Patterns of cranial shape diversification during the phylogenetic branching process of New World monkeys (Primates: Platyrrhini)

One of the central topics in evolutionary biology is understanding the processes responsible for phenotypic diversification related to ecological factors. New World monkeys are an excellent reference system to investigate processes of diversification at macroevolutionary scales. Here, we investigate the cranial shape diversification related to body size and ecology during the phylogenetic branching process of platyrrhines. To investigate this diversification, we used geometric morphometric techniques, a molecular phylogenetic tree, ecological data and phylogenetic comparative methods. Our statistical analyses demonstrated that the phylogenetic branching process is the most important dimension to understand cranial shape variation among extant platyrrhines and suggested that the main shape divergence among the four principal platyrrhine clades probably occurred during the initial branching process. The phylogenetic conservatism, which is the retention of ancestral traits over time within the four principal platyrrhine clades, could be the most important characteristic of platyrrhine cranial shape diversification. Different factors might have driven early shape divergence and posterior relative conservatism, including genetic drift, stabilizing selection, genetic constraints owing to pleiotropy, developmental or functional constraint, lack of genetic variation, among others. Understanding the processes driving the diversification among platyrrhines will probably require further palaeontological, phylogenetic and comparative studies.     

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.      

The ontogeny of cranial sexual dimorphism in two old world monkeys:Macaca fascicularis (Cercopithecinae) andNasalis larvatus (Colobinae)

Allometric and heterochronic approaches to sexual dimorphism have contributed much to our understanding of the evolutionary morphology of the primate skull and dentition. To date, however, extensive studies of sexual dimorphism have been carried out only on the great apes and a few cercopithecine monkeys. To fill this gap, representative dimensions of the skull were collected among ontogenetic series of two dimorphic Old World monkeys:Macaca fascicularis (Cercopithecinae) andNasalis larvatus (Colobinae). The ontogeny of cranial sexual dimorphism was evaluated with least-squares bivariate regression, analysis of covariance (ANCOVA), and analysis of variance (ANOVA). Results indicate that within each species the sexes typically exhibit nonsignificant differences in ANCOVAs of ontogenetic trajectories, except for bivariate comparisons with bicanine breadth. AmongMacaca fascicularis, ANOVAs between males and females of common dental ages show that adult, and frequently subadult, males are significantly larger than females, i.e., sexual dimorphism develops via time and rate hypermorphosis (males primarily grow for a longer time period as well as faster). AmongNasalis larvatus, however, comparisons between males and females of common dental ages indicate that only adult males are significantly larger than females, i.e., sexual dimorphism develops primarily via time hypermorphosis (males grow for a longer time period). Within both species, females appear to exhibit an early growth spurt at dental age 2; that is, many cranial measures for females tend to be larger than those for males. Measures of the circumorbital region (e.g., browridge height), body weight, and bicanine breadth exhibit typically the highest sexual dimorphism ratios. The fact that postcanine toothrow length and neurocranial volume (less so inNasalis) demonstrate very low dimorphism ratios generally supports assertions that postnatal systemic growth (and associated selective pressures thereon) exerts a greater influence on facial, but not neural, dental, or orbital, development (Cochard, 1985, 1987; Shea, 1985a,b, 1986; Shea and Gomez, 1988; Sheaet al., 1990). Additional consideration of ontogenetic differences between species generally supports previous functional interpretations of subfamilial differences in cranial form related to agonistic displays in cercopithecine monkeys (Ravosa, 1990).     

Midsagittal cranial shape variation in the genus Homo by geometric morphometrics

Midsagittal profiles of crania referred to different taxa of the genus Homo have been analyzed by geometric morphometric techniques. Comparisons between single specimens using the thin-plate-spline function suggest a generalized reduction of the lower face, associated with antero-posterior development of the braincase occurring (possibly in parallel evolution) along distinct human lineages. Furthermore, Neandertals display a projection of the midface, and modern humans show a derived globularity of the vault associated with midsagittal parietal bulging. Principal Component Analysis demonstrates a bimodal pattern of variation, which describes an "archaic" pole (rather heterogeneous in terms of taxonomy) clearly distinguishable from the modern one. The first two principal components - that explain together 80% of the total variance in shape - involve respectively fronto-parietal expansion and midfacial prognathism. These results contribute to identify different structural patterns in human evolution, supporting discontinuity rather than continuity of cranial shape among different taxa of the genus Homo, especially when considering the differences between Neandertals and early modern humans.     

Ecogeographical variation in skull morphometry of howler monkeys (Primates: Atelidae)

Our aim is to identify ecomorphological adaptations in the skull shape of the South American howler monkeys (species of the genus Alouatta, Lacépède, 1799, Primates, Atelidae). Since Alouatta is relatively homogenous in feeding ecology, we expect skull shape variation to be relatively conservative across species. We used geometric morphometrics to quantify craniodental morphology in six species of Alouatta. Multivariate regression, two-block Partial Least Squares, and variation partitioning were used to test for the impact of taxonomy, sexual dimorphism, allometry, geography and climate on skull shape. We found morphological overlap among species and sexes, although some discrimination occurs between species living in seasonal environments as opposed to rain forest species. There was a negative latitudinal gradient in skull size across species, with size explaining 34% of total shape variance. Latitude and climate, though important, were secondary in explaining shape variance. Amazonian Alouatta are larger, have thinner molars, wide incisors, and proportionally larger neurocranium. Overall, the shape of southern species seem well adapted to cope with proportionally tougher food items, whereas Amazonian species seem better equipped to deal with a diet richer in fruits, as confirmed by independent field observations. The small size of Alouatta in the South is possibly linked to the effect of competition with the larger folivorous atelid Brachyteles.     

The taxonomic implications of cranial shape variation in Homo erectus

The taxonomic status of Homo erectus sensu lato has been a source of debate since the early 1980s, when a series of publications suggested that the early African fossils may represent a separate species, H. ergaster. To gain further resolution regarding this debate, 3D geometric morphometric data were used to quantify overall shape variation in the cranial vault within H. erectus using a new metric, the sum of squared pairwise Procrustes distances (SSD). Bootstrapping methods were used to compare the H. erectus SSD to a broad range of human and nonhuman primate samples in order to ascertain whether variation in H. erectus most clearly resembles that seen in one or more species. The reference taxa included relevant phylogenetic, ecological, and temporal analogs including humans, apes, and both extant and extinct papionin monkeys. The mean cranial shapes of different temporogeographic subsets of H. erectus fossils were then tested for significance using exact randomization tests and compared to the distances between regional groups of modern humans and subspecies/species of the ape and papionin monkey taxa. To gauge the influence of sexual dimorphism on levels of variation, comparisons were also made between the mean cranial shapes of single-sex samples for the reference taxa. Results indicate that variation in H. erectus is most comparable to single species of papionin monkeys and the genus Pan, which included two species. However, H. erectus encompasses a limited range of variation given its extensive geographic and temporal range, leading to the conclusion that only one species should be recognized. In addition, there are significant differences between the African/Georgian and Asian H. erectus samples, but not between H. ergaster (Georgia+Africa, excluding OH 9 and Daka) and H. erectus sensu stricto. This finding is in line with expectations for intraspecific variation in a long-lived species with a wide, but probably discontinuous, geographic distribution.     

Hearing of old world monkeys (Cercopithecinae)

The characteristics of normal hearing were examined in the laboratory for seven species of Old World monkeys. Operant conditioning procedures, coupled with standard audiometric testing methods, were used to assess thresholds of hearing, frequency range of hearing, and differential sensitivity to auditory intensity and frequency. To produce tonal stimulation, an animal was trained to touch and maintain manual contact with a contact-sensitive key and to report hearing the tone by lifting his hand from the key; this response was followed by food reinforcement. When the reporting response occurred without the auditory signal, the animal was punished by a short suspension from the experiment. Additional contingencies were added to ensure stable and reliable responding, and threshold and differential acuity determinations were then made. Threshold was defined as the stimulus value responded to correctly 50% of the time. The frequency range of hearing of all the cercopithecoids tested extended from 60 to 40,000 Hz, an octave above the upper bound of 20,000 Hz for man but well below the 60–70,000 Hz limit for some prosimians. Absolute sensitivity for tonal stimulation in the most sensitive frequency range (1–8 kHz) was about 2 × 10^?4 microbars, comparable to that of other primates tested, including man. Thus, the Old World monkey appears only slightly less sensitive than man to small changes in intensity and frequency of acoustic stimulation. At 1000 Hz at 60 dB above the threshold of audibility, his limit of resolution is about 5 Hz for frequency and 2 dB for intensity.     

Patterns of dental wear and the role of the canine in Cercopithecinae.

The importance of dental wear patterns in understanding masticatory functions in primates has long been appreciated. However, studies of wear patterns among populations of nonhuman primates are few. The purpose of this investigation is to establish the developmental aspects of dental wear in the Cercopithecinae and to describe certain relevant morphological traits. Studies were made of dental casts from 200 primate specimens of Macaca nemestrina, Macaca mulatta, and Papio cynocephalus. These casts were taken at four-month intervals, beginning at two years of age and continuing over a period of six to seven years. The wear pattern starts with the rounding and eventual flattening of the protoconid and protocone of the erupted first molars. Once this stage is reached, the hypoconid and metaconid of the mandibular, and the hypocone and paracone of the maxillary molars are rounded and eventually flattened. This pattern is maintained until the cusp tips are removed and the dentin exposed, however, the entoconid and metacone are not subjected to significant wear at this stage. Analysis of these dental casts and museum specimens has provided data on the development of dental wear during the maturation of these primates. The distribution of forces acting upon the teeth produce diagnostic patterns of wear, which provide evidence of the force location and magnitude. In examining the data, the hypothesis of canine guidance and its limitation of mandibular motion was evaluated. Specimens whose canines were removed demonstrate that the canines play no significant role in the development or maintenance of dental wear planes.     

Patterns of morphometric variation in birds' tails: length, shape and variability

In Palaearctic birds, tail length was more variable than wing and tarsus, but not bill lengths. Tails of the ornamental shapes pin, lyre and graduated varied more in length than did non-ornamental shapes. Log coefficient of variation (C V) tail length showed an overall U-shaped relationship with longtailedness, but although the CV for most tail shapes increased in short-tailed species, only in ornamental shapes was C V also high in long-tailed species. C V of fork depth was lowest at a fork depth of 2, and considerably higher in shallow forked tails. CV streamer lengths were similar to CV deep fork depths. The more deeply forked tails thus seem ornamental. Phylogenetically independent contrasts confirmed in males, but not females, that long-tailed species had greater CV than medium-tailed species, and the greater CV of graduated than square tails, but the CV of short- and medium-tailed species did not differ. These comparisons, however, did not control for tail shape. The greater elongation and CV of tails with ornamental shapes are consistent with an influence of sexual/signal selection on these tails, and the increase in CV with longtailedness suggests that Weber's law applies to the perceptual threshold for tail length. Sexual selection may have a widespread, but moderate, influence on tail traits in birds.     

Patterns of genetic variation of the genusCapsicum (Solanaceae) in Mexico

The evolutionary relationships of 186 accessions ofCapsicum from Mexico were studied through enzyme electrophoresis. A total of 76 alleles representing 20 genetic loci coding for nine enzyme systems were observed and the allelic variations of enzymes were studied for geographical distribution. Allele frequencies were used to estimate the apportionment of gene diversity within and between populations and to construct a dendrogram based on a similarity matrix containingNei genetic distances. — The gene diversity estimates suggest that the structure ofCapsicum populations in Mexico consists of predominantly homozygous genotypes presumably due to a self-pollinated breeding system and population bottlenecks. Significant genetic differentiation was found mainly between populations of differing geographical regions.—Based on the results of this study, three species of domesticatedCapsicum can be identified in Mexico,C. annuum var.annuum, C. chinense, andC. pubescens. Semidomesticated and wild forms include two species,C. frutescens andC. annuum var.glabriusculum. A sharp geographical division results between the latter species;C. frutescens was collected exclusively in the southeastern states of Oaxaca, Chiapas, and Tabasco; whereas wild and semidomesticated forms from the rest of the country areC. annuum. Based upon the similarity of enzyme genotypes of semidomesticated and wild forms, the primary center of domestication of cultivatedC. annuum was estimated to be the region comprising the states of Tamaulipas, Nuevo Leon, San Luis Potosi, Veracruz, and Hidalgo in eastern Mexico. A possible second center of domestication is suggested to be localized in the state of Nayarit, western Mexico.     

Patterns of morphological variation among cardueline finches (Fringillidae: Carduelinae)

Patterns of variation in five morphological traits in cardueline finches were analysed. Among species, bill characters were the most and tail length the least variable. Species differed primarily in terms of body size, whereas genera differed in terms of bill size. Cardueline finches were far less variable compared with the amount of variation expected under a model of neutral random drift. This indicates that this group of birds is under strong stabilizing selection pressure. This could conform to models of stasis where populations are thought to travel only between adjacent adaptive peaks separated by shallow valleys. Changes in body size are correlated with speciation, whereas changes in bill morphology are correlated with divergences leading to the erection of new genera.     

Geometric morphometric analysis of shell shape variation in Conus (Gastropoda: Conidae)

Geometric morphometric techniques allow for the direct quantification and analysis of variation in biological shape and have been used in studies in systematic biology. However, these techniques have not been used for species discrimination in the gastropod genus Conus, a major taxon of significant tropical reef predators recognized for their peptide‐based toxins. Here, we used landmark digitization and analysis to show that five species commonly studied for their conotoxins –Conus consors, Conus miles, Conus stercusmuscarum, Conus striatus, and Conus textile – can be effectively distinguished from each other by their shape, as manifested in the results of a principal components analysis (PCA) and the generated thin‐plate splines. Two piscivorous species, C. stercusmuscarum and C. striatus, show clear overlaps in the PCA plot, although each taxon clusters within itself, as does each of the others. The loadings on the first two principal components show that the forms of the shells' aperture and spire are particularly important for discrimination. Phylogenetic analysis using neighbour‐joining methods shows that group separations are comparable with published phylogenetic schemes based on molecular data and feeding mode (i.e. piscivory, vermivory, molluscivory). The results of this study establish the utility of geometric morphometric methods in capturing the interspecific differences in shell form in the genus Conus. This may lead to the utilization of these methods on other gastropod taxa and the creation of species‐recognition programs based on shell shape. © 2012 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 165 , 296–310.     

SRY evolution in Cebidae (Platyrrhini: Primates)

Sex determination in mammals is dependent on the presence of SRY, which codes for a protein with a DNA binding motif (the HMG-box domain). Here we analyze the evolution of SRY among seven genera of New World monkeys belonging to the family Cebidae. Estimates of the number of synonymous and nonsynonymous substitutions indicated the absence of positive selection acting on SRY evolution. The presence of indels at the C-terminus coding region in different genera and species maintained an open reading frame, indicating a selective pressure constraining the evolution of this coding region. Available data on the fertility of natural and captive interspecific hybrids failed to show any relationship between SRY evolution and speciation for the genera herein studied. Our phylogenetic arrangement for Cebidae genera was similar to previous topologies based on mitochondrial and autosomal DNA sequences. This arrangement also corroborated the division of Cebus into two species groups. However, for Callithrix the differences among SRY topology and those derived from autosomal and mitochondrial genes suggested a Y-chromosome ancestral polymorphism.