Infant carrying in family groups of goeldi's monkeys (Callimico goeldii)

Goeldi's monkey (Callimico goeldii) is closely related to marmosets and tamarins. Like marmosets and tamarins, C. goeldii lives in family groups, and fathers and older offspring (helpers) participate in infant carrying. In contrast to the typical twin births in marmosets and tamarins, C. goeldii has only single offspring, and paternal carrying is delayed. We studied infant carrying following 26 births in eight groups of C. goeldii, testing hypotheses proposed in the literature on infant carrying in marmosets and tamarins. The infant was carried exclusively by the mother for the first 26.3 days after birth. Afterwards other group members participated in infant carrying. Whereas the C. goeldii mother is always the main carrier, the father does not always carry more than helpers. In contrast to other callitrichids, age and sex of sibling helpers was not found to have an effect on the participation in infant carrying. The participation in infant carrying in Callimico indicated intraindividual consistency, i.e., the amount of infant carrying performed by fathers and helpers following one birth correlated significantly with the amount of infant carrying of the same individuals following the next birth. We found a significant negative correlation between parental infant carrying and group size, indicating that helpers really do help, sharing the carrying burden with their parents. This is attributed to a clear trend for a reduction in maternal carrying in the presence of helpers, whereas fathers did not benefit from helpers. We conclude that the infant-carrying pattern in C. goeldii is different from the infant-carrying pattern in marmosets and tamarins. The main differences were that the mother instead of the father is the main carrier, and that there is a clear time delay between infant birth and when the father and helpers participate in infant carrying.     

Hormonal monitoring of age at sexual maturation in female Goeldi's monkeys (Callimico goeldii) in their family groups

The aim of this study was to determine whether or not sexual maturation is attained in the family group in captive‐born Goeldi's monkey (Callimico goeldii) and if so, at what age and body weight. To monitor ovarian activity in 14 female Goeldi's monkeys, urinary content of pregnanediol‐3α‐glucuronide (PdG) was determined using radioimmunoassay. Urinary samples were collected between the ages of 6 and 70 weeks. Subjects became sexually mature while still housed in their family groups, at a median age of 57 weeks (48–< 70 weeks). Median body weight at the age of sexual maturity was 473 g (N = 10; 420–543 g). This corresponded to 90% of the median non‐pregnant body weight of breeding females in our colony (526 g, N = 8). Therefore, Goeldi's monkey is similar to Leontopithecus but different from Cebuella, Callithrix, and Saguinus, in terms of daughters ovulating in the family group and at a relatively young age. Am. J. Primatol. 48:77–83, 1999. © 1999 Wiley‐Liss, Inc.     

Phylogenomics of species from four genera of New World monkeys by flow sorting and reciprocal chromosome painting

Background

The taxonomic and phylogenetic relationships of New World monkeys (Platyrrhini) are difficult to distinguish on the basis of morphology and because diagnostic fossils are rare. Recently, molecular data have led to a radical revision of the traditional taxonomy and phylogeny of these primates. Here we examine new hypotheses of platyrrhine evolutionary relationships by reciprocal chromosome painting after chromosome flow sorting of species belonging to four genera of platyrrhines included in the Cebidae family: Callithrix argentata (silvered-marmoset), Cebuella pygmaea (pygmy marmoset), Callimico goeldii (Goeldi's marmoset) and Saimiri sciureus (squirrel monkey). This is the first report of reciprocal painting in marmosets.

Results

The paints made from chromosome flow sorting of the four platyrrhine monkeys provided from 42 to 45 hybridization signals on human metaphases. The reciprocal painting of monkey probes on human chromosomes revealed that 21 breakpoints are common to all four studied species. There are only three additional breakpoints. A breakpoint on human chromosome 13 was found in Callithrix argentata, Cebuella pygmaea and Callimico goeldii, but not in Saimiri sciureus. There are two additional breakpoints on human chromosome 5: one is specific to squirrel monkeys, and the other to Goeldi's marmoset.

Conclusion

The reciprocal painting results support the molecular genomic assemblage of Cebidae. We demonstrated that the five chromosome associations previously hypothesized to phylogenetically link tamarins and marmosets are homologous and represent derived chromosome rearrangements. Four of these derived homologous associations tightly nest Callimico goeldii with marmosets. One derived association 2/15 may place squirrel monkeys within the Cebidae assemblage. An apparently common breakpoint on chromosome 5q33 found in both Saimiri and Aotus nancymae could be evidence of a phylogenetic link between these species. Comparison with previous reports shows that many syntenic associations found in platyrrhines have the same breakpoints and are homologous, derived rearrangements showing that the New World monkeys are a closely related group of species. Our data support the hypothesis that the ancestral karyotype of the Platyrrhini has a diploid number of 2n = 54 and is almost identical to that found today in capuchin monkeys; congruent with a basal position of the Cebidae among platyrrhine families.

     

Multi-directional chromosome painting maps homologies between species belonging to three genera of New World monkeys and humans

We mapped chromosomal homologies in two species of Chiropotes (Pitheciini, Saki Monkeys) and one species of Aotus (Aotinae, Owl Monkey) by multi-directional chromosome painting. Human chromosome probes were hybridized to Chiropotes utahicki, C. israelita and Aotus nancymae metaphases. Wooly Monkey chromosome paints were also hybridized to Owl Monkey metaphases. We established Owl Monkey chromosome paint probes by flow sorting and reciprocally hybridized them to human chromosomes. The karyotypes of the Bearded Saki Monkeys studied here are close to the hypothesized ancestral platyrrhine karytoype, while that of the Owl Monkey appears to be highly derived. The A. nancymae karyotype is highly shuffled and only three human syntenic groups were found conserved coexisting with 17 derived human homologous associations. A minimum of 14 fissions and 13 fusions would be required to derive the A. nancymae karyotype from that of the ancestral New World primate karyotype. An inversion between homologs to segments of human 10 and 16 suggests a link between Callicebus and Chiropotes, while the syntenic association of 10/11 found in Aotus and Callicebus suggests a link between these two genera. Future molecular cytogenetic work will be needed to determine whether these rearrangements represent synapomorphic chromosomal traits.     

A comparative study of the recombination pattern in three species of Platyrrhini monkeys (primates)

Homologous chromosomes exchange genetic information through recombination during meiotic synapsis, a process that increases genetic diversity and is fundamental to sexual reproduction. Meiotic studies in mammalian species are scarce and mainly focused on human and mouse. Here, the meiotic recombination events were determined in three species of Platyrrhini monkeys (Cebus libidinosus, Cebus nigritus and Alouatta caraya) by analysing the distribution of MLH1 foci at the stage of pachytene. Moreover, the combination of immunofluorescence and fluorescent in situ hybridisation has enabled us to construct recombination maps of primate chromosomes that are homologous to human chromosomes 13 and 21. Our results show that (a) the overall number of MLH1 foci varies among all three species, (b) the presence of heterochromatin blocks does not have a major influence on the distribution of MLH1 foci and (c) the distribution of crossovers in the homologous chromosomes to human chromosomes 13 and 21 are conserved between species of the same genus (C. libidinosus and C. nigritus) but are significantly different between Cebus and Alouatta. This heterogeneity in recombination behaviour among Ceboidea species may reflect differences in genetic diversity and genome composition.     

Investigation of marmoset hybrids (Cebuella pygmaea x Callithrix jacchus) and related Callitrichinae (Platyrrhini) by cross-species chromosome painting and comparative genomic hybridization

We report on the cytogenetics of twin offspring from an interspecies cross in marmosets (Callitrichinae, Platyrrhini), resulting from a pairing between a female Common marmoset (Callithrix jacchus, 2n = 46) and a male Pygmy marmoset (Cebuella pygmaea, 2n = 44). We analyzed their karyotypes by multi-directional chromosome painting employing human, Saguinus oedipus and Lagothrix lagothricha chromosome-specific probes. Both hybrid individuals had a karyotype with a diploid chromosome number of 2n = 45. As a complementary tool, interspecies comparative genomic hybridization (iCGH) was performed in order to screen for genomic imbalances between the hybrids and their parental species, and between Callithrix argentata and S. oedipus, respectively. These genomic imbalances were confined to centromeric and telomeric heterochromatin, while euchromatic chromosome regions appeared balanced in all species investigated. When comparing marmosets and tamarins, sequence divergence of centromeric heterochromatin was already clearly noticeable. In the C. argentata and C. pygmaea genomes numerous subtelomeric regions were affected by amplification of different repetitive sequences. Cross-species FISH with a microdissection-derived C. pygmaea repetitive probe revealed species specificity of this repetitive sequence at the molecular cytogenetic level of resolution.     

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.     

A classification of the New World species of Aster (Asteraceae)

In order effectively to list and comment on the results of cytological investigations inAster in a companion paper, a scheme of infrageneric classification is presented which utilizes the basic chromosome number as a pivotal diagnostic character. Reasons are stated as to why, with the exception ofUnamia Greene which is transferred toSolidago, and the commonly recognized generaLeucelene Greene,Machaeranthera Nees andXylorhiza Nutt., none of the segregate genera previously proposed or recorded in the literature is upheld. Instead, these taxa are being given subgeneric or sectional rank. Two additional subgenera are established to accommodate the species groups traditionally placed in “Aster proper,” which are characterized by having basic chromosome numbers ofx = 5 andx = 8, respectively. Altogether ten subgenera of the genusAster, five of them subdivided further into a total of 24 sections, are recognized as having representative species in the New World. All basionyms and type species are listed, and a number of new combinations and status changes are validated in accordance with the International Rules of Botanical Nomenclature. Where known (from literature and personal research), chromosome numbers are recorded for the species.     

Description of the cytochrome c oxidase subunit II gene in some genera of New World monkeys (primates,Platyrrhini)

Nucleotide sequence variation at the mitochondrial cytochrome c oxidase subunit II gene (COII) was analyzed in 27 New World monkey specimens, nine newly reported herein. The study involved comparisons among platyrrhines and also between platyrrhines and catarrhines. The analysis of the frequencies of transitions and transversions at each codon position showed transitional saturation at third codon position. Neighbor-Joining trees obtained from genetic distances estimated by means of Kimura's (1980) two-parameter model showed poor resolution of phylogenetic relationships among platyrrhine genera. Rates of nucleotide substitutions were largely homogeneous except in the genus Saimiri that showed low numbers of unique substitutions suggesting the maintenance of ancestral or plesiomorphic states of platyrrhine mt DNA nucleotide characters probably due to its large population sizes as compared to other platyrrhines.     

Molecular evidence of cryptic species within the Liriomyza huidobrensis (Diptera: Agromyzidae)

Phylogenetic relationships among populations of the polyphagous pea leafminer, Liriomyza huidobrensis (Blanchard), were investigated using DNA sequence data. Maximum parsimony analysis of 941 bp of mitochondrial cytochrome oxidase I and II genes showed that L. huidobrensis contains two well-defined monophyletic groups, one composed of specimens from California and Hawaii and one composed of specimens from South and Central America together with populations that have been recently introduced into other parts of the world. The differentiation between the two clades within L. huidobrensis is equivalent to that seen between other agromyzid species, suggesting that L. huidobrensis as currently defined contains two cryptic species. This finding is consistent with field observations of differences in pest status and insecticide resistance between L. huidobrensis populations. Until additional studies are complete, no changes in L. huidobrensis taxonomy are proposed. However, researchers and quarantine officials may wish to consider the findings of the current study in designing research, pest management, and quarantine programs for L. huidobrensis.     

Chromosomal localization of the telomeric (TTAGGG)n sequence in eight species of New World Primates (Neotropical Primates, Platyrrhini)

Chromosomal localization of the telomeric sequence (TTAGGG)(n) in eight New World Primates (Platyrrhini) (Alouatta caraya, Alouatta palliata, Alouatta guariba clamitans, Aotus azarae, Ateles chamek, Cebus nigritus, Cebus paraguayanus, and Saimiri boliviensis) using Fluorescence In Situ Hybridization (FISH) with a peptide nucleic acid (PNA) pantelomeric probe and their possible relationship with the C-banding pattern were analyzed. FISH showed telomeric signals only at the terminal regions of chromosomes from all the species analyzed. Although all of them showed centromeric C+ bands and different size and location of extracentromeric C+ bands, none, except Aotus azarae exhibited (peri)centromeric interstitial telomere-like sequences (ITS). The presence of ITS in Aotus azarae was limited to one pair of submetacentric chromosomes and very likely represents telomeric sequences remaining after a fusion event of ancestral chromosomes during karyotype evolution. Therefore, our data indicate that the distribution of heterochromatin blocks do not correlate with the presence of ITS. However, we cannot rule out the possibility that simple ITS arrays with a few copies of the (TTAGGG)(n) sequence, not detectable by conventional FISH, might play a role in the karyotypic evolution of Ceboidea. Further FISH and molecular studies will be needed to confirm this hypothesis.     

Molecular phylogeny of the New World monkeys (Platyrrhini,primates) based on two unlinked nuclear genes: IRBP intron 1 and ϵ-globin sequences

Nuclear sequences of the 1.8 kilobase (kb) long intron 1 of the interstitial retinol-binding protein gene (IRBP), previously determined for 11 of the 16 extant genera of New World monkeys (superfamily Ceboidea, infraorder Platyrrhini), have now been determined for the remaining 5 genera. The maximum parsimony trees found, first with IRBP sequences alone and then with tandemly combined IRBP and ϵ-globin gene sequences from the same species, supported a provisional cladistic classification with the following clusters. Subtribes Callitrichina (Callithrix, Cebuella), Callimiconina (Callimico), Leontopithecina (Leontopithecus) and Saguina (Saguinus) constitute subfamily Callitrichinae, and subfamilies Callitrichinae, Aotinae (Aotus), and Cebinae (Cebus, Saimiri) constitute family Cebidae. Subtribes Chiropotina (Chiropotes, Cacajao) and Pitheciina (Pithecia) constitute tribe Pitheciini; and tribes Pitheciini and Callicebini (Callicebus) constitute subfamily Pitheciinae. Subtribes Brachytelina (Brachyteles, Lagothrix) and Atelina (Ateles) constitute tribe Atelini, and tribes Atelini and Alouattini (Alouatta) constitute subfamily Atelinae. The parsimony results were equivocal as to whether Pitheciinae should be grouped with Atelinae in family Atelidae or have its own family Pitheciidae. The cladistic groupings of extant ceboids were also examined by different stochastic evolutionary models that employed the same stochastic process of nucleotide substitutions but alternative putative phylogenetic trees on which the nucleotide substitutions occurred. Each model, i.e., each different tree, predicted a different multinomial distribution of nucleotide character patterns for the contemporary sequences. The predicted distributions that were closest to the actual observed distributions identified the best fitting trees. The cladistic relationships depicted in these best fitting trees agreed in almost all cases with those depicted in the maximum parsimony trees. © 1996 Wiley-Liss, Inc.     

Divergence Times and the Evolutionary Radiation of New World Monkeys (Platyrrhini,Primates): An Analysis of Fossil and Molecular Data

The estimation of phylogenetic relationships and divergence times among a group of organisms is a fundamental first step toward understanding its biological diversification. The time of the most recent or last common ancestor (LCA) of extant platyrrhines is one of the most controversial among scholars of primate evolution. Here we use two molecular based approaches to date the initial divergence of the platyrrhine clade, Bayesian estimations under a relaxed-clock model and substitution rate plus generation time and body size, employing the fossil record and genome datasets. We also explore the robustness of our estimations with respect to changes in topology, fossil constraints and substitution rate, and discuss the implications of our findings for understanding the platyrrhine radiation. Our results suggest that fossil constraints, topology and substitution rate have an important influence on our divergence time estimates. Bayesian estimates using conservative but realistic fossil constraints suggest that the LCA of extant platyrrhines existed at ca. 29 Ma, with the 95% confidence limit for the node ranging from 27–31 Ma. The LCA of extant platyrrhine monkeys based on substitution rate corrected by generation time and body size was established between 21–29 Ma. The estimates based on the two approaches used in this study recalibrate the ages of the major platyrrhine clades and corroborate the hypothesis that they constitute very old lineages. These results can help reconcile several controversial points concerning the affinities of key early Miocene fossils that have arisen among paleontologists and molecular systematists. However, they cannot resolve the controversy of whether these fossil species truly belong to the extant lineages or to a stem platyrrhine clade. That question can only be resolved by morphology. Finally, we show that the use of different approaches and well supported fossil information gives a more robust divergence time estimate of a clade.     

Molecular phylogeny of ateline new world monkeys (Platyrrhini, atelinae) based on gamma-globin gene sequences: evidence that brachyteles is the sister group of lagothrix

Nucleotide sequences, each spanning approximately 7 kb of the contiguous gamma1 and gamma2 globin genomic loci, were determined for seven species representing all extant genera (Ateles, Lagothrix, Brachyteles, and Alouatta) of the New World monkey subfamily Atelinae. After aligning these seven ateline sequences with outgroup sequences from several other primate (non-ateline) genera, they were analyzed by maximum parsimony, maximum likelihood, and neighbor-joining algorithms. All three analyzes estimated the same phylogenetic relationships: [Alouatta [Ateles (Brachyteles, Lagothrix)]]. Brachyteles and Lagothrix are sister-groups supported by 100% of bootstrap replications in the parsimony analyses. Ateles joins this clade, followed by the basal genus Alouatta; these joinings were strongly supported, again with 100% bootstrap values. This cladistic pattern for the four ateline genera is congruent with that obtained in previous studies utilizing epsilon-globin, IRBP, and G6PD nuclear genomic sequences as well as mitochondrial COII sequences. Because the number of aligned nucleotide positions is much larger in the present datasetoff than in any of these other datasets, much stronger support was obtained for the cladistic classification that divides subfamily Atelinae into tribes Alouattini (Alouatta) and Atelini, while the latter divides into subtribes Atelina (Ateles) and Brachytelina (Brachyteles and Lagothrix).     

Karyotype evolution of eulipotyphla (insectivora): the genome homology of seven sorex species revealed by comparative chromosome painting and banding data

The genus Sorex is one of the most successful genera of Eulipotyphla. Species of this genus are characterized by a striking chromosome variability including XY1Y2 sex chromosome systems and exceptional chromosomal polymorphisms within and between populations. To study chromosomal evolution of the genus in detail, we performed cross-species chromosome painting of 7 Sorex species with S. granarius and S. araneus whole-chromosome probes and found that the tundra shrew S. tundrensis has the most rearranged karyotype among these. We reconstructed robust phylogeny of the genus Sorex based on revealed conserved chromosomal segments and syntenic associations. About 16 rearrangements led to formation of 2 major Palearctic groups after their divergence from the common ancestor: the S. araneus group (10 fusions and 1 fission) and the S. minutus group (5 fusions). Further chromosomal evolution of the 12 species inside the groups, including 5 previously investigated species, was accompanied by multiple reshuffling events: 39 fusions, 20 centromere shifts and 10 fissions. The rate of chromosomal exchanges upon formation of the genus was close to the average rate for eutherians, but increased during recent (about 6-3 million years ago) speciation within Sorex. We propose that a plausible ancestral Sorex karyotype consists of 56 elements. It underwent 20 chromosome rearrangements from the boreoeutherian ancestor, with 14 chromosomes retaining the conserved state. The set of genus-specific chromosome signatures was drawn from the human (HSA)-shrew comparative map (HSA3/12/22, 8/19/3/21, 2/13, 3/18, 11/17, 12/15 and 1/12/22). The syntenic association HSA4/20, that was previously proposed as a common trait of all Eulipotyphla species, is shown here to be an apomorphic trait of S. araneus.     

Molecular phylogenetics reveals a pattern of biome conservatism in New World anchovies (family Engraulidae)

Evolutionary transitions between marine and freshwater biomes are relatively rare events, yielding a widespread pattern of biome conservatism among aquatic organisms. We investigated biome transitions in anchovies (Engraulidae), a globally distributed clade of economically important fishes. Most anchovy species are near-shore marine fishes, but several exclusively freshwater species are known from tropical rivers of South America and were previously thought to be the product of six or more independent freshwater invasions. We generated a comprehensive molecular phylogeny for Engraulidae, including representatives from 15 of 17 currently recognized genera. Our data support previous hypotheses of higher-level relationships within Engraulidae, but show that most New World genera are not monophyletic and in need of revision. Ancestral character reconstruction reveals that New World freshwater anchovies are the product of a single marine to freshwater transition, supporting a pattern of biome conservatism. We argue that competition is the principal mechanism that regulates aquatic biome transitions on a continental scale.     

Molecular and morphological evidence for an origin of the aberrant genus Milula within himalayan species of Allium (Alliacae)

Phylogenetic relationships between Allium and the monotypic Himalayan genus Milula were analyzed using sequences of the nuclear ribosomal DNA internal transcribed spacer (ITS) region and of the intergenic spacers from the chloroplast trnD(GUC)-trnT(GGU) region. Both marker systems unambiguously placed Milula spicata within Allium subgenus Rhizirideum, close to A. cyathophorum. Morphologically, the main difference between Allium and Milula is the conspicuous spicate inflorescence of Milula vs the mostly capitate or umbellate inflorescences in Allium. Anatomical investigations of leaf characters support a close relationship of Milula with A. cyathophorum and A. mairei, whereas root characters are distinctive from other species of section Cyathophora. To maintain Allium as monophyletic, Milula has been included as A. spicatum in Allium subgenus Rhizirideum.     

A comparative analysis of the mole vole sibling species Ellobius tancrei and E. talpinus (Cricetidae, Rodentia) through chromosome painting and examination of synaptonemal complex structures in hybrids

A comparative genomic analysis was carried out in the mole vole sibling species Ellobius tancrei and E. talpinus. Performing fluorescent in situ hybridisation (Zoo-FISH) using chromosome paints from the field vole Microtus agrestis showed no differences in the allocation of syntenic groups in the karyotypes of these sibling species. The only difference between their karyotypes was the position of the centromere in one pair of chromosomes, which is assumed to be the result of an inversion. To verify this hypothesis, we analysed chromosome synapsis in prophase I of meiosis. We utilised a synaptonemal complex (SC) surface-spreading technique to visualise the process of chromosome synapsis in the spermatocytes and oocytes of first-generation hybrids and back-crosses of these sibling species. In prophase I of meiosis, immunocytochemical and electron microscopy analyses revealed that all bivalents had been fully adjusted. Even in the case of a submetacentric-acrocentric bivalent with different centromere locations, synapsis of SC lateral elements was fulfilled along the entire length of the chromosomes and the formation of an inversion loop was not observed. We hypothesise that a possible mechanism leading to the change in centromere position is the repositioning and/or generation of a neocentromere. Despite the great similarity in the karyotypes of these sibling species, they exhibited significant genomic diversification, which manifested as hybrid sterility and parous female death.     

Molecular phylogenetic analysis of Fringillidae, "New World nine-primaried oscines" (Aves: Passeriformes)

Systematic studies of Fringillidae have long been problematic due to their apparent recent and explosive diversification. We present phylogenetic hypotheses of 44 fringillids that represent the overall diversity of the family, based on 3.2 kb of mitochondrial DNA sequences, and phylogenetic analyses for a subset of fringillids based on new and published mitochondrial cytochrome b sequences. Monophyly of Fringillidae and its two constituent subfamilies, Fringillinae and Emberizinae, was consistently supported with the exceptions of Peucedramus being placed outside of Fringillinae and Euphonia being placed within Fringillinae instead of within Emberizinae. Within Emberizinae, Thraupini (tanagers), Cardinalini (cardinals and grosbeaks), and Emberizini (New World sparrows) did not form separate monophyletic groups. Our results indicate that Emberizinae consists of three clades, each with a different overall geographical distribution. Several taxa traditionally considered members of Thraupini fall outside of the thraupine clade, including the only North American genus, Piranga. Consequently, the thraupine clade includes only Neotropical species. Increasing evidence suggests that Fringillidae, often called "New World nine-primaried oscines," does not in fact have a New World origin.