Cranial evolution in sakis (Pithecia, Platyrrhini). II: Evolutionary processes and morphological integration

Patterns of interspecific differentiation in saki monkeys (Pithecia) are quantitatively described and possible evolutionary processes producing them are examined. The comparison of species correlation matrices to expected patterns of morphological integration reveal significant and similar patterns of development-based cranial integration among species. Aspects of the facial region are more heavily influenced by general size variation than features of the neural region. The comparison of pooled within- and between-groups V/CV matrices suggests that genetic drift might be a sufficient explanation for saki cranial evolution. Differential natural selection gradients are also reconstructed because selection may also have caused population differentiation through evolutionary time. These gradients illustrate the inherent multivariate nature of selection, being a consequence of the interaction between existing morphological integration (correlation) among traits and the action of natural selection. Yet, our attempt to interpret selection gradients in terms of their functional significance did not result in any clear association between selection and function. Perhaps this is also an indication that morphological evolution in sakis was mostly neutral.     

Dermatoglyphic patterns and pattern intensities of the genus Cacajao (Cebidae,platyrrhini) with observations on interspecific and subspecific differentiation

Palmar and plantar dermatoglyphic pattern types, area and total pattern intensities (API and TPI), and pattern intensity (PI) profiles are presented for the South American genus Cacajao of the subfamily Pitheciinae. The data are based on prints from 41 bald-head uacaries (C. calvus), 9 white bald-head uacaries (C. c. calvus), and 15 black-head uacaries (C. melanocephalus). In each extremity, loops of differing orientation were the most frequent pattern type; whorls were dominant at palmar interdigital (I) area 3 in C. calvus and at both I3 and I4 in C. melanocephalus. Open fields characterized the palmar thenar and plantar proximal hypothenar, thenar, calcar, and I3 and I4. There was little evidence of significant sexual dimorphism as assessed from PI values. The genus displayed significant asymmetry at palmar I3 (P?0.001) and plantar distal hypothenar (P?0.004). There were significant group differences between C. calvus and C. c. calvus in the palmar thenar API and plantar TPIs. The combined bald-head sample of C. calvus and C. c. calvus differed from C. melanocephalus in API of palmar I4 and plantar distal thenar, I2, and distal hypothenar (marginally), and in plantar TPIs. In PI profiles, C. melanocephalus departed from the pattern shared by C. calvus and C. c. calvus in both palmar and plantar interdigital areas. As a genus, the uacaries have markedly low plantar TPI values relative to palmar values (palm-sole index > 195). Of eight comparison cebid genera, only Chiropotes, another pitheciine genus, approximated these values.     

Systematics and evolution of the Jacchus group of marmosets (Platyrrhini)

Interspecific differentiation and geographic variation patterns in 39 skull traits of eastern Brazilian marmosets are analyzed. Eastern Callithrix taxa are distinct morphologically, and no evidence of intergradation among taxa is observed. Instead, there are sharp, stepped morphological boundaries among taxa, consistent with species‐level distinction. The morphological similarity cluster diagram obtained from Mahalanobis distances is different from available molecular trees, and the general picture emerging is that the eastern Callithrix taxa should be considered as good species arising recently in South American history. In particular, C. kuhlii is morphologically distinct from other marmoset taxa, including C. geoffroyi and C. penicillata, which were previously hypothesized to be the parental populations that formed C. kuhlii by hybridization. Furthermore, C. kuhlii populations from southeastern Bahia do not overlap morphologically with any C. penicillata population, including the upper São Francisco River populations that display skin colors and pelage patterns to some extent similar to true Kuhli's marmosets. There is a negative, though insignificant, correlation between the morphological distance matrix and a Mahalanobis distance matrix estimated from nine climatic variables, a pattern opposite to that expected under a parapatric speciation model. This result, together with the lack of clinal variation in skull traits, suggests that an allopatric model of speciation might best explain eastern marmoset diversification. Am J Phys Anthropol 2003. © 2002 Wiley‐Liss, Inc.     

Abundance, use of space, and activity patterns of white-faced sakis (Pithecia pithecia) in French Guiana.

White-faced sakis (Pithecia pithecia) are among the least studied neotropical primates. The combination of shy and quiet behavior, their ability to move silently, and the extreme difficulty of capturing them may explain why very few field studies have been undertaken in undisturbed habitats. During the course of a wildlife rescue in French Guiana, six individuals were captured and translocated to a safe area of primary rainforest. In this area, based on the observation of 35 groups, the average group size was 2.3 animals (SD = 1.2) and a density of 0.28 group/km(2) (0.64 individuals/km(2)) was estimated from transect censuses. Our study focused successively on three radio-collared animals (two males and one female) over a 287-day period, starting from release to the loss of the animal. From the study start, the triangulation method was used prior to habitutation to human presence, followed thereafter by 1,327 hr of visual monitoring. The translocated animals settled down, and two of them had a stable and compact home range. Two of them merged in association with members of the resident population. A resident group had a much larger home range than previously reported: 148 and 287 ha, using grid cells and 100% minimum convex polygon techniques, respectively. A group composed of two translocated individuals (one male and one female) had a home range of 68 and 135 ha using the same techniques. Additionally, two solitary animals used 152 and 162 1-ha quadrats. We observed animals (translocated and residents) moving quickly in one direction up to 11.5 km. The mean daily path length of resident animals was 1,880 m. Sakis used the lower strata of the forest more when in group, and the intermediate strata more when solitary. Allogrooming is fairly common in social groups. On average, the activity period ranged from 7:17 to 15:59 hr.     

Digesta passage and fiber digestibility in captive white-faced sakis (Pithecia pithecia)

Wild white-faced sakis (Pithecia pithecia) ingest primarily seeds that provide a diet that is lipid-rich and moderately high in dietary fiber. Although little anatomical information is available on sakis, evidence from other vertebrate seed predators suggests that such a diet is correlated with adaptations in gut morphology or physiology. Milton [1984] reported a 20 hr transit time (TT=transit time or time of first appearance in feces) of a particulate marker for a single monk saki (Pithecia monachus). This suggests that TT for Pithecia sakis may be four to five times longer than what has been reported for soft-fruit-eating platyrrhines, such as Ateles and Cebus. During a captive study, we calculated an average TT of 14.7+/-0.4 hr (n=5 trials started in the evening) for a chromic oxide (Cr(2)O(3)) marker that follows liquid digesta and TTs of 14.5 hr (trial started the previous evening) and 23.0 hr (trial started the previous morning) for two trials using particulate markers. Mean retention time (MRT) for the liquid marker ranged from 15.3 hr to 37.7 hr in four trials that lasted longer than 90 hr. Marker recovery was incomplete for the particulate markers in these trials, and thus MRT could only be determined for the liquid phase marker. Three 5-day trials on a low-fiber, blended diet revealed high fiber fraction digestibilities (neutral detergent fiber (NDF)=77.4% and acid detergent fiber (ADF)=74.4%). Data collected for this study and nutritional data from wild sakis suggest that pitheciin seed predators may have a potential for fiber digestibility that is intermediate between ripe-pulp frugivores and folivores.     

Effect of life history on the squirrel monkey (Platyrrhini,Saimiri) cranium

Among primates, squirrel monkeys uniquely possess an interorbital fenestra, in which the midline bony orbitosphenoid septum is largely absent and the soft tissues of the orbits are separated only by a thin membrane. Neural development may contribute to the approximation of the orbits to the midline in Saimiri, insofar as other platyrrhines with relatively large brains also have relatively narrow interorbital spaces compared to their near relatives. In Saimiri the narrow spacing of the orbits is further exacerbated by intense predation pressure on infants that may select for precocial neonates. The result is a large-headed neonate that is subject to unusual parturition constraints. These parturition constraints apply to the size and dolichocephalic shape of the squirrel monkey head in general, and to the relatively large eyes and approximated orbits in particular. The unique interorbital condition in Saimiri is an example of the effects of life history on skeletal morphology. © 1995 Wiley-Liss, Inc.     

Selected aspects of female white-faced saki (Pithecia pithecia) reproductive biology in captivity

Little is known regarding the reproductive biology of the white-faced saki. Although sakis have been in zoos since the mid-1970s, little attention has been paid to the reproductive biology of this threatened species. This study describes the results of a 3-year study of the reproduction of the white-faced saki in captivity. Using noninvasive methods to determine levels of estrone conjugates (E₁C) and pregnanediol-3-glucuronide (PdG) in daily urine samples, we have characterized the female reproductive cycle of this species. Nonconceptive ovarian cycles were 16.95 ± 1.57 (SD) days, gestational length was 146.1 ± 5.2 (SD) days, and the length of lactationally induced infertility varied among females but averaged 163 ± 40.6 (SD) days. Attempts to accelerate puberty by pairing a young female with an adult male was without effect. Puberty occurred at 32 months of age in one female. This study provides information that enhances our understanding of the reproductive biology of this species. © 1995 Wiley-Liss, Inc.     

ABO Blood groups in cebidae (Platyrrhini,Primates) from the Rio Jamari Region

Blood and saliva samples were collected from 84Aotus azarae boliviensis, 31Ateles paniscus chamek, 130Callicebus brunneus, 130Cebus apella, 117Pithecia irrorata irrorata, and 117Saimiri ustus. Saliva samples were investigated for human ABH antigens by the standard hemagglutination inhibition test. Two species,P. irrorata andC. brunneus showed monomorphism, presenting only the A blood group. Among the polymorphic species,A. paniscus andC. apella presented theO (30 and 3) and A (1 and 127) phenotypes, and the B (80) and AB (4) phenotypes were detected inA. azarae. S. ustus was the only species that presented all the four phenotypes. The observed distribution was as expected assuming Hardy-Weinberg equilibrium to be present in those species that could be tested. The ABH substances were titrated and a comparison among species was made. Serum samples were used to detect natural antibodies and the results showed some disagreement between serum and saliva phenotypes.     

Cranial differentiation and evolution in Thrichomys apereoides (Rodentia: Echinyidae)

Thrichomys apereoides is an echimyid rodent which ranges in distribution from north-eastern and central Brazil into Paraguay, and currently five subspecies are recognized. Recent morphometric analyses of population samples formally assignable to T. a. laurentius and T. a. inermis , which occur in north-eastern Brazil, have shown that a major group of populations including both subspecies differ in cranial shape from a single population allocated to T. a. laurentius . In this study we employed mathematical models of evolutionary quantitative genetics to assess the role that random drift and selection may have played in the evolution of cranial shape differences in T. apereoides . The hypothesis of evolution due to drift was rejected and the selective forces necessary to account for shape differences were estimated. Minimum selective mortalities of the order of 10^-3 of per generation were sufficient to explain the observed morphologic differentiation.     

Taxonomy,skull diversity and evolution in a species complex of Myotis (Chiroptera: Vespertilionidae): a geometric morphometric appraisal

Phylogenetic relationships between taxa are not necessarily reflected by morphological data due to widespread homoplasy and convergence. However, combining morphological and molecular data provides insights into the evolution of biological forms and into the potential factors involved. Here we focus on a complex of three taxa of bats with unclear taxonomic affinities: Myotis myotis, Myotis blythii and Myotis punicus. Traditional morphometric methods failed to separate them, whereas recent molecular‐based studies suggested that they constitute separate biological species. In the present study, landmark‐based geometric morphometrics methods have been used to analyse the skull variability of 218 specimens belonging to this species complex. Patterns of size and shape delimitate three morphological groups that are congruent with the proposed taxonomic assignments, and therefore support species rank for all three major groups. These morphometrics results, however, suggest that M. myotis and M. punicus share shape characteristics in the rostrum and in the posterior part of the skull that differ from M. blythii. Because previous molecular phylogenetic analyses suggested that M. myotis and M. blythii are sister species, we interpret the similitude in skull morphology between M. myotis and M. punicus as a convergence probably related to their similar feeding habits. Within the taxon M. punicus, the skull of Corsican and Sardinian populations significantly differs from that of Maghrebian ones, suggesting the existence of further cryptic taxonomic diversity. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 529–538.     

Combining geometric morphometrics and pattern recognition to identify interspecific patterns of skull variation: case study in sympatric Argentinian species of the genus Calomys (Rodentia: Cricetidae: Sigmodontinae)

Sympatric species of vesper mice Calomys laucha and Calomys musculinus are difficult to discriminate, especially in natural history collections where they are identified by external body measurements and cranial characteristics. Accurate identification of these two species can be important because only one of them, C. musculinus , is a Junin virus reservoir, the aetiological agent of the Argentine Hemorragic Fever. Research has focused into the development of molecular techniques to unambiguously identify these species. We apply statistical procedures from the field of pattern recognition to three-dimensional geometric morphometric data based on skull landmarks to identify sympatric species C. laucha , C. musculinus and Calomys venustus . Pattern recognition techniques correctly identified the three species without any prior information on specimen identity. By contrast to expectations, C. venustus differed from the other two species mainly on the basis of shape and not by its centroid size. The main sources of difference between C. laucha and C. musculinus were of shape, specifically localized at the landmarks defined by: (1) the sutures between the premaxillaries, the nasals and the frontals; (2) the sutures between the parietals, the frontals and the squamosals; and (3) the suture between the parietals and the interparietal. Nevertheless, allometries dominate the patterns of interspecific variation between these latter species and may partly explain past identification difficulties. Morphological evolution is discussed. The need for objective methods to define phenotypic clusters is highlighted with respect to the need for fast and precise biodiversity assessments.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 365–378.     

Synteny of human chromosomes 14 and 15 in the platyrrhines (Primates, Platyrrhini)

In order to study the intra- and interspecific variability of the 14/15 association in Platyrrhini, we analyzed 15 species from 13 genera, including species that had not been described yet. The DNA libraries of human chromosomes 14 and 15 were hybridized to metaphases of Alouatta guariba clamitans, A. caraya, A. sara, Ateles paniscus chamek, Lagothrix lagothricha, Brachyteles arachnoides, Saguinus midas midas, Leontopithecus chrysomelas, Callimico goeldii, Callithrix sp., Cebus apella, Aotus nigriceps, Cacajao melanocephalus,Chiropotes satanas and Callicebus caligatus. The 14/15 hybridization pattern was present in 13 species, but not in Alouatta sara that showed a 14/15/14 pattern and Aotus nigriceps that showed a 15/14/15/14 pattern. In the majority of the species, the HSA 14 homologue retained synteny for the entire chromosome, whereas the HSA 15 homologue displayed fragmented segments. Within primates, the New World monkeys represent the taxon with the highest variability in chromosome number (2n = 16 to 62). The presence of the HSA 14/15 association in all species and subspecies studied herein confirms that this association is the ancestral condition for platyrrhines and that this association has been retained in most platyrrhines, despite the occurrence of extensive inter- and intrachromosomal rearrangements in this infraorder of Primates.     

Exaggerated allometric structures in relation to demographic and ecological parameters in Lucanus cervus (Coleoptera: Lucanidae)

Enlarged weapons and ornamental traits under sexual selection often show a positive allometric relationship with the overall body size. The present study explores the allometry of mandibles and their supporting structure, the head, in males of the European stag beetle, Lucanus cervus. This species shows a remarkable dimorphism in mandible shape and size that are used by males in intraspecific combats. Stag beetles were captured, measured, weighed, and released in the framework of a capture‐mark‐recapture study. The relationship of mandible length (ML) and head width in respect to the overall body size was described by a segmented regression model. A linear relationship was detected between ML and head width. The scaling relationships for both ML and head width identified the same switchpoint, highlighting the advantages of using combined results of weapons and their supporting structures in such analysis. These results led to a more consistent distinction of males in two morphologies: minor and major. The survival probability of individuals was dependent on the morphological class and was higher for minor males than for major. Elytron length and body mass of the individuals did not show any significant variation during the season. Differences in predatory pressure were detected between morphs by the collection and analysis of body fragments due to the predatory activity of corvids. Morphological differences and shift in demographic and ecological parameters between the two classes suggested that selection continues to favor intrasexual dimorphism in this species throughout a trade‐off mechanism between costs and benefits of carrying exaggerated traits. J. Morphol. 276:1193–1204, 2015. © 2015 Wiley Periodicals, Inc.     

Differences in shape and size of skull and mandible in Talpa species (Mammalia: Eulipotyphla) from Turkey

We analysed with landmark-based images morphological differences between four species of Talpa which resemble each other morphologically and are all highly adapted to underground life. Subtle shape differences of the skull and mandibular bones were found between all species. However, there is also broad overlap between all species. Talpa caucasica had the largest skull and mandibles, and Talpa levantis the smallest.     

Naturally occurring fatal herpes simplex virus 1 infection in a family of white-faced saki monkeys (Pithecia pithecia pithecia)

A family of three white-faced saki monkeys (Pithecia pithecia pithecia) died 48-96 hours after the onset of anorexia, nasal discharge, pyrexia and oral ulceration. One animal also had clonic seizures. Lesions found post-mortem consisted of oral and esophageal ulcers, hepatic and intestinal necrosis, meningoencephalitis and sporadic neuronal necrosis. Intranuclear inclusion bodies and syncytial cells were present in oral lesions and affected areas of liver. Herpes simplex virus 1 (HSV-1) was identified as the etiology of disease by virus isolation, polymerase chain reaction, or in situ hybridization in all three animals. Immunohistochemistry for detection of apoptotic DNA and activated caspase-3 showed significant levels of apoptosis in oral and liver lesions and occasional apoptotic neurons in the brain. These findings demonstrate the vulnerability of white-faced saki monkeys to HSV-1 and provide initial insight into the pathogenesis of fatal HSV-1-induced disease, indicating that apoptosis plays a significant role in cell death.     

Use of levonorgestrel as an effective means of contraception in the white‐faced saki (Pithecia pithecia)

This study examines the use levonorgestrel (Norplant^®‐2) as a means of contracepting white‐faced sakis (Pithecia pithecia). A 70‐mg silastic tubule of levonorgestrel was implanted subdermally between the scapulae in four multiparous and two nulliparous females. Implants remained in the females housed with males of proven fertility for 81 to 734 days. All females experienced low, acyclic levels of estrone conjugates (E₁C, < 500 ng/mg Cr) and pregnanediol‐3‐glucuronide (PdG, < 1.5 μg/mg Cr) after insertion of the implant. In five females having nine contraceptive bouts, ovulation was completely blocked for the entire duration of Norplant insertion (range: 81–734 days) as evidenced by a lack of cyclic changes in excretory hormone levels. However, one female was observed to have cyclic ovarian hormonal levels 5.8 months after Norplant insertion. Thus, levonorgestrel can be an effective method for blocking cyclic ovarian hormonal changes for 1 year (n = 2) and possibly as long as 2 years (n = 3). Zoo Biol 21:49–57, 2002. © 2002 Wiley‐Liss, Inc.     

In situ hybridization (FISH) maps chromosomal homologies between Alouatta belzebul (Platyrrhini,Cebidae) and other primates and reveals extensive interchromosomal rearrangements between howler monkey genomes

We hybridized whole human chromosome specific probes to metaphases of the black-and-red howler monkey Alouatta belzebul in order to establish chromosomal homology between humans and black-and-red howlers. The results show that the black-and-red howler monkey has a highly rearranged genome and that the human chromosome homologs are often fragmented and translocated. The number of hybridization signals we obtained per haploid set was 40. Nine human chromosome probes gave multiple signals on different howler chromosomes, showing that their synteny is disturbed in A. Belzebul. Fourteen black-and-red howler autosomes were completely hybridized by one human autosomal paint, six had two signals, three had three signals, and one chromosome had four signals. Howler chromosomes with multiple signals have produced 12 chromosomal syntenies or hybridization associations which differ from those found in humans: 1/2, 2/20, 3/21, 4/15, 4/16, 5/7, 5/11, 8/18, 9/12, 10/16, 14/15, and 15/22. The hybridization pattern was then compared with those found in two red howler taxa and other mammals. The comparison shows that even within the genus Alouatta numerous interchromosomal rearrangements differentiate each taxa: A. belzebul has six unique apomorphic associations, A. seniculus sara and A. seniculus arctoidea share seven derived associations, and additionally A. seniculus sara has four apomorphic associations and A. seniculus arctoideaseven apomorphic associations. A. belzebul appears to have a more conserved karyotype than the red howlers. Both red and black-and-red howlers are characterized by Y-autosome translocations; the peculiar chromosomal sex system found in the red howler taxa could be considered a further transformation of the A. belzebul sex system. The finding that apparently morphologically similar or even identical taxa have such extreme genomic differences has important implications for speciation theory and neotropical primate conservation. Am. J. Primatol. 46:119–133, 1998. © 1998 Wiley-Liss, Inc.     

Cranial variation in Meriones tristrami (Rodentia: Muridae: Gerbillinae) and its morphological comparison with Meriones persicus,Meriones vinogradovi and Meriones libycus: a geometric morphometric study

Jirds (genus Meriones) comprise a group of rodents, of which the biodiversity is still poorly known. Reason for this is that several species of similar morphologies are known to occur sympatrically. In the north‐west of Iran, four such species occur: Meriones tristrami, Meriones persicus, Meriones vinogradovi and Meriones libycus, prone to several issues of taxonomical ambiguity. A proper characterization of morphological distinctiveness between these species, in relation to the variation within species, could provide the required information for species diagnosis and identification. As some cranial characters of M. tristrami, M. persicus and M. vinogradovi are quite similar, demarcations of species‐specific phenotypic variation have proven to be difficult. To tackle this problem, this study involves a geometric morphometric analysis of skull shape and size, incorporating a large representative sample of these four species, originating from most parts of their natural distribution range (especially for M. tristrami). It is first tested whether M. tristrami can be distinguished from the other sympatric species, and if so, to what degree the species shows a geoclimatic pattern in its skull shape and size when comparing different populations. The shape and size analyses show that M. libycus can be distinguished because of its largest skull and the relatively largest tympanic bulla, and that M. tristrami can be distinguished from the other species. At an intraspecific level in M. tristrami, the Iranian groups (Qazvin and west Iran) do not differ in shape among them, but do so in skull size. They could, however, be distinguished in skull shape from the non‐Iranian populations included (Turkey and Jordan). To what degree this continuous data can now be translated into discrete and diagnostic features, useful for taxonomic purposes, remains to be studied.