo sapiens, a human being; one skull prepared to show brain case.

Gibbon skulls (1) are relatively light and there is little difference in the skulls of males and females, they have the largest canines, relatively speaking, of all apes.

The skulls of the heavier great apes and humans (2-5) are robust to protect the brain from damage.

Orangutan skulls (2) slope markedly backwards, unlike the skulls of gorillas (3) and chimpanzees (4).

The skulls of male gorillas (3) and orangutans are much more heavily built than the females and also have substantial midline (sagittal) and neck (nuchal) crests to provide additional attachment surfaces for neck muscles.

The human cranium (5) is smooth-domed and lacks crests; the brain cavity is very large.

The skull of the chimpanzee (4) is very like a human skull .

Molar pattern: Living homioid primates exhibit a simple Y5-pattern in the lower dentition; the upper molars have 4 cusps with a diagonal crest (crista obliqua). Compared to the Cercopithecoidea, the Hominoidea exhibit a more primitive molar pattern without bilophodont shearing crests. The lower molars are distinguished by an enlarged talonid section and by 5 main cusps. If viewed from the lingual side, the grooves between the cusps take a y-shaped form, which explains the name Y5-pattern.The upper molars are of a more or less square shape. They are derived from the hypothetical primitve molar pattern of anthropoid primates in that the originally three-cusped tooth was "upgraded" to a four-cusped tooth through the enlargement of a minor supplementary cusp (hypoconus), which, however, remained separated from the rest of the occusal surface by an oblique shearing crest, the crista obliqua.

The anterior lower premolar varies in its form from a long shearing blade in gibbons (sectorial front dentition) to a two-cusped "molarised" tooth in humans. Most hominoid primates have relatively broad incisors. The canines are more variable than those of the Cercopithecoidea, both in their shape and in the extent of their sexual dimorphism.

The thorax is broadened and the vertebral column is slightly shifted away from a dorsal position towards the center of the thoracal cavity. The latter characteristic is most strongly developed in humans.The scapulae are shifted away from a position lateral of the thorax to a more dorsal position, and the claviculae, which connect with the scapulae, are elongated to match the new position of the latter

Homo H 72 Chlorocebus Ce 83 Papio Ce 95-97

Presbytis Co 75-78 Miopithecus Ce 83 Theropithecus Ce 100

Lophocebus Ce 78 Cercocebus Ce 83-84 Pan H 102-106

Colobus Co 78-79 Macaca Ce 84-100

Gorilla H 116

Cercopithecus Ce 79-86 Piliocolobus Co 87 Hylobates H 126-130

Procolobus Co 80 Erythrocebus Ce 92 Hoolock H 129

Semnopithecus Co 80-83 Nasalis Co 94 Pongo H 139

Trachypithecus Co 82-83 Pygathrix Co 95 Nomascus H 140

Allenopithecus Ce 83 Mandrillus Ce 95 Symphalangus H 147

Intermembral index = (humerus length + radius length) x 100 / (femur length + tibia length); Abbreviations: Ce=Cercopithecinae, Co=Colobinae, H=Hominoidea

Various genera of the Catarrhini, sorted by their intermembral indices (indices from Fleagle, 1999)

 Some vertebral numbers of selected members of the Anthropoidea (average values, after Schultz, 1961).

Ventral view of the rump skeleton of an adult female macaque compared to selected members of the Hominoidea, all brought to the same size (after Schultz, 1969, p. 78).

· Ischial callosities reduced in size (Hylobatidae) or absent· Femur with broad condyles.· Feet with robust big toe (Hallux), excpet in orangutans (genus Pongo

Hominoids also differ from cercopithecoid primates in several behavioral and ecological characteristics. It is often unknown, however, whether these are derived hominoid traits or pimitive anthropoid features.

In general (relative to their body size) hominoid primates exhibit a longer gestation period and a longer maturation period (i.e. the time until they reach sexual maturity).

Hominoid social structure is normally organized around matrilines, and the females don't usually stay in their natal groups. When forageing for food, several species appear to adopt a fission-fusion-organisation.

dwarf gibbons (genus Hylobates) 5-7 kg, hoolocks (Hoolock) and crested gibbons (Nomascus) 7-10 kg, siamangs (Symphalangus) 10-12 kg. There is virtually no sexual dimorphism in either the canine teeth or body size.relatively simple molar teeth with low, rounded cusps, sectorial front teeth and long, dagger like canines in both sexes· short snout, large orbits, relatively wide inter-orbital distance, globular braincase, shallow mandibula with broad ascending ramus

Body Size

o Thescientificnames Symphalangus and syndactylus both mean 'fingers that have grown together'.

o In the feet of the siamang, the second and third digit are actually joined by connective tissue at the base. This condition is known as syndactyly.

o It occasionally occurs in other gibbon species, as well, but is quite rare and the connection is usually less extensive.

o Gibbons are the only apes, that consistently exhibit ischial callosities. In addition, the females have noticeable sexual swellings, during which the Labiae majorae undergo cyclic changes in their colour and form.

Locomotion

1. In order to prevent the whole body from rotating with each step during bipedal walking, a counter-rotation of the upper body in the opposite direction is needed.

2. In humans, this counter-rotation this takes place in the chest area. In gibbons, however, this counter-rotation occurs in the hip, which makes the movement look more awkward.

3. The complete upright posture observed in humans is possible because of two curvatures in the spinal column, the so-called lordoses. This brings the body's center of gravity directly over the bearing area of the feet.

4. The gibbon lacks these curvatures of the spinal column and achieves a similar result be bending both his hip-joint and his knee joints when standing upright .

5. The bended knees further help to cushion the forces of forward locomotion during walking, whereas humans resolve this by the rolling motion of their feet.

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Bruce, E. J., and Ayala, F. J. (1979). Phylogenetic relationships between man and the apes: Electrophoretic evidence. Evolution 33: 1040–1056. Haimoff, E. H., Chivers, D. J., Gittins, S. P., and Whitten, A. J. (1982). A phylogeny of gibbons (Hylobates spp.) based on morphological and behavioural characters. Folia Primatol. 39: 213–237. Geissmann, T. (2002). Taxonomy and evolution of gibbons. Evol. Anthrop. Suppl. 1: 28–31.

 

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Groves, C. P. (2001). Primate Taxonomy.Washington: Smithsonian Institution Press.

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Napier, J. R., and Napier, P. H. (1967). “A Handbook of Living Primates,” Academic Press, London.Schultz, A. H. (1933). Observations on the growth, classification and evolutionary specialization of gibbons and siamangs. Human Biol. 5: 212–255 and 385–428. Simonetta, A. (1957). Catalogo e sinonimia annotata degli ominoidi fossili ed attuali (1758–1955). Atti Soc. Toscana Sci. Nat. Pisa Ser. B 64: 53–113.

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