Role of the prehensile tail during ateline locomotion: experimental and osteological evidence

The dynamic role of the prehensile tail of atelines during locomotion is poorly understood. While some have viewed the tail of Ateles simply as a safety mechanism, others have suggested that the prehensile tail plays an active role by adjusting pendulum length or controlling lateral sway during bimanual suspensory locomotion. This study examines the bony and muscular anatomy of the prehensile tail as well as the kinematics of tail use during tail-assisted brachiation in two primates, Ateles and Lagothrix. These two platyrrhines differ in anatomy and in the frequency and kinematics of suspensory locomotion. Lagothrix is stockier, has shorter forelimbs, and spends more time traveling quadrupedally and less time using bimanual suspensory locomotion than does Ateles. In addition, previous studies showed that Ateles exhibits greater hyperextension of the tail, uses its tail to grip only on alternate handholds, and has a larger abductor caudae medialis muscle compared to Lagothrix. In order to investigate the relationship between anatomy and behavior concerning the prehensile tail, osteological data and kinematic data were collected for Ateles fusciceps and Lagothrix lagothricha. The results demonstrate that Ateles has more numerous and smaller caudal elements, particularly in the proximal tail region. In addition, transverse processes are relatively wider, and sacro-caudal articulation is more acute in Ateles compared to Lagothrix. These differences reflect the larger abductor muscle mass and greater hyperextension in Ateles. In addition, Ateles shows fewer side-to-side movements during tail-assisted brachiation than does Lagothrix. These data support the notion that the prehensile tail represents a critical dynamic element in the tail-assisted brachiation of Ateles, and may be useful in developing inferences concerning behavior in fossil primates.     

On caudal prehensility and phylogenetic constraint in lizards: The influence of ancestral anatomy on function in Corucia and Furcifer

We examined caudal anatomy in two species of prehensile‐tailed lizards, Furcifer pardalis and Corucia zebrata. Although both species use their tails to grasp, each relies on a strikingly different anatomy to do so. The underlying anatomies appear to reflect phylogenetic constraints on the consequent functional mechanisms. Caudal autotomy is presumably the ancestral condition for lizards and is allowed by a complex system of interdigitating muscle segments. The immediate ancestor of chameleons was nonautotomous and did not possess this specialized anatomy; consequently, the derived arrangement in the chameleon tail is unique among lizards. The limb functions as an articulated linkage system with long tendinous bands originating from longitudinal muscles to directly manipulate vertebrae. Corucia is incapable of autotomy, but it is immediately derived from autotomous ancestors. As such, it has evolved a biomechanical system for prehension quite different from that of chameleons. The caudal anatomy in Corucia is very similar to that of lizards with autotomous tails, yet distinct differences in the ancestral pattern and its relationship to the subdermal tunic are derived. Instead of the functional unit being individual autotomy segments, the interdigitating prongs of muscle have become fused with an emphasis on longitudinal stacks of muscular cones. The muscles originate from the vertebral column and a subdermal collagenous tunic and insert within the adjacent cone. However, there is remarkably little direct connection with the bones. The muscles have origins more associated with the tunic and muscular septa. Like the axial musculature of some fish, the tail of Corucia utilizes a design in which these collagenous elements serve as an integral skeletal component. This arrangement provides Corucia with an elegantly designed system capable of a remarkable variety of bending movements not evident in chameleon tails. J. Morphol. 239:143–155, 1999. © 1999 Wiley‐Liss, Inc.     

The Ontogeny of Prehensile‐Tail Use in Cebus capucinus and Alouatta palliata

A study of the platyrrhine prehensile tail provides an opportunity to better understand how ecological and biomechanical factors affect the ability of primates to distribute mass across many different kinds of arboreal supports. Young individuals experience ontogenetic changes in body mass, limb proportions, and motor skills that are likely to exert a strong influence on foraging strategies, social behaviors, support use, and associated prehensile‐tail use. In this research, I examine ontogenetic patterns of prehensile‐tail use in Cebus capucinus and Alouatta palliata. I collected behavioral data on activity, positional context, support size, and prehensile‐tail use in five age categories of white‐faced capuchins and mantled howlers during a 12‐month period at Estación Biológica La Suerte in northeastern Costa Rica. Infant and juvenile howlers and capuchins were found to use their prehensile tails significantly more often than adults during feeding, foraging, and social behavior. Prehensile‐tail use did not show predictable increases during growth. In both species, adults used their prehensile tails in mass‐bearing modes significantly less often than juveniles. Despite differences in tail anatomy in Cebus and Alouatta, prehensile‐tail use was observed to follow an increasing trajectory from infancy, peaking during juvenescence, and then decreasing in older juveniles and adults. In both species, it appeared that adult patterns of prehensile‐tail use reflected the demands placed on young juveniles. Am. J. Primatol. 74:770‐782, 2012. © 2012 Wiley Periodicals, Inc.     

Systematics and morphological evolution within the moss family Bryaceae: a comparison between parsimony and Bayesian methods for reconstruction of ancestral character states

The Bryaceae are a large cosmopolitan moss family including genera of significant morphological and taxonomic complexity. Phylogenetic relationships within the Bryaceae were reconstructed based on DNA sequence data from all three genomic compartments. In addition, maximum parsimony and Bayesian inference were employed to reconstruct ancestral character states of 38 morphological plus four habitat characters and eight insertion/deletion events. The recovered phylogenetic patterns are generally in accord with previous phylogenies based on chloroplast DNA sequence data and three major clades are identified. The first clade comprises Bryum bornholmense, B. rubens, B. caespiticium, and Plagiobryum. This corroborates the hypothesis suggested by previous studies that several Bryum species are more closely related to Plagiobryum than to the core Bryum species. The second clade includes Acidodontium, Anomobryum, and Haplodontium, while the third clade contains the core Bryum species plus Imbribryum. Within the latter clade, B. subapiculatum and B. tenuisetum form the sister clade to Imbribryum. Reconstructions of ancestral character states under maximum parsimony and Bayesian inference suggest fourteen morphological synapomorphies for the ingroup and synapomorphies are detected for most clades within the ingroup. Maximum parsimony and Bayesian reconstructions of ancestral character states are mostly congruent although Bayesian inference shows that the posterior probability of ancestral character states may decrease dramatically when node support is taken into account. Bayesian inference also indicates that reconstructions may be ambiguous at internal nodes for highly polymorphic characters.     

The ecological role of the prehensile tail in white-faced capuchins (Cebus capucinus).

Prehensile tails appear to have evolved at least twice in platyrrhine evolution. In the atelines, the tail is relatively long and possesses a bare area on the distal part of its ventral surface that is covered with der-matoglyphs and richly innervated with Meissner's corpuscles. In contrast, the prehensile tail of Cebus is relatively short, fully haired, and lacks specialized tactile receptors. Little is currently known regarding tail function in capuchins, and whether their prehensile tail serves a greater role in feeding or traveling. In this paper we examine patterns of positional behavior, substrate preference, and tail use in wild white-faced capuchins (Cebus capucinus) inhabiting a wet tropical forest in northeastern Costa Rica. Observational data were collected over the course of 3 months on adult capuchins using an instantaneous focal animal time sampling technique. Differences in the frequency and context of tail use, and the estimated amount of weight support provided by the tail relative to other appendages during feeding/foraging and traveling were used as measures of the ecological role of this specialized organ in capuchin positional behavior. During travel, quadrupedal walking, leaping, and climbing dominated the capuchin positional repertoire. The capuchin tail provided support in only 13.3% of travel and was principally employed during below branch locomotor activities. In contrast, tail-assisted postures accounted for 40.6% of all feeding and foraging records and occurred primarily in two contexts. The tail was used to suspend the individual below a branch while feeding, as well as to provide leverage and weight support in above-branch postures associated with the extraction of prey from difficult to search substrates. A comparison of tail use in Cebus, with published data on the atelines indicates that both taxa possess a grasping tail that is capable of supporting the animal's full body weight. In capuchins and howling monkeys, the tail appears to be used more frequently and serves a greater weight-bearing role during feeding than during traveling. In Ateles, and possibly Brachyteles, and Lagothrix, however, the prehensile tail serves a dual role in both feeding and forelimb suspensory locomotion. Additional relationships between white-faced capuchin feeding, positional behavior, extractive foraging techniques, and prehensile tail use are discussed.     

Phylogeny,biogeography, and morphological ancestral character reconstruction in the Mediterranean genus Fumana (Cistaceae)

Fumana is a diverse genus of the Cistaceae family, consisting of 21 currently accepted species. In this study, nuclear (ITS) and plastid (matK, trnT‐L) molecular markers were used to reconstruct the phylogeny and to estimate divergence times, including 19 species of Fumana. Phylogenetic analyses (Bayesian Inference, Maximum Parsimony and Maximum Likelihood) confirmed the monophyly of Fumana and did not support the infrageneric divisions previously established. The results support four main clades that group species that differ in vegetative and reproductive characters. Given the impossibility to define morphological characters common to all species within the clades, our proposal is to reject infrageneric divisions. Molecular dating and ancestral area analyses provide evidence for a Miocene diversification of the genus in the north‐western Mediterranean. Ancestral state reconstructions revealed ancestral character states for some traits related to xeric and arid habitats, suggesting a preadaptation to the Mediterranean climate.     

Contribution of homoplasy and of ancestral polymorphism to the evolution of genes in anthropoid primates

Molecular phylogenies of lineages that split from one another in short succession are often difficult to resolve because different loci and different sites within the same locus yield incongruent relationships. The incongruity is commonly attributed to two causes: differential assortment of ancestral polymorphisms and homoplasy. To assess the relative contribution of these two causes, sequences of 57 segments from 51 loci in six primate lineages (human, chimpanzee, gorilla, orangutan, macaque, and tamarin, abbreviated as H, C, G, O, M, and T, respectively) were subjected to "partitioning" analysis, in which phylogenetically informative sites were identified in all 15 pairwise comparisons of each of the 57 segments and tallied for their support or lack thereof for each of the theoretically possible phylogenies. The six lineages include one of the best known cases of a difficult-to-resolve phylogeny: the trichotomy (H, C, G), in which the three lineages may have diverged from each other within a short period of time. In this period many of the ancestral polymorphisms apparently persisted and yielded phylogenetically incongruent signals. By contrast, no ancestral polymorphism is expected to have survived during the interval separating the divergences of the O, M, and T lineages from the ancestor of the (H, C, G) group. Any phylogenetic incompatibilities at sites in the O, M, and T lineages relative to the (H, C, G) group are therefore presumably the result of homoplasy. The frequency of homoplasy estimated in this manner is unexpectedly high: 12% for the (H, C, G) clade and 19% for the (H, C, G, O) clade. At least three-quarters of the 48% incompatibility observed in the (H, C) clade is attributable to the sorting out of ancestral polymorphisms coupled with intragenic recombination. Possible reasons for this high level of homoplasy in the O, M, and T lineages are discussed, and a computer simulation has been carried out to produce a model explaining the observed data.     

The evolution of virulence in primate malaria parasites based on Bayesian reconstructions of ancestral states

Plasmodium parasites, the causative agents of malaria, are generally considered as harmful parasites, but many of them cause mild symptoms. Little is known about the evolutionary history and phylogenetic constraints that generate this interspecific variation in virulence due to uncertainties about the phylogenetic associations of parasites. Here, to account for such phylogenetic uncertainty, phylogenetic methods based on Bayesian statistics were followed in combination with sequence data from five genes to estimate the ancestral state of virulence in primate Plasmodium parasites. When recent parasites were categorised according to the damage caused to the host, Bayesian estimates of ancestral states indicated that the acquisition of a harmful host exploitation strategy is more likely to be a recent evolutionary event than a result of an ancient change in a character state altering virulence. On the contrary, there was more evidence for moderate host exploitation having a deep origin along the phylogenetic tree. Moreover, the evolution of host severity is determined by the phylogenetic relationships of parasites, as severity gains did not appear randomly on the evolutionary tree. Such phylogenetic constraints can be mediated by the acquisition of virulence genes. As the impact of a parasite on a host is the result of both the parasite’s investment in reproduction and host sensitivity, virulence was also estimated by calculating peak parasitemia after eliminating host effects. A directional random-walk evolutionary model showed that the ancestral primate malarias reproduced at very low parasitemia in their hosts. Consequently, the extreme variation in the outcome of malaria infection in different host species can be better understood in light of the phylogeny of parasites.     

The definition,recognition, and interpretation of convergent evolution,and two new measures for quantifying and assessing the significance of convergence

Convergent evolution is an important phenomenon in the history of life. Despite this, there is no common definition of convergence used by biologists. Instead, several conceptually different definitions are employed. The primary dichotomy is between pattern‐based definitions, where independently evolved similarity is sufficient for convergence, and process‐based definitions, where convergence requires a certain process to produce this similarity. The unacknowledged diversity of definitions can lead to problems in evolutionary research. Process‐based definitions may bias researchers away from studying or recognizing other sources of independently evolved similarity, or lead researchers to interpret convergent patterns as necessarily caused by a given process. Thus, pattern‐based definitions are recommended. Existing measures of convergence are reviewed, and two new measures are developed. Both are pattern based and conceptually minimal, quantifying nothing but independently evolved similarity. One quantifies the amount of phenotypic distance between two lineages that is closed by subsequent evolution; the other simply counts the number of lineages entering a region of phenotypic space. The behavior of these measures is explored in simulations; both show acceptable Type I and Type II error. The study of convergent evolution will be facilitated if researchers are explicit about working definitions of convergence and adopt a standard toolbox of convergence measures.     

Life history evolution and genome size in subtribe Oncidiinae (Orchidaceae)

• Background and Aims Within Oncidiinae, there are severalgroups of species that are effectively annuals, and we wishedto see if these species had smaller genome sizes than averagefor the subtribe. • Methods Fifty-four genome size estimates (50 of whichare new) for species in subtribe Oncidiinae (Orchidaceae) wereexamined for the first time in a phylogenetic context to evaluatehypotheses concerning genome sizes and life history traits. • Results and Conclusions Within the limits of still relativelysparse sampling, the species that are effectively annuals doappear to have smaller genome sizes than average. However, thegenome sizes of their immediate sister group are also small,indicating that changes in genome size preceded the change inlife history traits. Genome sizes and chromosome numbers alsodo not correlate; some slowly growing species have lower chromosomenumbers but large genomes and vice versa. Based on a surveyof the literature on orchids, it is also clear that epiphyticspecies have smaller genome sizes than do terrestrial species,which could be an effect of different water relations or thefact that most terrestrial orchids are geophytic or have distinctgrowth and dormancy phases.     

Accelerated evolution and loss of a domain of the sperm-egg-binding protein SED1 in ancestral primates

Proteins involved in sperm-egg binding have been shown to evolve rapidly in several groups of invertebrates and vertebrates. Mammalian SED1 (secreted protein containing N-terminal Notch-like type II epidermal growth factor (EGF) repeats and C-terminal discoidin/F5/8 C domains) is a recently identified sperm surface protein that binds the egg zona pellucida and facilitates sperm-egg adhesion. SED1-null male mice are subfertile. Here we examine the SED1 gene from 11 mammalian species and provide evidence that it underwent accelerated evolution in ancestral primates, most likely driven by positive selection. Specifically, the intensity of the positive selection across various protein domains of SED1 was heterogeneous. Although one of the 2 Notch-like EGF domains, which mediate protein-protein binding, was lost in primate SED1, the second EGF domain evolved under strong positive selection favoring polar to nonpolar amino acid replacements. By contrast, the 2 discoidin/F5/8 type C domains, which are involved in protein-cell membrane binding, do not show definite signs of positive selection. The structural modification and occurrence of directional selection in ancestral primates but not any other lineage suggest that the function of SED1 may have changed during primate evolution. These results reveal a different evolutionary pattern of SED1 from that of many other sperm-egg-binding proteins, which often show diversifying selection occurring in multiple lineages.     

Rate heterogeneity, ancestral character state reconstruction, and the evolution of limb morphology in Lerista (Scincidae, Squamata)

Rates of phenotypic evolution derive from numerous interrelated processes acting at varying spatial and temporal scales and frequently differ substantially among lineages. Although current models employed in reconstructing ancestral character states permit independent rates for distinct types of transition (forward and reverse transitions and transitions between different states), these rates are typically assumed to be identical for all branches in a phylogeny. In this paper, I present a general model of character evolution enabling rate heterogeneity among branches. This model is employed in assessing the extent to which the assumption of uniform transition rates affects reconstructions of ancestral limb morphology in the scincid lizard clade Lerista and, accordingly, the potential for rate variability to mislead inferences of evolutionary patterns. Permitting rate variation among branches significantly improves model fit for both the manus and the pes. A constrained model in which the rate of digit acquisition is assumed to be effectively zero is strongly supported in each case; when compared with a model assuming unconstrained transition rates, this model provides a substantially better fit for the manus and a nearly identical fit for the pes. Ancestral states reconstructed assuming the constrained model imply patterns of limb evolution differing significantly from those implied by reconstructions for uniform-rate models, particularly for the pes; whereas ancestral states for the uniform-rate models consistently entail the reacquisition of pedal digits, those for the model incorporating among-lineage rate heterogeneity imply repeated, unreversed digit loss. These results indicate that the assumption of identical transition rates for all branches in a phylogeny may be inappropriate in modeling the evolution of phenotypic traits and emphasize the need for careful evaluation of phylogenetic tests of Dollo's law.     

Detection of "punctuated equilibrium" by bayesian estimation of speciation and extinction rates, ancestral character states, and rates of anagenetic and cladogenetic evolution on a molecular phylogeny

Algorithms are presented to simultaneously estimate probabilities of speciation and extinction, rates of anagenetic and cladogenetic phenotypic evolution, as well as ancestral character states, from a complete ultrametric species-level phylogeny with dates assigned to all bifurcations and one or more phenotypes in three or more extant species, using Metropolis-Hastings Markov Chain Monte Carlo sampling. The algorithms also estimate missing phenotypes of extant species and numbers of speciation events that occurred on all branches of the phylogeny. The algorithms are discussed and their performance is evaluated using simulated data. That evaluation shows that precise estimation of rates of evolution of one or a few phenotypes requires large phylogenies. Estimation accuracy improves with the number of species on the phylogeny.     

Shape at the cross‐roads: homoplasy and history in the evolution of the carnivoran skull towards herbivory

Patterns of skull shape in Carnivora provide examples of parallel and convergent evolution for similar ecomorphological adaptations. However, although most researchers report on skull homoplasies among hypercarnivorous taxa, evolutionary trends towards herbivory remain largely unexplored. In this study, we analyse the skull of the living herbivorous carnivorans to evaluate the importance of natural selection and phylogenetic legacy in shaping the skulls of these peculiar species. We quantitatively estimated shape variability using geometric morphometrics. A principal components analysis of skull shape incorporating all families of arctoid carnivorans recognized several common adaptations towards herbivory. Ancestral state reconstructions of skull shape and the reconstructed phylogenetic history of morphospace occupation more explicitly reveal the true patterns of homoplasy among the herbivorous carnivorans. Our results indicate that both historical constraints and adaptation have interplayed in the evolution towards herbivory of the carnivoran skull, which has resulted in repeated patterns of biomechanical homoplasy.     

Plastomic data shed new light on the phylogeny,biogeography, and character evolution of the family Crassulaceae

Crassulaceae is a mid-sized family of angiosperms, most species of which are herbaceous succulents, usually with 5-merous flowers and one or two whorls of stamens. Although previous phylogenetic studies revealed seven major “clades” in Crassulaceae and greatly improved our understanding of the evolutionary history of the family, relationships among major clades are still contentious. In addition, the biogeographic origin and evolution of important morphological characters delimiting infrafamilial taxa have not been subject to formal biogeographic and character evolution analyses based on a well-supported phylogeny backbone. In this study, we used plastomic data of 52 species, representing all major clades revealed in previous studies to reconstruct a robust phylogeny of Crassulaceae, based on which we unraveled the spatiotemporal framework of diversification of the family. We found that the family may originate in southern Africa and then dispersed to the Mediterranean, from there to eastern Asia, Macaronesia, and North America. The crown age of Crassulaceae was dated at ca. 63.93 million years ago, shortly after the Cretaceous–Paleogene (K-Pg) boundary. We also traced the evolution of six important morphological characters previously used to delimit infrafamilial taxa and demonstrated widespread parallel and convergent evolution of both vegetative (life form and phyllotaxis) and floral characters (number of stamen whorls, petals free or fused, and flower merism). Our results provide a robust backbone phylogeny as a foundation for further investigations, and also some important new insights into biogeography and evolution of the family Crassulaceae.     

The evolution of femoral osteology and soft tissues on the line to extant birds (Neornithes)

Femoral osteology and soft tissues evolved in a stepwise pattern in archosauromorph reptiles on the line to crown group birds. Crocodylia retains most ancestral archosaurian traits, whereas Dinosauromorpha (including birds) acquired many more derived traits. The complex sequence of changes included major shifts of several thigh muscle insertions. Medial rotation of the proximal femur (e.g. the femoral head) in archosaurs moved the greater trochanter laterally, bringing along the insertion of M. pubo-ischio-femoralis externus. Within Dinosauromorpha, the lesser trochanter moved proximally away from the trochanteric shelf. Presumably the lesser trochanter indicates the insertion of M. iliotrochantericus caudalis whereas the trochanteric shelf indicates the insertion of M. iliofemoralis externus. An accessory trochanter at the base of the lesser trochanter marks the insertion of M. pubo-ischio-femoralis internus 2 in tetanuran theropods. I propose hypotheses for the homologies of several intermuscular lines and other features on the femoral shaft. On the line to Neornithes, most changes of femoral morphology predated Aves and the origin of flight; few femoral features are unique to birds. Overall, the pattern of morphological evolution is consistent with stepwise functional evolution of the hindlimb within Dinosauromorpha on the line to Neornithes. The clade Ornithurae evolved the last few hindlimb apomorphies that characterize extant birds, in conjunction with more flexed hip and knee joints.     

Parallel evolution and ecological selection: replicated character displacement in spadefoot toads

Ecological character displacement—trait evolution stemming from selection to lessen resource competition between species—is most often inferred from a pattern in which species differ in resource-use traits in sympatry but not in allopatry, and in which sympatric populations within each species differ from conspecific allopatric populations. Yet, without information on population history, the presence of a divergent phenotype in multiple sympatric populations does not necessarily imply that there has been repeated evolution of character displacement. Instead, such a pattern may arise if there has been character displacement in a single ancestral population, followed by gene flow carrying the divergent phenotype into multiple, derived, sympatric populations. Here, we evaluate the likelihood of such historical events versus ongoing ecological selection in generating divergence in trophic morphology between multiple populations of spadefoot toad (Spea multiplicata) tadpoles that are in sympatry with a heterospecific and those that are in allopatry. We present both phylogenetic and population genetic evidence indicating that the same divergent trait, which minimizes resource competition with the heterospecific, has arisen independently in multiple sympatric populations. These data, therefore, provide strong indirect support for competition''s role in divergent trait evolution.     

The evolution of face processing in primates

The ability to recognize faces is an important socio-cognitive skill that is associated with a number of cognitive specializations in humans. While numerous studies have examined the presence of these specializations in non-human primates, species where face recognition would confer distinct advantages in social situations, results have been mixed. The majority of studies in chimpanzees support homologous face-processing mechanisms with humans, but results from monkey studies appear largely dependent on the type of testing methods used. Studies that employ passive viewing paradigms, like the visual paired comparison task, report evidence of similarities between monkeys and humans, but tasks that use more stringent, operant response tasks, like the matching-to-sample task, often report species differences. Moreover, the data suggest that monkeys may be less sensitive than chimpanzees and humans to the precise spacing of facial features, in addition to the surface-based cues reflected in those features, information that is critical for the representation of individual identity. The aim of this paper is to provide a comprehensive review of the available data from face-processing tasks in non-human primates with the goal of understanding the evolution of this complex cognitive skill.