Ontogeny and homoplasy in the papionin monkey face

SUMMARY Recent molecular research has provided a consistent estimate of phylogeny for the living papionin monkeys (Cercocebus, Lophocebus, Macaca, Mandrillus, Papio, and Theropithecus). This phylogeny differs from morphological phylogenies regarding the relationships of the mangabeys (Cercocebus and Lophocebus) and baboons (Mandrillus, Papio, and Theropithecus). Under the likely assumption that the molecular estimate is correct, the incongruence between the molecular and morphological data sets indicates that the latter include numerous homoplasies. Knowledge of how these homoplasies emerge through development is important for understanding the morphological evolution of the living papionins, and also for reconstructing the phylogenetic relationships and adaptations of their fossil relatives. Accordingly, we have used geometric morphometric techniques and the molecular phylogeny to investigate the ontogeny of a key area of morphological homoplasy in papionins, the face. Two analyses were carried out. The first compared allometric vectors of Cercocebus, Lophocebus, Macaca, Mandrillus, and Papio to determine which of the facial resemblances among the genera are homoplasic and which are plesiomorphic. The second analysis focused on early post‐natal facial form in order to establish whether the facial homoplasies exhibited by the adult papionins are to some degree present early in the post‐natal period or whether they develop only later in ontogeny. The results of our analyses go some way to resolving the debate over which papionin genera display homoplasic facial similarities. They strongly suggest that the homoplasic facial similarities are exhibited by Mandrillus and Papio and not by Cercocebus and Lophocebus, which share the putative primitive state with Macaca. Our results also indicate that Mandrillus and Papio achieve their homoplasic similarities in facial form not through simple extension of the ancestral allometric trajectory but through a combination of an extension of allometry into larger size ranges and a change in direction of allometry away from the ancestral trajectory. Thus, the face of Mandrillus is not simply a hypermorphic version of the face of its sister taxon, Cercocebus, and the face of Papio is not merely a scaled‐up version of the face of its sister taxon, Lophocebus. Lastly, our results show that facial homoplasy is not restricted to adult papionins; it is also manifest in infant and juvenile papionins. This suggests that the homoplasic facial similarities between Mandrillus and Papio are unlikely to be a result of sexual selection.     

Estimation of body weights from craniometric variables in baboons

Body weights of adult baboons (genera Papio, Mandrillus, and Theropithecus) were gathered from notes of collectors and museum records. However, these data were insufficient to establish mean body weights for all baboon groups. Thus, log cube roots of mean body weights were regressed as functions of the logs of several cranial and dental variables. The resulting least squares regression coefficients were used to estimate weights for 503 adult baboons from cranial measurements. The ability of the various regression functions to assess baboon body weight was determined by comparing reported and estimated mean and individual body weights. The best estimator of baboon body weights was the function derived from the factor scores of a principal components analysis of seven craniometric variables regressed on body weight. However, each of these craniometric variables singly was nearly as precise an estimator of body weight as the multivariate combination of all seven. Other measurements such as dental dimensions and foramen magnum area estimated weight less accurately. Body weight estimates derived from the regression analyses coupled with museum and literature records allowed an assessment of size relationships among all baboon groups.     

A reassessment of the taxonomic status and phyletic relationships of Papio baringensis and Papio quadratirostris (Primates: Cercopithecidae)

Comparison of the skulls of Papio baringensis Leakey 1969 from the Chemeron Formation and P. quadratirostris Iwamoto 1982 from the Usno Formation with those of Theropithecus gelada, T. brumpti, T. darti, T. oswaldi, and several species of Papio indicate that the species from Chemeron and Usno exhibit all, or most, respectively, of the shared derived characters of Theropithecus. We propose that they be removed from Papio and placed in Theropithecus as T. baringensis and T. quadratirostris. Comparison of the specimens of T. baringensis and T. quadratirostris with those of T. brumpti indicate that the former two species have some of the derived characters of T. brumpti but are primitive in others. We propose that the three species form the following phyletic lineage: T. baringensis-T. quadratirostris-T. brumpti. With these referrals, there are now six species of the genus Theropithecus. Based on geologic grounds, the specimens from Chemeron are about 4.0 million years (m.y.), that from Usno between 3.3 and 3.4 m.y., and those of T. brumpti between 2.0 and 2.8 m.y. in age. We also show that the most complete specimen of Papio sp. nov. from Olduval Gorge belongs to T. oswaldi. With the removal of these specimens from Papio, the East African fossil record of this genus, apart from isolated teeth, comprises only 21 specimens, while that of Theropithecus comprises at least 300 specimens.     

Nuclear gene trees and the phylogenetic relationships of the mangabeys (Primates: Papionini)

Phylogenetic relationships of mangabeys within the Old World monkey tribe Papionini are inferred from analyses of nuclear DNA sequences from five unlinked loci. The following conclusions are strongly supported, based on congruence among trees derived for the five separate gene regions: (1) mangabeys are polyphyletic within the Papionini; (2) Cercocebus is the sister taxon to the genus Mandrillus; and (3) Lophocebus belongs to a clade with Papio and Theropithecus, with Papio as its most likely sister taxon. Morphologically based phylogenies positing mangabey monophyly were evaluated by mapping the sequences for each locus on these trees. The data seem to fit these trees poorly in both maximum-parsimony and likelihood analyses. Incongruence among nuclear gene trees occurred in the interrelationships among Lophocebus, Papio, and Theropithecus. Several factors that may account for this incongruence are discussed, including sampling error, random lineage sorting, and introgression.      

Allometry, sexual dimorphism, and phylogeny: A cladistic analysis of extant African papionins using craniodental data

This study conducts a phylogenetic analysis of extant African papionin craniodental morphology, including both quantitative and qualitative characters. We use two different methods to control for allometry: the previously described narrow allometric coding method, and the general allometric coding method, introduced herein. The results of this study strongly suggest that African papionin phylogeny based on molecular systematics, and that based on morphology, are congruent and support a Cercocebus/Mandrillus clade as well as a Papio/Lophocebus/Theropithecus clade. In contrast to previous claims regarding papionin and, more broadly, primate craniodental data, this study finds that such data are a source of valuable phylogenetic information and removes the basis for considering hard tissue anatomy “unreliable” in phylogeny reconstruction. Among highly sexually dimorphic primates such as papionins, male morphologies appear to be particularly good sources of phylogenetic information. In addition, we argue that the male and female morphotypes should be analyzed separately and then added together in a concatenated matrix in future studies of sexually dimorphic taxa. Character transformation analyses identify a series of synapomorphies uniting the various papionin clades that, given a sufficient sample size, should potentially be useful in future morphological analyses, especially those involving fossil taxa.     

PHYLOGENETIC ANALYSES OF THE BRYOPSIDALES (ULVOPHYCEAE,CHLOROPHYTA) BASED ON RUBISCO LARGE SUBUNIT GENE SEQUENCES1

Current taxonomy of the Bryopsidales recognizes eight families; most of which are further categorized into two suborders, the Bryopsidineae and Halimedineae. This concept was supported by early molecular phylogenetic analyses based on rRNA sequence data, but subsequent cladistic analyses of morphological characters inferred monophyly in only the Halimedineae. These conflicting results prompted the current analysis of 32 taxa from this diverse group of green algae based on plastid‐encoded RUBISCO large subunit (rbcL) gene sequences. Results of these analyses suggested that the Halimedineae and Bryopsidineae are distinct monophyletic lineages. The families Bryopsidaceae, Caulerpaceae, Codiaceae, Derbesiaceae, and Halimediaceae were inferred as monophyletic, however the Udoteaceae was inferred as non‐monophyletic. The phylogenetic position of two taxa with uncertain subordinal affinity, Dichotomosiphon tuberosus Lawson and Pseudocodium floridanum Dawes & Mathieson, were also inferred. Pseudocodium was consistently placed within the halimedinean clade suggesting its inclusion into this suborder, however familial affinity was not resolved. D. tuberosus was the inferred sister taxon of the Halimedineae based on analyses of rbcL sequence data and thus a possible member of this suborder.     

Intergeneric hybrids of the lower (42-chromosome) monkey species of the Sukhumi monkey colony

A cytogenetic study has been carried out of 2 intergeneric hybrids between Papio and Macaca genera and 17 hybrids between Papio and Theropithecus genera, obtained at the Sukhumi monkey colony for the period since 1949 up to 1964. Intermediate or mosaic-intermediate heredity of the phenotypic features of the initial parental species are noted in all the hybrids.Hybrids between Macaca and Papio genera resembled baboons according to the body build and colour of eyes, but acoording to the form of head, face, hair colour, sexual skin and ischial callosities they resembled macaques. More or less domination of the gelade phenotype (head form, location of nostrils, saddle-like nose, hair colour, body build) is seen in the Papio × Theropithecus hybrids. At the same time, the structure of sexual skin and ischial callosities had an intermediate type between baboons and gelades. Instead of the sexual skin, characteristic of gelades, the appearance of a new feature (hair-free nipple fields up to 6 cm in diameter) has been noted on the chest of the hybrids. The carotype of the hybrids between Macaca, Papio and Theropithecus genera consists of 42 chromosomes, as in the initial species, the homologues of most pairs being significantly similar.The results of crossings and chromosome study allow one to conclude that African species—hamadryas baboons and gelades—are genetically closer to each other than Asian rhesus macaques and African hamadryas baboons, having been isolated from one another geographically for a long period of time. In this connection, intergeneric hybrids between Papio and Theropithecus genera are obtained more easily and the hybrid retains fertility unlike the non-fertile hybrid between macaques and baboons, which is obtained with difficulty.     

Associations between the drill (Mandrillus leucophaeus) and sympatric monkeys in Korup National Park,Cameroon

Studies of polyspecific associations among African forest primates have primarily focused on arboreal Cercopithecus and Procolobus/Colobus species. We examined the association frequency of the terrestrial drill (Mandrillus leucophaeus) with six sympatric monkey species in Korup National Park, Cameroon, testing reports that Mandrillus associations are infrequent and transient. We conducted 3,284 km of trail walks for 12 months (February–June 2006; July 2007 to January 2008), recording species composition in 612 primate clusters. Using a Markov chain Monte Carlo test, we compared the observed frequency of dyadic associations against null models of “no association.” A novel conservative statistical approach which addresses possible dependence of observations close in time was also used, further strengthening confidence in our findings. Drills associated with all monkeys throughout the study period, and were with at least one other species (range 1–5) in half of the encounters. The association frequency of drills with red‐capped mangabeys (Cercocebus torquatus) was greater than expected by chance, which is interesting given the morphological adaptation of the Mandrillus‐Cercocebus clade for the exploitation of the same dietary niche, hard seeds. The difference we observed in the use of forest strata by drills and mangabeys may reflect a strategy to reduce food competition while in association. The nature and duration of observed drill associations varied. Although some associations seemed to be chance encounters, others lasted for hours with the involved species foraging together. Am. J. Primatol. 73:127–134, 2011. © 2010 Wiley‐Liss, Inc.     

Bases génétiques de la spéciation et de la taxonomie chez les Babouins

This review gives a synthesis on the present knowledge on the use of several electrophoretic markers in examining speciation and taxonomy in baboons (genus Papio, Mendrillus and Theropithecus). In the various species studied, the amplitude of variation is small and the average rate of individual heterozygosity low; this seems partly due to the inbreeding which occurs within the groups. In these sub-populations, and when the frquencies are in equilibrium, it is possible to calculate the number of genetic migrants by generation between groups, which averages 3–18% according to species. The genetic distances between species allow one to establish in the genus Papio that the species P. hamadryas is the most differentiated and on the whole these species are comparable to geographical races of a polytypic species according to the measures obtained. Calculation of electrophoretic distances shows tht within Papio both P. papio and P. anubis are indistinguishable and that the three other species. P. cynocephalus, P. ursinus and P. hamadryas, diverge from this basic group. According to these criteria, both Mandrillus species diverge on the average of 30% of their genes, and according to the paleontological dates of divergence between Papio and Theropithacus, Papio would have appeared approximately 3.5 million years ago, a date in agreement with the information obtained from fossils. The electrophoretic study of inter-specific hybrids allows the intensity of the migratory flux betwen the different groups of Papio anubis and P. hanadryas in natural conditions to be calculated, and shows a partial inhibition of the paternal component of hybrids P. anubix × P. cynocephalus. It is concluded that two interesting research problems are the study of inbreeding in the different groups, and the influence of the genetic regulation in the evolution of various species. The evolution of different species within the group seems to constitute an excellent animal model from the diversification of fossils hominids during the Pleistocene epoch.     

Distances electrophorétiques entre les différentes espèces de babouins du genre Papio et le gelada Theropithecus

The time of separation of different species of Papio and of Theropithecus lineages is estimated from the results of electrophoretic examination of various enzymes in their red blood cells.     

Molecular phylogeny and divergence time of the water penny genus Eubrianax (Coleoptera: Psephenidae) in Japan

The phylogenetic relationships among the Japanese members of the genus Eubrianax (Coleoptera: Psephenidae) were examined using the mitochondrial cytochrome oxidase subunit I (COI) gene and nuclear 28S rRNA gene sequences. Based on the molecular phylogeny as well as morphological features, the species status of Eubrianax brunneicornis Nakane, 1952 was proposed. The phylogenetic analyses recovered monophyly of the previously proposed pellucidus species group with four Japanese species, whereas a single Japanese species of the granicollis group was included in the lineage of the ramicornis group with five Japanese species. The divergence times of the species were estimated by dating the phylogenetic tree against the fossil record and a molecular clock based on the COI gene. The divergence of the Japanese species was inferred to have occurred during the Pliocene epoch.     

Hominid and gelada baboon evolution: Agreement between molecular and fossil time scales

The time of origin of the hominid lineage has long been debated. Macromolecular studies have consistently shown genetic distances between living humans and African apes to be quite small. The molecular clock hypothesis proposes that the time of separation of these lineages is relatively recent (in the range of 4–8 million years ago) and not 15 million years or more ago as usually suggested. Three independent molecular comparisons yield a mean estimate of 4.6 million years for the hominid-African pongid divergence. The relationship of Theropithecusand Papiois a parallel case within Primates of two taxa which are quite similar at the molecular level, but which are usually thought to have separated relatively long ago. The two cases of seeming discordance between different lines of evidence are analogous. Each involves a speciation event which eventually resulted in one substantially derived lineage and one or more relatively unchanged lineages. In each case, claims of the antiquity of the divergence event extend to at least twice the age of the first certain appearance of the more derived lineage in the fossil record. Finally, in each case, the molecular clock model suggests a range of possible divergence times that overlaps with the first appearances of undoubted hominids and Theropithecusin the fossil record. This test involving paleontological evidence supports the molecular clock hypothesis.     

Genotypic and phenotypic diversity of cyanobacteria assigned to the genus <Emphasis Type="Italic">Phormidium</Emphasis> (Oscillatoriales) from different habitats and geographical sites

In this study, 30 strains of filamentous, non-heterocystous cyanobacteria from different habitats and different geographical regions assigned to diverse oscillatorian genera but here collectively referred to as members of the Phormidium group have been characterized using a polyphasic approach by comparing phenotypic and molecular characteristics. The phenotypic analysis dealt with cell and filament morphology, ultrastructure, phycoerythrin content, and complementary chromatic adaptation. The molecular phylogenetic analyses were based on sequences of the 16S rRNA gene and the adjacent intergenic transcribed spacer (ITS). The sequences were located on multiple branches of the inferred cyanobacterial 16S rRNA tree. For some, but not all, strains with identical 16S rDNA sequences, a higher level of discrimination was achieved by analyses of the less conserved ITS sequences. As shown for other cyanobacteria, no correlation was found between position of the strains in the phylogenetic tree and their geographic origin. Genetically similar strains originated from distant sites while other strains isolated from the same sampling site were in different phylogenetic clusters. Also the presence of phycoerythrin was not correlated with the strains’ position in the phylogenetic trees. In contrast, there was some correlation among inferred phylogenetic relationship, original environmental habitat, and morphology. Closely related strains came from similar ecosystems and shared the same morphological and ultrastructural features. Nevertheless, structural properties are insufficient in themselves for identification at the genus or species level since some phylogenetically distant members also showed similar morphological traits. Our results reconfirm that the Phormidium group is not phylogenetically coherent and requires revision.     

The relation of canine size to pattern and extent of attrition in baboons

For most genera of animals the association between dental morphology and diet is such that inferences concerning the diet can be made on the basis of the dentition alone. The canine is the one tooth that appears exempt from such generalisation and exhibits a wide range of variability of size and shape in all groups. In order to determine the effect of dimorphism of the canine on the dental apparatus, male and female specimens of Theropithecus and Papio baboons were examined. Occlusal relationships and dental pathology for 21 Theropithecus and 40 Papio skulls were recorded, and crown height measurements obtained for maxillary incisors, buccal and lingual molar cusps. Attrition was the most common and severe cause of abscess formation in older animals: the pattern of attrition differed in adult males and females, the latter showing more wear of the incisor and lingual molar cusps. Partial correlations for incisor, buccal and lingual molar cuspal crown height show a significant correlation between incisor and lingual cusp attrition in juveniles of both sexes and adult females (p < 0.01). Adult males show no correlation of attrition. It is proposed that the correlation of incisor and lingual molar cusp attrition is associated with anterior-posterior grinding movements, such as take place during incision, that the large canine present in the male limits such movements, the sharp blade-like canine being employed as a cutting tool. This use of the canine by reducing functional demands on other teeth, prolongs the utility of the dental apparatus, and hence the lifespan of its possessor.     

Integrated analysis for identifying Portulaca oleracea and its sub-species based on chloroplastic and nuclear DNA barcoding

The taxonomy of Portulaca oleracea has been considered as being complex since the aggregate is composed of many subspecies or a group of micro-species based on seed-coat characters, seed size, and chromosome number. In order to enlarge the background of the extent of genetic variability between and within Tunisian P. oleracea accessions, a combined morphological and molecular approach was adapted, in the present survey. The morphological analyses of the spontaneous Tunis population display high intra population variability characterized by two distinct morphotypes corresponding to the botanical forms (wild and cultivated plant). Furthermore, the molecular approach based on sequences data related to chloroplastic and ribosomal DNA, was used to understand this variability. The obtained results highlighted the greater molecular variability of this plant and allowed to segregate between morphotypes and genotypes of Portulaca. Mostly, this work shows the important contribution of DNA barcoding approach in resolving low-level-taxonomy problems to distinguish between natural populations and varieties.     

Phylogenetic Relationships Among Hypotrichous Ciliates Determined with the Macronuclear Gene Encoding the Large, Catalytic Subunit of DNA Polymerase α

The complete macronuclear DNA polymerase α gene, previously sequenced in Oxytricha nova, has been cloned from a genomic macronuclear library and sequenced for the hypotrich O. trifallax. Macronuclear DNA clones of DNA polymerase α encoding ∼1000 amino acids, or approximately two-thirds of the open reading frame, have been obtained by PCR and sequenced for Halteria grandinella, Holosticha species, Paraurostyla viridis, Pleurotricha lanceolata, Stylonychia lemnae Teller, Sty. mytilus, Uroleptus gallina, and Urostyla grandis. Phylogenetic relationships inferred from DNA polymerase α amino acid sequences have been used to clarify taxonomic relationships previously determined by morphology of the cell cortex. Hypotrich phylogenies based on DNA polymerase α amino acid sequences are incongruent with morphological and other molecular phylogenies. Based upon these data, we assert that, contrary to morphological data, O. nova and O. trifallax are different species, and we propose that the oligotrich Halteria grandinella be reclassified as a hypotrich. This work also extends the available data base of eukaryotic DNA polymerase α sequences, and suggests new amino acid sequence targets for mutagenesis experiments to continue the functional dissection of DNA pol α biochemistry at the molecular level. Received: 7 January 1997 / Accepted: 7 April 1997     

Macroevolutionary relationships of species of Drosophila melanogaster group based on mtDNA sequences

The phylogenetic relationships among the Drosophila melanogaster group species were analyzed using approximately 1700 nucleotide-long sequences of the mitochondrial DNA. Phylogenetic analysis was performed using this region consisting of a part of the cytochrome b (cytb) coding gene, the entire coding sequences of tRNA-Leu, tRNA-Ser and the first subunit of NADH dehydrogenase (NADH1), and a part of the 16S-rRNA gene. The study of these sequences showed that this region of mtDNA is very invariable, as regards with the type of the genes that it contains, as well as the order that they are located on it. The resulting phylogenetic trees reveal a topology that separates the species into three main ancestral lines, leading to the following subgroups: (a) ananassae subgroup, (b) montium subgroup, and (c) melanogaster and Oriental subgroups. The inferred topology complements and generally agrees with previously proposed classifications based on morphological and molecular data.     

Phylogenetic position of the house dust mite subfamily Guatemalichinae (Acariformes: Pyroglyphidae) based on integrated molecular and morphological analyses and different measures of support

Based on multilocus phylogenetic analyses (18S, 28S, EF1‐α, SRP54, HSP70, CO1, 10 860 nt aligned), we show that the house dust mite subfamily Guatemalichinae is nested within non‐onychalgine pyroglyphid mites and forms the sister group to the genus Sturnophagoides (bootstrap support 100, posterior probability 1.0). Because high bootstrap support values may be misleading in the presence of incongruence, we evaluate robustness of the Guatemalichinae+Sturnophagoides clade using: (1) internode certainty indices to estimate the frequency of conflicting bipartitions in maximum‐likelihood bootstrap trees, (ii) consensus networks to investigate conflict among different loci; and (iii) statistical hypothesis testing based on information theory, both multi‐scale and regular bootstrap. Results suggest that this grouping is very well supported given the data. The molecular analyses were integrated with detailed morphological study using scanning electron and light microscopy. We suggest that the subfamilial status of Guatemalichinae should be reconsidered, and this lineage should be placed within the subfamily Dermatophagoidinae. The latter subfamily is currently accepted in the literature as a monophyletic group but was here inferred as paraphyletic and was not supported by any morphological synapomorphy. The paraphyly involved the most species‐rich and medically important genus, Dermatophagoides. Our findings suggest the need for a comprehensive revision of the higher‐level relationships of pyroglyphid house dust mites using both DNA sequences and morphology coupled with a broad taxonomic sampling.     

Three novel species of Stemphylium from Sinkiang, China: their morphological and molecular characterization

Three new species of Stemphylium were isolated from diseased leaves of Luffa cylindrica, Lycium chinense and Cucumis melo growing in the Sinkiang province of Northwest China. Stemphylium luffae, S. lycii and S. cucumis are described by morphological and molecular phylogenetic analyses. The principal morphological characteristics of these three species are congruent with those of Stemphylium. They are distinguished from morphologically similar Stemphylium species based on characteristics of their conidia and conidiophores. In order to establish the molecular phylogenetic status of these species, DNA loci including the internal transcribed spacer (ITS) nuclear rDNA region and the glyceraldehyde-3-phosphate dehydrogenase (gpd) genes were amplified and sequenced. Phylogenetic analyses using Maximum-Parsimony (MP) and Neighbor-Joining (NJ) were performed on the combined DNA sequences of ITS and gpd gene regions. Both morphological observations and molecular analyses support S. luffae, S. lycii and S. cucumis as three new taxa.