Phylogeny of Recent Canidae (Mammalia, Carnivora): relative reliability and utility of morphological and molecular datasets

Zrzavý, J. & ?i?ánková, V. (2004). Phylogeny of Recent Canidae (Mammalia, Carnivora): relative reliability and utility of morphological and molecular datasets. — Zoologica Scripta, 33, 311–333. Phylogenetic relationships within the Canidae are examined, based on three genes (cytb, COI, COII) and 188 morphological, developmental, behavioural and cytogenetic characters. Both separate and combined phylogenetic analyses were performed. To inspect the phylogenetic ‘behaviour’ of individual taxa, basic phylogenetic analysis was followed by experimental cladistic analyses based on different data‐partition combinations and taxon‐removal analyses. The following phylogeny of the Recent Canidae is preferred: (1) Urocyon is the most basal canid; (2) Vulpes is a monophyletic genus (including Fennecus and Alopex); (3) the doglike canids (DC) form a clade (=Dusicyon + Pseudalopex + Lycalopex + Cerdocyon + Atelocynus + Chrysocyon + Speothos + Lycaon + Cuon + Canis), split into two subclades, South American and Afro‐Holarctic, with uncertain position of the Chrysocyon + Speothos subclade; (4) Canis is paraphyletic due to the position of Lycaon and Cuon. Otocyon and Nyctereutes are the most problematic canid genera, causing an unresolved branching pattern of Otocyon, Vulpes, Nyctereutes and DC clades. Reclassification of the two basal species of ‘Canis’ into separate genera is proposed (Schaeffia for ‘C.’ adustus, Lupulella for ‘C.’ mesomelas). Although the morphological dataset ranked poorly in both separate and simultaneous analyses (measured by number of minimum‐length topologies, relative number of resolved nodes in the strict consensus of all minimum‐length topologies, consistency and retention indices, nodal dataset influence, and number of extra steps required by the data partition to reach the topology of the combined tree), the morphological synapomorphies represent nearly one quarter of all synapomorphies in the combined tree. Among the hidden morphological support of the combined tree the developmental and behavioural characters are conspicuously abundant.     

Phylogeny and divergence of the pinnipeds (Carnivora: Mammalia) assessed using a multigene dataset

Background  

Phylogenetic comparative methods are often improved by complete phylogenies with meaningful branch lengths (e.g., divergence dates). This study presents a dated molecular supertree for all 34 world pinniped species derived from a weighted matrix representation with parsimony (MRP) supertree analysis of 50 gene trees, each determined under a maximum likelihood (ML) framework. Divergence times were determined by mapping the same sequence data (plus two additional genes) on to the supertree topology and calibrating the ML branch lengths against a range of fossil calibrations. We assessed the sensitivity of our supertree topology in two ways: 1) a second supertree with all mtDNA genes combined into a single source tree, and 2) likelihood-based supermatrix analyses. Divergence dates were also calculated using a Bayesian relaxed molecular clock with rate autocorrelation to test the sensitivity of our supertree results further.     

Phylogeny of the Procyonidae (Mammalia: Carnivora): molecules, morphology and the Great American Interchange

The Procyonidae (Mammalia: Carnivora) have played a central role in resolving the controversial systematics of the giant and red pandas, but phylogenetic relationships of species within the family itself have received much less attention. Cladistic analyses of morphological characters conducted during the last two decades have resulted in topologies that group ecologically and morphologically similar taxa together. Specifically, the highly arboreal and frugivorous kinkajou (Potos flavus) and olingos (Bassaricyon) define one clade, whereas the more terrestrial and omnivorous coatis (Nasua), raccoons (Procyon), and ringtails (Bassariscus) define another clade, with the similar-sized Nasua and Procyon joined as sister taxa in this latter group. These relationships, however, have not been tested with molecular sequence data. We examined procyonid phylogenetics based on combined data from nine nuclear and two mitochondrial gene segments totaling 6534bp. We were able to fully resolve relationships within the family with strongly supported and congruent results from maximum parsimony, maximum likelihood, minimum evolution, and Bayesian analyses. We identified three distinct lineages within the family: a (Nasua, Bassaricyon) clade, a (Bassariscus, Procyon) clade, and a Potos lineage, the last of which is sister to the other two clades. These findings, which are in strong disagreement with prior fossil and morphology-based assessments of procyonid relationships, reemphasize the morphological and ecological flexibility of these taxa. In particular, morphological similarities between unrelated genera possibly reflect convergence associated with similar lifestyles and diets rather than ancestry. Furthermore, incongruence between the molecular supermatrix and a morphological character matrix comprised mostly of dental characters [Baskin, J.A., 2004. Bassariscus and Probassariscus (Mammalia, Carnivora, Procyonidae) from the early Barstovian (Middle Miocene). J. Vert. Paleo. 24, 709-720] may be due to non-independence among atomized dental characters that does not take into account the high developmental genetic correlation of these characters. Finally, molecular divergence dating analyses using a relaxed molecular clock approach suggest that intergeneric and intrageneric splits in the Procyonidae mostly occurred in the Miocene. The inferred divergence times for intrageneric splits for several genera whose ranges are bisected by the Panamanian Isthmus is significant because they suggest diversification well precedes the Great American Interchange, which has long been considered a primary underlying mechanism for procyonid evolution.     

“Laughter” and “Smile” in Barbary Macaques (Macaca sylvanus)

In an observational study on semi-free Barbary macaques it was investigated whether the phylogenetic roots of human laughter and smile can be traced back to the genus Macaca. On the basis of morphological similarity a ‘relaxed open-mouth display’ as the phylogenetic precursor of the laughter, and a ‘silent bared-teeth display’ as the possible ancestor of the smile can be distinguished in the repertory of the Barbary macaque. Behavioural sequences from focal animal protocols were analyzed in order to establish message and meaning of both displays. Relaxed open-mouth display is regularly observed in the play interactions of juveniles. It is associated with partner-directed behaviour, it is frequently answered by a relaxed open-mouth display of the receiver, and accompanied by a special vocalization. Although up to 50% of the juvenile's play partners were higher ranking than themselves voluntary participation was the rule. Most characteristically, the behaviour patterns shown by both play partners are highly symmetrical and synchronized. Silent bared-teeth display is typically accompanied by evasive or submissive body movements, and occurs primarily in dyadic interactions, mainly by the lower ranking individual. It is not an unidirectional sign of a linear dominance hierarchy, though. Silent bared-teeth display is a frequent answer to aggressive behaviour shown by the receiver. After its performance, an increase of body contact between sender and receiver was observed. Behavioural sequences of senders and receivers are complementary, but lose their asymmetry after occurrence of the display. It is concluded that these results further support Van Hooff 's (1972) view that human laughter and smile have different phylogenetic roots: while silent bared-teeth display is a signal of submission and appeasement, relaxed open-mouth display is rightly called the ‘play face’, and is an expression of fun.     

Pair-rearing infant monkeys (Macaca nemestrina) using a “rotating-peer” strategy

Appropriate rearing conditions for captive primates are important for both research and breeding purposes. In an earlier study, pigtailed macaque infants that were pair-reared with a single continuous partner exhibited excessive social clinging and could not adapt to living in large social groups at 8–10 months of age. In the present study, eight macaques were pair-reared until they were 6 months old. Each member of an animal's four-monkey social group served as a home-cage partner. In an attempt to reduce excessive mutual clinging, the pairs were rotated every 2–3 days to increase the variability of social stimulation in the home cage. However, these infants developed abnormal social behaviors that were in some cases even more extreme than those exhibited by infants pair-reared with a single continuous partner. A second goal of this experiment was to study interlaboratory reliability for the development of social behavior. The animals were divided into two groups, one housed in a nursery and the other in a biological safety level 3 virus laboratory. Some differences were detected between the two groups, demonstrating the necessity of controls in biobehavioral developmental research. Am. J. Primatol. 41:141–149, 1997. © 1997 Wiley-Liss, Inc.     

Investigating South American biogeographic history using patterns of skull shape variation on Cerdocyon thous (Mammalia: Canidae)

Patterns of geographic variation of the canid Cerdocyon thous have historically been obscured by its remarkable intraspecific morphological variability. The observed distribution is highly associated with phytophysiognomy, a feature considered highly dynamic along geological time. In the present study, we tested whether vegetation distribution during the Holocene Glacial Maximum of South America (HGM) explains the patterns of morphological variation within Cerdocyon thous . The species was divided in groups according to paleohabitats that could support their presence during the HGM, and then tested for differences in skull morphometrics. The results obtained demonstrate that the climatic changes during the HGM influenced the population structure of this species, resulting in the establishment of geographical groups with different degrees of morphological cohesion. Higher morphological cohesion found in the Northern group might be explained by the marked discontinuity between its geographical range and the rest of the species'distribution. The Eastern and Southern morphological divergence is less striking and, although this could be related to past vegetation distribution, the disappearance of those barriers leads to a population structure that could be slowly breaking down.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 77–84.     

Mechanisms behind active trends in body size evolution of the Canidae (Carnivora: Mammalia)

Clade-level interactions can impart trends on observed characters. In this study, origination and extinction events were compiled for the three subfamilies of the Canidae (dogs): Hesperocyoninae, Borophaginae, and Caninae. These events were binned into 2-million-year time slices, and median body masses were calculated for each time slice. Originations and extinctions were classified as "large" or "small" relative to these median values. Likelihood ratios demonstrate that originations were significantly biased from random in four time slices, while extinctions were never significantly different from random. Two models were chosen by the Akaike Information Criterion to describe the evolutionary dynamics of canid body size. Both proposed a consistent, significant bias toward larger originations, punctuated by episodic "pulses" of increased bias toward larger originations and a Quaternary "pulse" favoring smaller originations, tracking the Quaternary diversification of foxlike canids. These pulses correspond in each subfamily to periods of rapid taxonomic diversification and the appearances of morphologies associated with hypercarnivorous diets. Together, the diversity data, the appearance of hypercarnivory, and the biases in originations document competitive interactions between Hesperocyoninae and Borophaginae and suggest that body size trends were driven, in part, by clade-level dynamics in the Canidae.     

Ecoregional Vulnerability Assessment for the Functional Richness of South American Carnivorans (Mammalia: Carnivora)

Mapping geographic trends in biodiversity is a key step in conservation planning, which has been mainly focused on taxonomic criteria or species of particular concern. More recently, higher consideration of ecosystem functioning has been advocated, allocating more attention to traits and functional diversity of species assemblages. Carnivorans (Mammalia: Carnivora) are charismatic, albeit threatened, species that variously affect ecosystem functioning through consumptive processes, and whose functional diversity depends on traits associated with their trophic habits and energetic requirements. Yet, analyses of spatial trends in the diversity and vulnerability of carnivoran assemblages have mostly focused on taxonomic and phylogenetic criteria. Then, the present study assessed the vulnerability of the functional richness of South American carnivoran assemblages, both at continental and regional levels. As a first diagnostic of vulnerability, the form of the association between functional richness and species richness (FRS) was assessed through simulations. The resulting nearly linear association indicated low functional redundancy and high sensitivity to global extinctions. A more realistic FRS accounting for actual extinction threats exacerbated losses of functional richness. Further, a positive correlation between effect and response traits suggests non-compensatory responses to environmental stressors by functionally redundant species and, thus, sensitivity of carnivoran functional richness to ongoing trends in land conversion and habitat degradation. Regionally, functional richness paralleled latitudinal gradients in species richness, but vulnerability did not entirely match these variables in space, nor did it risk estimates that accounted for regions’ conservation status. This suggests regional differentiation in conservation priorities, complementing existing taxonomically oriented prioritization schemes.     

In the Pursuit of the Predatory Behavior of Borophagines (Mammalia,Carnivora, Canidae): Inferences from Forelimb Morphology

Here, we perform an ecomorphological study on the major bones (humerus, radius, and ulna) of the carnivoran forelimb using three-dimensional geometric morphometrics. More specifically, we test the association between forelimb morphology and predatory behavior. Our results suggest that the main morphological adaptions of carnivorans to different predatory behaviors relate to: (i) the capacity to perform long and efficient runs as in pounce/pursuit and pursuit predators; (ii) the ability to maneuver as in occasional predators; and (iii) the capacity to exert and resist large loads as in ambushing predators. We used borophagine canids as a case study, given the controversy on the predatory behavior of this extinct subfamily. Our results indicate that borophagines displayed a limited set of adaptions towards efficient running, including reduced joint mobility in both the elbow and the wrist, aspects in which they resemble the living canids. Furthermore, they had forelimbs as powerful as those of the extant ambushing carnivorans (i.e., most felids). This combination of traits suggests that the predatory behavior of borophagines was unique among carnivorans, as it was not fully equivalent to any of the living species.     

The South American Gomphotheres (Mammalia, Proboscidea, Gomphotheriidae): Taxonomy, Phylogeny, and Biogeography

The taxonomic history of South American Gomphotheriidae is very complex and controversial. Three species are currently recognized: Amahuacatherium peruvium, Cuvieronius hyodon, and Notiomastodon platensis. The former is a late Miocene gomphothere whose validity has been questioned by several authors. The other two, C. hyodon and N. platensis, are Quaternary taxa in South America, and they have distinct biogeographic patterns: Andean and lowland distributions, respectively. South American gomphotheres became extinct at the end of the Pleistocene. We conducted a phylogenetic analysis of Proboscidea including the South American Quaternary gomphotheres, which resulted in two most parsimonious trees. Our results support a paraphyletic Gomphotheriidae and a monophyletic South American gomphothere lineage: C. hyodon and N. platensis. The late Miocene gomphothere record in Peru, Amahuacatherium peruvium, seems to be a crucial part of the biogeography and evolution of the South American gomphotheres.     

Genesis and structure of the so-called “balbiani body” or “yolk nucleus” in the oocyte of dugesia dorotocephala (turbellaria,tricladida)

Oogenesis of the fresh-water triclad Dugesia dorotocephala has been studied by electron microscopical methods, with particular regard to the genesis and composition of the so-called “Balbiani body.” Its origin is clearly recognizable in young oocytes where the few mitochondria present seem to gather at the level of the perinuclear ooplasm. Here they surround dense masses of finely granular, fibrillar material probably coming from the nucleus. During the previtelloge ic period, mitochondria rapidly increase in number while the dense masses progressively dissolve. In the vitellogenic oocytes the Balbiani body shows its final configuration: it appears as a large area (up to 15-20 pm in diameter) consisting of innumerable densely packed mitochondria, some smooth vesicles and free ribosomes. This aggregate of cytoplasmic organelles remains unmodified in the mature oocytes. The function of the “Balbiani body” of D. dorotocephala is as yet unclear; it can only be asserted that it is not correlated with yolk production in which the endoplasmic reticulum and the Golgi complex are involved.     

Phylogeny of the Carnivora (Mammalia): Congruence vs Incompatibility among Multiple Data Sets

The purpose of this study was to determine the higher-level phylogenetic relationships among Carnivora, using a conditional data combination (CDC) approach to analyzing multiple data sets. New nucleotide sequences (851 base pairs from intron I of the transthyretin gene) among 22 representatives of the 11 families of Carnivora were generated and analyzed in concert with, and comparison to, other mitochondrial and morphological character data. Conditional data combination analyses of the four independent data sets (transthyretin intron I, cytochromeb,partial 12S rRNA, and morphology) indicate that the phylogenetic results derived from each generally agree, with two exceptions. The first exception, signal heterogeneity in comparisons involving transthyretin and morphology, provides an example where phylogenetic conclusions drawn from total evidence analyses may differ from conclusions drawn from CDC analyses. The second exception demonstrates that while a CDC method may reject the null hypothesis of homogeneity for a particular partition, including that partition in combined analyses, may nevertheless provide an overall increase in phylogenetic signal, in terms of nodal support for most associations, without altering the topology derived from the combined homogeneous data partitions. Phylogenetic reconstruction among the feliform families supports a sister-group relationship between the hyaenas (Hyaenidae) and mongooses (Herpestidae) and places the African palm civet (Nandinia) as basal to all other living Feliformia. Among the caniform families, CDC analyses strongly support the previously enigmatic red panda (Ailurus) as a monotypic lineage that is sister to Musteloideasensu stricto(mustelids plus procyonids), in addition to pinniped monophyly and a sister-group relationship between the walrus and sea lions.     

A critique of the “ultra‐high risk” and “transition” paradigm

The transdiagnostic expression of psychotic experiences in common mental disorder (anxiety/depression/substance use disorder) is associated with a poorer prognosis, and a small minority of people may indeed develop a clinical picture that meets criteria for schizophrenia. However, it appears neither useful nor valid to observe early states of multidimensional psychopathology in young people through the “schizo”‐prism, and apply misleadingly simple, unnecessary and inefficient binary concepts of “risk” and “transition”. A review of the “ultra‐high risk” (UHR) or “clinical high risk” (CHR) literature indicates that UHR/CHR samples are highly heterogeneous and represent individuals diagnosed with common mental disorder (anxiety/depression/substance use disorder) and a degree of psychotic experiences. Epidemiological research has shown that psychotic experiences are a (possibly non‐causal) marker of the severity of multidimensional psychopathology, driving poor outcome, yet notions of “risk” and “transition” in UHR/CHR research are restrictively defined on the basis of positive psychotic phenomena alone, ignoring how baseline differences in multidimensional psychopathology may differentially impact course and outcome. The concepts of “risk” and “transition” in UHR/CHR research are measured on the same dimensional scale, yet are used to produce artificial diagnostic shifts. In fact, “transition” in UHR/CHR research occurs mainly as a function of variable sample enrichment strategies rather than the UHR/CHR “criteria” themselves. Furthermore, transition rates in UHR/CHR research are inflated as they do not exclude false positives associated with the natural fluctuation of dimensional expression of psychosis. Biological associations with “transition” thus likely represent false positive findings, as was the initial claim of strong effects of omega‐3 polyunsatured fatty acids in UHR samples. A large body of UHR/CHR intervention research has focused on the questionable outcome of “transition”, which shows lack of correlation with functional outcome. It may be more productive to consider the full range of person‐specific psychopathology in all young individuals who seek help for mental health problems, instead of “policing” youngsters for the transdiagnostic dimension of psychosis. Instead of the relatively inefficient medical high‐risk approach, a public health perspective, focusing on improved access to a low‐stigma, high‐hope, small scale and youth‐specific environment with acceptable language and interventions may represent a more useful and efficient strategy.     

“Capacity”, “best interests”, “will and preferences” and the UN Convention on the Rights of Persons with Disabilities

The United Nations (UN) Convention on the Rights of Persons with Disabilities (CRPD) is the most up‐to‐date international legal instrument concerning the rights of persons with disabilities. Such persons are taken to include those with serious mental disorders. According to an authoritative interpretation of a crucial Article (Article 12 ‐ Equal recognition before the law) by the UN CRPD Committee, involuntary detention and treatment of people with mental health disabilities are prohibited under the Convention. Both conventional mental health law and “capacity‐based” law are deemed to violate the Convention. However, some other UN bodies are not in full agreement (for example, the UN Human Rights Committee and the Subcommittee on Prevention of Torture and Other Cruel, Inhuman or Degrading Treatment or Punishment), while others are less explicitly absolutist (for example, the Human Rights Council). Furthermore, strong criticisms of the position of the CRPD Committee have been mounted from a number of academic quarters. These criticisms center on whether the role of a person's ability to make a decision can be ignored, no matter the circumstances. Much of the above debate turns on the concept of “legal capacity” and the now often‐repeated precept that one must always respect the “will and preferences” of the person with a disability. However, “will and preferences” remains undefined. In this paper, I offer an analysis of “will and preferences” that can clarify interventions that may be acceptable or non‐acceptable under the terms of the UN Convention.     

Corrigenda to “estimation of stature from long limb bones of American Whites and Negroes,” American Journal Physical Anthropology (1952)

The amount of disparity between the lengths of the radii and ulnae of 177 Negro female skeletons of the Terry Collection was questioned. An error was found and corrections have been made in the relevant statistics and tables.     

Distribution of the Character States “Early Sympetaly” and “Late Sympetaly” Within the “Sympetalae Tetracyclicae” and Presumably Allied Groups*

Within the Asteridae (“Sympetalae Tetracyclicae”) two main developmental patterns can be distinguished as regards the formation of corolla tubes, namely “early” and “late sympetaly”. Since the character “ontogeny of sympetaly”, after intensive studies, proved to be valuable for systematic considerations, we now recognize two blocks of orders within the Asteridae (and related groups): the Asteridae A-block and the Asteridae B-block (Figs. 82 and 83). By and large this bipartition referring mainly to the corolla tube development corresponds well with major lineages indentified by recent molecular data (see, e.g., Chase et al., 1993). Asteridae A-block is characterized predominantely by “late sympetaly” the “early sympetaly” in Rubiales and Oleales can be interpreted as derived within this block or can be linked with that in Asteridae B-block. Asteridae B-block is uniform throughout in its “early sympetaly”. In this block it is a primitive character, as judged from its occasional occurrence in the choripetalous Cornales and Apiales (Apiaceae, Araliaceae, Pittosporaceae), which can be regarded as ancestral for block B.