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Evolution of the sweetness receptor in primates. II. Gustatory responses of non-human primates to nine compounds known to be sweet in man.

The gustatory responses of nine compounds, namely glycine, D-phenylalanine, D-tryptophan, cyanosuosan, magapame, sucrononate, campame, cyclamate and superaspartame, all known as sweet in man, were studied in 41 species or subspecies of non-human primates, selected among Prosimii (Lemuridae and Lorisidae), Platyrrhini (Callitrichidae and Cebidae) and Catarrhini (Cercopithecidae, Hylobatidae and Pongidae). The first six compounds are generally sweet to all primates, which implies that they interact with the primate sweetness receptors essentially through constant recognition sites. Campame is sweet only to Cebidae and Catarrhini, cyclamate only to Catarrhini, superaspartame principally to Callitrichidae and Catarrhini, which implies that all these compounds interact with the receptors partly through variable recognition sites. From the present work, from other previous results (where notably it was observed that alitame is sweet to all primates, ampame only to Prosimii and Catarrhini, and aspartame only to Catarrhini), and from the multipoint attachment (MPA) theory of sweetness reception (as elaborated by Nofre and Tinti from a detailed study of structure-activity relationships of various sweeteners in man), it is inferred that the primate sweetness receptors are very likely made up of eight recognition sites, of which the first, second, third, fourth, seventh and eighth are constant, and the fifth and sixth variable. From these results and from the MPA theory, it is also inferred that the recognition sites of the primate sweetness receptors could be: Asp-1 or Glu-1, Lys-2, Asp-3 or Glu-3, Thr-4, X-5, X-6, Thr-7, Ser-8, where the variable recognition sites X-5 and X-6 would be: Ala-5 and Ala-6 for Callitrichidae, Ser-5 and Ala-6 for Cebidae, Ala-5 and Thr-6 for Prosimii, and Thr-5 and Thr-6 for Catarrhini. By using Tupaiidae (tree shrews) as a reference outgroup and by means of other structural and functional molecular considerations, it appears that Callitrichidae have retained the most primitive receptor among the four types of primate receptors. The possible taxonomic and phylogenetic implications of these findings are discussed.

Animals

Intergroup infant kidnapping in Hanuman langur.

The Hanuman langur, Presbytis entellus (Primates, Cercopithecidae, Colobinae), is under investigation in its wild state around Jodhpur, Rajasthan, India, since 1967. Jodhpur constitutes its extreme western range of distribution beyond which lies the Great Indian Desert. Infant transfer, infant killing [see Mohnot, 1971a, b], and intergroup infant kidnapping were frequently observed in this habitat. Details pertaining to intergroup infant kidnapping by allomothers of neighboring groups are presented here.

Agonistic Behavior

The primary structure of the mandrill (Mandrillus sphinx, Primates) hemoglobin.

The complete primary structure of the hemoglobin from the Mandrill (Mandrillus sphinx, Primates) is presented. This hemoglobin comprises two components in approximately equal amounts (HB I and Hb II). The alpha-chains differ in positions 5 (A3) and 9 (A7) having Ala and Asn in the alpha I-chains and Asp and His in the alpha II-chains. The beta-chains are identical. The components could be separated by DEAE-Sephacel chromatography. The globin chains were obtained by carboxymethylcellulose chromatography or high-performance liquid chromatography. The sequences were established by automatic liquid or gas phase Edman degradation of the chains and their tryptic peptides. The alpha-chains show 9 and 11 and the beta-chains 8 exchanges compared with the corresponding human chains, respectively. In the beta-chains one alpha 1/beta 1- and one alpha 1/beta 2-contact is substituted. A comparison of the primary structures of the Mandrill hemoglobin chains with those of other species of the Cercopithecidae family shows that Mandrillus sphinx should be placed between Cercopithecus and Macaca on one side and Papio, Theropithecus and Cercocebus on the other.

Amino Acid Sequence

Evolution of protamine P1 genes in primates.

Protamine P1 genes have been sequenced by PCR amplification and direct DNA sequencing from 9 primates representing 5 major families, Cebidae (new world monkeys), Cercopithecidae (old world monkeys), Hylobatidae (gibbons), Pongidae (gorilla, orangutan, and chimpanzee), and Hominidae (human). In this recently diverged group of primates these genes are clearly orthologous but very variable, both at the DNA level and in their expressed amino acid sequences. The rate of variation amongst the protamine P1s indicates that they are amongst the most rapidly diverging polypeptides studied. However, some regions are conserved both in primates and generally in other placental mammals. These are the 13 N-terminal residues (including a region of alternating serine and arginine residues (the motif SRSR, res. 10-13) susceptible to Ser phosphorylation), a tract of six Arg residues (res. 24-29) in the center of the molecule, and a six-residue region (RCCRRR, res. 39-44), consisting of a pair of cysteines flanked by arginines. Detailed consideration of nearest-neighbor matrices and trees based on maximum parsimony indicates that P1 genes from humans, gorillas, and chimpanzees are very similar. The amino acid and nucleotide differences between humans and gorillas are fewer than those between humans and chimpanzees. This finding is at variance with data from DNA-DNA hybridization and extensive globin and mitochondrial DNA sequences which place human and chimpanzee as closest relatives in the super family, Hominoidea. This may be related to the fact that protamine P1s are expressed in germ line rather than somatic cells.(ABSTRACT TRUNCATED AT 250 WORDS)

Amino Acid Sequence

Chromosomal evolution in primates: tentative phylogeny from Microcebus murinus (Prosimian) to man.

The karyotypes of more than 60 species of Primates are studied and compared, with the use of almost all existing banding techniques. There is a very close analogy of chromosome banding between the Simians studied and man. The quantitative or qualitative variations detected all involve the heterochromatin. It is very likely that all the euchromatin (nonvariable R and Q bands) is identical in all the species. Approximately 70% of the bands are common to the Simians and to the Lemurs (Prosimians). In the remaining 30%, technical difficulties prevented a valuable comparison, but this does not exclude the possibility that a complete analogy may exist. Thus, it is very likely that chromosomal evolutions of the Simians, and probably of all the Primates, has occurred without duplication or deficiency of the euchromatin. Approximately 150 rearrangements could be identified and related to the human chromosomes. The types of rearrangement vary from one group (suborder, family, genus) to another. For instance, Robertsonian translocations are preponderant among the Lemuridae (44/57), but are nonexistent among the Pongidae. Chromosome fissions are very frequent amng the Cercopithecidae (10/23), but were not found elsewhere, and pericentric inversions are preponderant in the evolution of Pongidae and man (17/28). This suggest that the chromosomal evolution may be directed by the genic constitution (favouring the occurrence of a particular type of rearrangement, by enzymatic reaction), by the chromosomal morphology (the probability that Robertsonian translocation will be formed depends at least partially on the number of acrocentrics), and by the reproductive behaviour of the animals. Reconstitution of the sequence of the chromosomal rearrangements allowed us to propose a fairly precise genealogy of many Primates, giving the positions of the Catarrhines, the Platyrrhines, and the Prosimians. It was also possible to reconstruct the karyotypes of ancestors that died out several dozen million years ago. The possible role of chromosomal rearrangements in evolution is discussed. It appears necessary to consider different categories of rearrangements separately, depending on their behaviour. The 'nonfavoured' rearrangements, such as pericentric inversions, need to occur in an isolated small population for implanting, by an equivalent of genic derivation. The 'favoured' rearrangements, e.g., Robertsonian translocations, may occur and diffuse in panmictic populations, and accumulate. Their role of gametic barrier could be much more progressive. For discrimination between these two categories, it was necessary to differentiate the selective advantage or disadvantage of the rearrangement itself. It was not possible to show that chromosomal rearrangements play a direct role in modification of the phenotype by position effect. Comparison of the rearrangement that have occurred during evolution and those detected in the human population shows a strong correlation for some of them...

Animals

DNA hybridization evidence of hominoid phylogeny: a reanalysis of the data.

Sibley and Ahlquist (1984, 1987) presented the results of a study of 514 DNA-DNA hybrids among the hominoids and Old World monkeys (Cercopithecidae). They concluded that the branching order of the living hominoid lineages, from oldest to most recent, was gibbons, orangutan, gorilla, chimpanzees, and human. Thus, a chimpanzee-human clade was indicated, rather than the chimpanzee-gorilla clade usually suggested from morphological evidence. The positions of the gibbon and orangutan branches in the phylogeny are supported by substantial evidence, but whether the chimpanzee lineage branched most recently from the human lineage or from the gorilla lineage remains controversial. The conclusions of Sibley and Ahlquist (1984, 1987) have been supported by several independent studies cited by Sibley and Ahlquist (1987), plus the DNA sequence data of Hayasaka et al. (1988), Miyamoto et al. (1988), Goodman et al. (1989, 1990), and the DNA-DNA hybridization data of Caccone and Powell (1989). The laboratory and data analysis methods have been criticized by Marks et al. (1988) and Sarich et al. (1989). In response to these critics, and for our own interests, we present a reanalysis of the Sibley and Ahlquist data, including a description of the corrections applied to the "raw counts." The validity of the laboratory methods is supported by the congruence of tree topology and delta values with those of Caccone and Powell (1989), although their tetraethylammonium chloride technique differs from the hydroxyapatite method in several respects. The utility of the T50H distance measure is indicated by its congruence with percent sequence divergence at least to delta T50H 30, as noted by Goodman et al. (1990). The Sibley and Ahlquist uncorrected data indicate that Pan is genetically closer to Homo than to Gorilla, but that Gorilla may be genetically closer to Pan than to Homo. Melting curves are presented for the pertinent experiments, plus one that includes representatives of most of the groups of living primates.

Animals

Macroevolutionary inferences from primate phylogeny.

We apply new statistical methods to a recent estimate of the phylogeny of all living primate species to test a range of models of cladogenesis. Null models in which probabilities of speciation and extinction do not differ among contemporaneous lineages are not consistent with the phylogeny. We present evidence that the net rate of cladogenesis (speciation rate minus extinction rate) increased in the lineage leading to the Cercopithecidae (Old World monkeys), and that there have been further increases in some lineages within that family. Such increases suggest the occurrence of clade selection, although we have not identified the selected trait or traits. There is no evidence that the net rate of cladogenesis is a function either of how many primate lineages are already present or of time. Intriguingly, three other clades--Strepsirhini, Platyrrhini and Hominoidea--appear to have had very similar rates of clade growth, in spite of their great biological differences.

Animals

Evolution of pro-protamine P2 genes in primates.

Protamines P1 and P2 form a family of small basic peptides that represent the major sperm proteins in placental mammals. In human and mouse protamine P2 is one of the most abundant sperm proteins. The protamine P2 gene codes for a P2 precursor, pro-P2 which is later processed by proteolytic cleavages in its N-terminal region to form the mature P2 protamines. We have used polymerase chain amplification to directly sequence the pro-P2 genes of the five major primate families: red howler (Alouatta seniculus) is a New World monkey (Cebidae); the two macaque species, Macaca mulatta and M. nemistrina are Old World monkeys (Cercopithecidae), the gibbon, Hylobates lar, represents one branch of the apes (Hylobatidae); the orangutan, Pongo pygmaeus, gorilla, Gorilla gorilla and two species of chimpanzee Pan paniscus and Pan troglodytes represent a second ape family (Pongidae). These pro-P2 genes are compared with that of human [Domenjoud, L., Nussbaum, G., Adham, I. M., Greeske, G. & Engel, W. (1990) Genomics 8, 127-133]. The overall size and organization of the genes are conserved within the group. The mean length of pro-P2 is 101 residues, with an increase to 102 in M. nemistrina and a decrease to 99 residues in red howler (A. seniculus). In gorilla and red howler one of two 79-bp tandem repeats that occurs 3' of the gene is deleted. Of the 101 deduced amino acids examined, an amino acid change occurs in one or more primates at 45 positions. Considering only the most recently diverged group, the human/gorilla/chimpanzee clade, this represents a very high mutation rate of 0.99 changes/100 sites in 10(6) years. This rapid mutation rate is characteristic of both members of the protamine gene family, P1 and P2. Consideration of the variable nature of the sequences at the multiple sites of proteolysis during the processing of the pro-P2 indicates either that there are several processing enzymes of differing specificities, or more likely that the folded structure of the pro-P2 limits accessibility of a non-specific protease to certain exposed sites.

Alouatta

Comparative RB1 gene mapping in Homo sapiens, Pithecia pithecia, Macaca sylvana, and Cercopithecus aethiops tantalus.

The chromosomal localization of the gene for retinoblastoma (RB1), which has been mapped to band 13q14 in man, was studied by in situ hybridization on metaphase chromosomes of selected primates, including Pithecia pithecia, Macaca sylvana, and Cercopithecus aethiops tantalus. The results allowed us to determine the position of the bands homologous to human chromosome band 13q14 in these species. Hybridization analysis corroborated the results of previous studies that defined the chromosome homologous to human chromosome 13 (HSA 13) in these species. By comparing RB1 localizations and banding patterns, it is shown that the rearrangement separating HSA 13 from its homologous chromosome in Cercopithecidae is not a pericentric inversion, as suggested by earlier studies. Since the banding pattern and RB1 localization are not changed, the modification of the centromeric index is explained by a centromeric shift or by two inversions, one pericentric and one paracentric.

Animals

Scanning electron microscopy of baboon spermatozoa.

Ejaculated baboon sperm was observed by scanning electron microscopy. The plasma membrane was generally smooth except on the acrosome where it was probably slightly wrinkled. The head was short, oval, paddle-shaped and tapering at its anterior end. The anterior segment of the acrosome was surrounded by a marginal thickening; the postacrosomal region was limited anteriorly by the equatorial segment and caudally by the posterior ring. Subsurface structures were visible in the tail, such as the relatively long and regular helix of mitochondria in the middle piece and the columns and ribs of the sheath in the principal piece. The morphology and dimensions of the baboon sperm was compared with that of other Primates and found very close to that of other Cercopithecidae.

Acrosome

The taste responses in primates to the proteins thaumatin and monellin and their phylogenetic implications.

Electrophysiological and behavioural methods have been applied to 34 species of the primates and, for comparison, to the Madagascan hedgehog to determine their responses to the proteins thaumatin and monellin. These substances elicit an intensely sweet taste sensation in man. All Catarrhina prefer monellin to water. The responses of the Prosimii as well as those of the South American primates to monellin are different, some species show a reaction, other species are not sensitive. In the case of thaumatin neither the Prosimii--including Tupaia and Tarsius--nor the South American primates show any response to this protein. Only the Cercopithecidae, the Hylobatidae and the Pongidae respond to this protein like man and prefer this substance to water. This physiological aspect of taste constitutes a clear dichotomy within the order Primates. This capability to taste thaumatin probably developed as long as 38 million years ago.

Animals

Cytogenetic study of five species of Cercopithecus.

The G- and C-banded karyotypes of five species of Cercopithecus are reported. The chromosome numbers are: for C. ascanius katangae 2 n = 66 (XX); for C. petaurista petaurista 2 n = 66 (XY); for C. mona mona 2 n = 68 (XX); for C. pogonias grayi 2 n = 72 (XY) and for C. hamlyni 2 n = 64 (XY). We always found three types of chromosome: metacentric, sub-metacentric and acrocentric. The 'marker chromosomes' typical of the Cercopithecidae are of the last type. The karyotype of C. pogonias grayi shows a characteristic pair of acrocentric autosomes which is again found in the hybrid karyotypes.

Animals

Physiologic measures of nonhuman primates during physical restraint and chemical immobilization.

The arterial acid-base balance and other selected physiologic measures of physically restrained and chemically immobilized nonhuman primates from the families Callithricidae, Cebidae, Cercopithecidae, and Pongidae were compared. The physically restrained primates had significantly lower pH, pCO2, and base excess values, but they had significantly higher pO2 values, rectal temperatures, and pulse and respiration rates. Of 56 physically restrained primates, 30 (54%) experienced severe metabolic acidosis, with pH values less than 7.2; 15 (27% of total) had pH values less than 7.1. Two types of behavior were observed during the physical restraint of golden marmosets. Some of the marmosets were excited during restraint, with a great deal of struggling and vocalizing. The other marmosets were quiet and calm, with minimal struggling. The excited group had significantly lower pH, pCO2, and base excess values, but significantly higher pO2 values, rectal temperatures, and pulse and respiration rates. Primates immobilized with ketamine or tiletaminezolazepam had a near normal acid-base balance and were handled more easily than the physically restrained animals.

Animals

[Role of chromosomes in evolution: a new interpretation].

The number of possible meiotic segregations of paternal and maternal chromosomes is 2N (N = haploid chromosome number). In eutherian Mammals, where large variations of N exist, 2N may be very different in related species, genes, or families. For instance, in Cercopithecidae, species with the highest value (N = 36) make 2(15) = 32,768 more gametic chromosome combinations than those with the lowest value (N = 21). It is also shown that the number of chiasmata varies from species to species and is proportional to the haploid number of arms NF/2 of the karyotype. Thus, increase or decrease of both N and NF/2, often concomitant, both increase or decrease genetic mixing. The chromosomal phylogeny of Primates, Carnivora and Rodentia shows that pure dichotomic evolution is rare, at contrast with populational (non dichotomic) evolution which seems most frequent. In these Mammals, the few examples of dichotomic evolution are observed in groups with low values of N and NF/2. It is concluded that dichotomic evolution, which should be favoured by the transmission of groups of linked mutant alleles, is prevented, in most instances, by the high recombination rate in karyotypes with high values of N and NF/2. Thus the mode of speciation would depend on karyotype modifications by long term effects on population genetics, in addition to the immediate effects of gametic barriers due to chromosomal rearrangements in the heterozygous state.

Alleles

Spermiation and epididymal maturation of spermatozoa in the bonnet macaque (Macaca radiata) as viewed by scanning electron microscopy.

Spermiation and epididymal maturation of spermatozoa were studied in the bonnet monkey (Macaca radiata) by light and scanning electron microscopy. The morphology, location, and release of residual body were observed during spermiation. Along the epididymal duct, the shape of spermatozoa changed, the constriction at the anulus disappeared, the marginal thickening diminished in length, and the cytoplasmic droplet regressed and moved toward the posterior end of the middle piece. Mature spermatozoa were very similar to those of other Cercopithecidae, and they showed a forward motility and a drop in eosin stainability.

Animals

Phylogenetic development of brain and brain sulci in primates.

The purpose of this study was to investigate the phylogenetic development of the cerebrum and cerebral sulcus in primates. The species selected were Macacus, Hylobates, Pan and Homo sapiens. These samples are classified as old world monkeys (Cercopithecidae), anthropoid apes (Pongidae), and Man (Hominidae). Although these four species divided up and went their separate ways from about the Oligocene era, the pattern of the cerebral sulci is similar. Of various cerebral sulci, the cingulate and calcarine sulci were selected, because they run on the medial surface of the cerebrum. The length of these sulci and fronto-occipital (FO) length were measured by a "cotton-thread" method. With the increase of size (FO-length) and weight of the brain, these sulci became longer, but there were no significant differences in the ratio of the calcarine sulcus to the FO-length among these four species. On the contrary, the ratio of the cingulate sulcus to the FO-length in Pan and Homo sapiens was significantly higher than in the other species, indicating that this ratio becomes higher with the phylogenetic development. The results of the present study suggest that the ratios of these sulci to the FO-length can be used as good indices to assess the degree of the phylogenetic development of the brain.

Animals

Brief communication: new primate remains from the Miocene of Namibia, southern Africa.

Miocene primates from southern Africa are extremely rare. For this reason we wish to place on record several interesting new fossil primate specimens recently recovered from the Miocene sites of Berg Aukas and Harasib in the Otavi Mountain region of northern Namibia. The new finds consist of a virtually complete atlas vertebra from Berg Aukas attributable to the hominoid Otavipithecus namibiensis and two teeth and four postcranial fragments from Harasib referrable to Cercopithecoidea. The atlas vertebra exhibits anatomical characteristics intermediate between those of modern cercopithecoids and hominoids which may be indicative of a transition from pronograde to orthograde postures. The cercopithecoid remains show that the earliest Old World monkeys known from southern Africa were small, approximately the size of vervet monkeys. These new specimens are important because they provide the first evidence relating to possible positional behaviors of Otavipithecus and the earliest fossil record of cercopithecoids from southern Africa.

Animals

Skull of Catopithecus browni, an early tertiary catarrhine.

Fossil crania from quarry L-41, Fayum, Egypt, representing Catopithecus browni, a primate similar in size to callitrichids but with a catarrhine dental formula, provide the geologically earliest record of an anthropoidean skull. Catopithecus had postorbital closure developed to the stage seen in extant anthropoideans, with direct contact between zygomatic plate and maxillary tuber, isolating an anterior orbital fissure from the inferior orbital fissure. The auditory region also resembles that of later anthropoideans: The posterior carotid foramen is placed adjacent to the jugular fossa; a large promontory canal crosses the promontorium; and the annular ectotympanic is fused ventrally to the bulla. The incisors and canines show an assemblage of features found only among modern anthropoideans and adapoids. The face is characterized by a relatively deep maxilla, broad ascending wing of the premaxilla, and long nasal bones, yielding a moderate muzzle similar to that of Aegyptopithecus. The small braincase bears an anteriorly broad frontal trigon and a posteriorly developed sagittal crest. The mandibular symphysis is unfused even in mature adults. The encephalization quotient (EQ) probably falls within the range of Eocene prosimians, much lower than the EQs of Neogene anthropoideans.

Animals