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Complete mitochondrial genome of Critically Endangered Blue-throated Macaw (Ara glaucogularis): Its comparison with partial mitogenome of Scarlet Macaw (Ara macao)
Abstract
Abstract Blue-throated Macaw (Ara glaucogularis) is Critically Endangered species of parrot endemic to small Bolivian area. In this study, full mitochondrial genome of considered species was sequenced. It is 16,983 bp long and contains 13 protein-coding genes, 2 rRNAs, 22 tRNAs and a control region. It`s comparison with published Ara macao mitogenome revealed their high degree of identity. On the other hand, analysis of both the genome compositions showed incompleteness of Ara macao CYTB gene. Hence, mitogenome of Ara macao species occurred only partial sequence. In consequence, Ara glaucogularis mitogenome is the first complete Macaw sequence, which will be indispensable to refine the phylogenetic relationships within the tribe Arini and will enrich the resource of markers for systematic, phylogenetic and population genetic studies.
... So far, only one representative mitogenome of each morphological pair of large Ara species was sequenced (Seabury et al., 2013;Urantowka, 2014Urantowka, , 2015. Therefore, in this study, A. ararauna mitogenome (living captive individual) was sequenced (16 982 bp; GeneBank accession no. ...
... KF010315) to gain a source of molecular data appropriate for future examination of evolutionary diversification of Macaws. The mitogenome revealed gene arrangement previously reported for other Ara species (Urantowka, 2014(Urantowka, , 2015. The sequence was also compared with A. glaucogularis mtDNA and comparison of these sequences showed their 94.06% identity. ...
Six genera of the Arini tribe form morphologically diverse group termed as Macaws. The presence of bare facial area distinguishes them from other members of the tribe. Genera and species of Macaw group differ in pattern of this bare skin as well as in body size. The genus Ara contains eight extant species. Two of them are classified as medium-sized Macaws and other six species are classified as large Macaws. Based on morphological similarities and differences, large Macaw species can be segregated into three pairs according to their plumage coloration. So far, representative mitochondrial genomes were sequenced only for Ara glaucogularis (blue and yellow coloration), Ara macao (predominantly red/scarlet) and Ara militaris (predominantly green) species. Ara ararauna is the second of two Ara species with predominant blue and yellow plumage. Hitherto, close phylogenetic relation of these two species was shown using only ND2 genes or incomplete combined COI/Cytb/ND2 sequences. Therefore, Ara ararauna mitogenome, which was sequenced in this study, will be indispensable to refine the phylogenetic relationships within Macaws group.
... Here, we report the first mitogenome of Aratinga, Aratinga solstitialis (GenBank accession no. JX441869) and compared it with other Arini representatives: Ara glaucogularis (Urantowka 2016), Eupsittula pertinax (Pacheco et al. 2011), Psittacara mitratus (Urantowka et al. 2016a), Pyrrhura rupicola (Urantowka et al. 2016b), and Thectocercus acuticaudatus (Urantowka et al. 2013). A phylogenetic analysis confirmed undoubtedly that the obtained mtDNA belongs to Aratinga solstitialis ( Figure 1). ...
Arini with 19 genera is the most diversified tribe of the neotropical parrots from Arinae subfamily. So far, among this tribe, the genus Aratinga appeared to be the most problematic for the taxonomists. The typical representative of this genus is Aratinga solstitialis, whose complete mitochondrial genome were sequenced and compared with five other representatives of Arini mitogenomes. Despite the conservatism in their general organization, some changes in A + T% composition of individual genes, start/stop codon usage and intergenic regions accumulated during evolution.
Background
Conures are a morphologically diverse group of Neotropical parrots classified as members of the tribe Arini, which has recently been subjected to a taxonomic revision. The previously broadly defined Aratinga genus of this tribe has been split into the ‘true’ Aratinga and three additional genera, Eupsittula, Psittacara and Thectocercus. Popular markers used in the reconstruction of the parrots’ phylogenies derive from mitochondrial DNA. However, current phylogenetic analyses seem to indicate conflicting relationships between Aratinga and other conures, and also among other Arini members. Therefore, it is not clear if the mtDNA phylogenies can reliably define the species tree. The inconsistencies may result from the variable evolution rate of the markers used or their weak phylogenetic signal. To resolve these controversies and to assess to what extent the phylogenetic relationships in the tribe Arini can be inferred from mitochondrial genomes, we compared representative Arini mitogenomes as well as examined the usefulness of the individual mitochondrial markers and the efficiency of various phylogenetic methods.
Results
Single molecular markers produced inconsistent tree topologies, while different methods offered various topologies even for the same marker. A significant disagreement in these tree topologies occurred for cytb, nd2 and nd6 genes, which are commonly used in parrot phylogenies. The strongest phylogenetic signal was found in the control region and RNA genes. However, these markers cannot be used alone in inferring Arini phylogenies because they do not provide fully resolved trees. The most reliable phylogeny of the parrots under study is obtained only on the concatenated set of all mitochondrial markers. The analyses established significantly resolved relationships within the former Aratinga representatives and the main genera of the tribe Arini. Such mtDNA phylogeny can be in agreement with the species tree, owing to its match with synapomorphic features in plumage colouration.
Conclusions
Phylogenetic relationships inferred from single mitochondrial markers can be incorrect and contradictory. Therefore, such phylogenies should be considered with caution. Reliable results can be produced by concatenated sets of all or at least the majority of mitochondrial genes and the control region. The results advance a new view on the relationships among the main genera of Arini and resolve the inconsistencies between the taxa that were previously classified as the broadly defined genus Aratinga. Although gene and species trees do not always have to be consistent, the mtDNA phylogenies for Arini can reflect the species tree.
Electronic supplementary material
The online version of this article (doi:10.1186/s12862-017-1012-1) contains supplementary material, which is available to authorized users.
Arini tribe with 19 genera is the most diversified tribe of neotropical parrots. Six of them are classified as macaws and nine as conures. The presence of bare facial area distinguishes macaws from conures and other members of this tribe. However, such morphological division seems to be disputable as the smallest macaw (monotypic Diopsittaca genus) turned out to be more closely related to three monotypic conures genera (Guaruba, Leptosittaca, Thectocercus) than to other macaws. We sequenced the complete mitochondrial genome of Guaruba guarouba to enrich the resource of molecular markers for examination of phylogenetic relationships between macaws and conures.
The Military Macaw is one of the eight species of the genus Ara. The genus is one of six genera, which form morphologically diverse group termed as Macaws. Parrots of this group differ in body size on demand of the genus and species. Six of Ara species are classified as large Macaws. Based on morphological similarities and differences, these species can be segregated into three pairs according to their plumage coloration. Representative mitochondrial genomes were sequenced only for A. glaucogularis (blue and yellow coloration) and A. macao (predominantly red/scarlet). Ara militaris is one of two predominantly green species and full mitochondrial genome of considered species was sequenced in this study.
It’s comparison with A. glaucogularis and A. macao mitogenomes revealed higher degree of identity between militaris and macao sequences than between militaris and glaucogularis mtDNAs. Ara militaris mitogenome will be indispensable to refine the phylogenetic relationships within Macaw group.
Abstract Primolius is a genus of midsized Macaws comprising three species. Blue-headed Macaws (Primolius couloni) are native to eastern Peru, extreme western Brazil and north-western Bolivia. In this study, full mitochondrial genome of considered species was sequenced. It is 16,995 bp long and contains 13 protein-coding genes, 2 rRNAs, 22 tRNAs and a control region. Its comparison with published Blue-throated Macaw (Ara glaucogularis) mitogenome revealed their high degree of identity. Primolius couloni mitogenome is the first complete genomic sequence of this genus. It will be indispensable to refine the phylogenetic relationships within the tribe Arini and will enrich the resource of markers for systematic, phylogenetic and population genetic studies.
Abstract The Red-bellied Macaw (Orthopsittaca manilata) is a species of the monotypic genus Orthopsittaca. The genus is one of the six genera, which form morphologically diverse group termed as Macaws. Individuals of Orthopsittaca manilata species are found in extremely large Amazonian area of South America. In this study, full mitochondrial genome of considered species was sequenced. It is 16,985 bp long and contains 13 protein-coding genes, 2 rRNAs, 22 tRNAs and a control region. Its comparison with published Blue-throated Macaw (Ara glaucogularis) mitogenome revealed their high degree of identity. Presented Orthopsittaca manilata mitogenome is the first complete genomic sequence of this genus. It will enrich the resource of molecular markers for future examination of evolutionary diversification of Macaws. It will be also indispensable to refine the phylogenetic relationships within the tribe Arini.
We offer here a diagnosed higher-level classification of New World parrots to reflect relationships inferred from a consensus of recent DNA-based phylogenies and morphological and behavioral studies. General understanding of the position of New World parrots among the Psittaciformes through the later 20 th century stems from Smith’s (1975) exhaustive review of structural morphology and behavior, which supplanted previous hypotheses ( e.g. Verheyen 1956; Boetticher 1959; Brereton 1963; Wolters 1975). In his study, which covered over 54 genera, including 20 of the roughly 31 from the New World (Collar 1997; Dickinson 2003), Smith (1975) concluded that the New World parrots were monophyletic. Moreover, he considered the New World parrots sufficiently divergent from other parrots to be accorded subfamily rank because they share several unique morphological and behavioral characters, including imperforate neonatal ear canals, double-sided “dyck texture” (Dyck 1971) pigmentation of remiges, lack of cutaneous pigmentation, and one-legged copulatory stance.
The nearly-neutral theory, which proposes that most mutations are deleterious or close to neutral, predicts that the ratio of non-synonymous over synonymous substitution rates (dN/dS), and potentially also the ratio of radical over conservative amino-acid replacement rates (Kr/Kc), are negatively correlated with effective population size. Previous empirical tests, using life-history traits (LHT) such as body-size or generation-time as proxies for population size, have been consistent with these predictions. This suggests that large-scale phylogenetic reconstructions of dN/dS or Kr/Kc might reveal interesting macroevolutionary patterns in the variation in effective population size among lineages. In this work, we further develop an integrative probabilistic framework for phylogenetic covariance analysis introduced previously, so as to estimate the correlation patterns between dN/dS, Kr/Kc and 3 life-history traits, in mitochondrial genomes of birds and mammals. Kr/Kc displays stronger and more stable correlations with LHT than does dN/dS, which we interpret as a greater robustness of Kr/Kc, compared to dN/dS, the latter being confounded by the high saturation of the synonymous substitution rate in mitochondrial genomes. The correlation of Kr/Kc with LHT was robust when controlling for the potentially confounding effects of nucleotide compositional variation between taxa. The positive correlation of the mitochondrial Kr/Kc with LHT is compatible with previous reports, and with a nearly-neutral interpretation, although alternative explanations are also possible. The Kr/Kc model was finally used for reconstructing life-history evolution in birds and mammals. This analysis suggests a fairly large-bodied ancestor in both groups. In birds, life-history evolution seems to have occurred mainly through size reduction in Neoavian birds, whereas in placental mammals, body mass evolution shows disparate trends across subclades. Altogether, our work represents a further step towards a more comprehensive phylogenetic reconstruction of the evolution of life-history and of the population-genetics environment.
Data deposition to NCBI Genomes
This Whole Genome Shotgun project has been deposited at DDBJ/EMBL/GenBank under the accession AMXX00000000 (SMACv1.0, unscaffolded genome assembly). The version described in this paper is the first version (AMXX01000000). The scaffolded assembly (SMACv1.1) has been deposited at DDBJ/EMBL/GenBank under the accession AOUJ00000000, and is also the first version (AOUJ01000000). Strong biological interest in traits such as the acquisition and utilization of speech, cognitive abilities, and longevity catalyzed the utilization of two next-generation sequencing platforms to provide the first-draft de novo genome assembly for the large, new world parrot Ara macao (Scarlet Macaw). Despite the challenges associated with genome assembly for an outbred avian species, including 951,507 high-quality putative single nucleotide polymorphisms, the final genome assembly (>1.035 Gb) includes more than 997 Mb of unambiguous sequence data (excluding N’s). Cytogenetic analyses including ZooFISH revealed complex rearrangements associated with two scarlet macaw macrochromosomes (AMA6, AMA7), which supports the hypothesis that translocations, fusions, and intragenomic rearrangements are key factors associated with karyotype evolution among parrots. In silico annotation of the scarlet macaw genome provided robust evidence for 14,405 nuclear gene annotation models, their predicted transcripts and proteins, and a complete mitochondrial genome. Comparative analyses involving the scarlet macaw, chicken, and zebra finch genomes revealed high levels of nucleotide-based conservation as well as evidence for overall genome stability among the three highly divergent species. Application of a new whole-genome analysis of divergence involving all three species yielded prioritized candidate genes and noncoding regions for parrot traits of interest (i.e., speech, intelligence, longevity) which were independently supported by the results of previous human GWAS studies. We also observed evidence for genes and noncoding loci that displayed extreme conservation across the three avian lineages, thereby reflecting their likely biological and developmental importance among birds.
Mitochondrial (mt) genes and genomes are among the major sources of data for evolutionary studies in birds. This places mitogenomic studies in birds at the core of intense debates in avian evolutionary biology. Indeed, complete mt genomes are actively been used to unveil the phylogenetic relationships among major orders, whereas single genes (e.g., cytochrome c oxidase I [COX1]) are considered standard for species identification and defining species boundaries (DNA barcoding). In this investigation, we study the time of origin and evolutionary relationships among Neoaves orders using complete mt genomes. First, we were able to solve polytomies previously observed at the deep nodes of the Neoaves phylogeny by analyzing 80 mt genomes, including 17 new sequences reported in this investigation. As an example, we found evidence indicating that columbiforms and charadriforms are sister groups. Overall, our analyses indicate that by improving the taxonomic sampling, complete mt genomes can solve the evolutionary relationships among major bird groups. Second, we used our phylogenetic hypotheses to estimate the time of origin of major avian orders as a way to test if their diversification took place prior to the Cretaceous/Tertiary (K/T) boundary. Such timetrees were estimated using several molecular dating approaches and conservative calibration points. Whereas we found time estimates slightly younger than those reported by others, most of the major orders originated prior to the K/T boundary. Finally, we used our timetrees to estimate the rate of evolution of each mt gene. We found great variation on the mutation rates among mt genes and within different bird groups. COX1 was the gene with less variation among Neoaves orders and the one with the least amount of rate heterogeneity across lineages. Such findings support the choice of COX 1 among mt genes as target for developing DNA barcoding approaches in birds.
This volume consist of eight main sections. Initially origins and evolutionary relationships are examined, followed by a brief section on the classification of the parrots. Next a section reviews the natural history of the parrots, briefly covering: general behaviour; distribution; habitat; movements; social behaviour; diet; breeding; and nocturnal species. Conservation status ics covered next. The main threats to parrots are then outlined and discussed: habitat loss; live bird trade; introduced species; persecution and hunting; and storms'climatic change. A brief section then looks at captive breeding. The mian body of the book is taken up with colour plates and a systematic section. The systematic section contains the following information, for each species: identification notes; voice; distribution and status (including distribution maps); ecology; description; sex/age; measurements; geographical variation; and references.
Abstract Maroon-fronted Parrot (Rhynchopsitta terrisi) is an endangered parrot endemic to pine-oak forests in north-eastern Mexico. According to all present classifications, R. terrisi as well as Rhynchopsitta pachyrhyncha are treated as a separate species based on some morphological and behavioral discrepancies. Despite this formal separation of the two species, some taxonomists conjecture their conspecific character. However, mutual taxonomic position of both species/subspecies was never verified by molecular research. We sequenced full mitochondrial genome of R. terrisi and constructed phylogenetic tree using sequences of mitochondrial ND2 gene from R. terrisi. R. pahyrchyncha and some other representative species of the tribe Arini. Our results indicated that in contrast to formal classification, both Rhynchopsitta taxa should be treated as subspecies.
Abstract Socorro Conure (Aratinga brevipes.Aratinga holochlora brevipes) is a parrot endemic to the Island of Socorro. According to some taxonomists the species is considered a subspecies of Green Conure (Aratinga holochlora). Some other classifications treat brevipes as a separate species based on relatively minor morphological differences between both species/subspecies. However, taxonomic position of Aratinga brevipes was never determined by molecular research. We sequenced full mitochondrial genome of the species and constructed phylogenetic tree using sequences of mitochondrial ND2 gene from A. brevipes and some other representatives of Conures group. Our results showed, that despite Aratinga brevipes is closely related to Aratinga holochlora, this Conure should be treated as a separate species.
Blue-crowned Parakeet (Aratinga acuticaudata) is a South American parrot species with a taxonomic position not confirmed by molecular studies. We sequenced full mitochondrial genome and constructed phylogenetic tree using sequences of mitochondrial ND2 gene from A. acuticaudata and some other representatives of Conures group. Our results confirmed previously described distribution of Aratinga species into three clades, but surprisingly did not classify Blue-crowned Parakeet to any of them. We found that A. acuticaudata shares the closest relationship with Diopsittaca nobilis and forms a separate clade together with Guaruba guarouba and Leptosittaca branickii species with a significant node. Our results confirm lack of monophyly of the genus Aratinga and underline the need of its taxonomic revision.
The exinct macaw Ara autochthones, previously known only from a single bone from an archaeological site on St. Croix, Virgin Islands, is here identified from several associated bones from an archaeological site in south-central Puerto Rico. The species belongs to a distinctive intermediate size-class and was larger than the Cuban Macaw Ara tricolor. It is assumed to have been endemic to the West Indies, but prehistoric interisland transport of parrots by humans makes interpreting the natural distribution of the species impossible in the absence of fossils. Historical reports of macaws elsewhere in the West Indies are rendered dubious for the same reason.
We report complete mitochondrial (mt) genomes for a penguin (little blue, Eudyptula minor) and a goose (greater white-fronted, Anser albifrons). A revised annotation of avian and reptile mt genomes has been carried out, which improves consistency of labeling gene start and stop positions. In conjunction with this, a summary of mt gene features is presented and a number of conserved patterns and interesting differences identified. The protein-coding genes from the two new genomes were analysed together with those from 17 other birds plus outgroup (reptile) taxa. The unrooted amino acid tree from 19 avian genomes was locally stable with many high bootstrap values using several maximum likelihood methods. In particular, Anseriformes (goose and duck) grouped strongly with Galliformes (chicken) to form Gallianseres, while the penguin paired firmly with the stork. The position where the outgroup joined the avian tree varied with the combination of outgroup taxa used. The three best supported positions of the root were passerine, but the traditional rooting position between paleognaths and neognaths could not be excluded.
The eBird/Clements checklist of birds of the world: Version 6
- J F Clements
- Schulenberg
- M J Iliff
- B L Sullivan
- C L Wood
- D Roberson
Version A classification of the bird species of South America
- Remsen Jr
- J V Cadena
- C D Jaramillo
- A Nores
- M Pacheco
- J F Pérez-Emán
- J Robbins