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Article

Origin and Diversification of the Genera Aratinga, Eupsittula, and Psittacara (Aves: Psittacidae)

by
Gabriela Padilla-Jacobo
1,*,
Tiberio Cesar Monterrubio-Rico
2,
Horacio Cano-Camacho
1 and
María Guadalupe Zavala-Páramo
1,*
1
Centro Multidisciplinario de Estudios en Biotecnología, FMVZ, Universidad Michoacana de San Nicolás de Hidalgo, Km 9.5 Carretera Morelia-Zinapécuaro, Posta Veterinaria, Morelia 58000, Mexico
2
Laboratorio de Ecología de Vertebrados Terrestres Prioritarios, Facultad de Biología, Universidad Michoacan de San Nicolás de Hidalgo, Morelia 58194, Mexico
*
Authors to whom correspondence should be addressed.
Diversity 2025, 17(3), 155; https://doi.org/10.3390/d17030155
Submission received: 24 December 2024 / Revised: 4 February 2025 / Accepted: 22 February 2025 / Published: 25 February 2025
(This article belongs to the Section Phylogeny and Evolution)
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Abstract

:
The arrival of psittacine in North America is well known but undefined. It is widely accepted that these birds originated in South America, and it has been suggested that different factors have promoted the biodiversity of birds in Mexico. However, in general, for North American psittacine, there are no proposed divergence times, and the possible influence of different geological events on these processes is unknown. In this study, phylogenetic relationships, divergence times, and ancestral areas of the genera Aratinga, Eupsittula, and Psittacara and related genera were estimated to propose hypotheses of the origin, diversification, and dispersal of groups under a Bayesian inference framework based on mitochondrial molecular markers. Of seven monophyletic clades within the Arini tribe, four coincided with the genera Psittacara, Eupsittula, Rhynchopsitta, and Pyrrhura, while Aratinga was grouped with Conuropsis and Cyanopsitta. Diversification of the analyzed genera probably occurred during the Miocene and around the Miocene–Pliocene boundary. The results suggest that the most likely origin of these genera is the Amazonian or Chaco regions. The diversification of these groups seems to be related to geoclimatic events associated with the uplift of the central and northern portions of the Andes and the closure of the Isthmus of Panama. We propose routes from south to north in the Neotropics and the use of the Greater and Lesser Antilles as a northward path.

1. Introduction

Psittaciformes are one of the most representative avian orders, since their coloration, cognitive capacity, and ability to imitate human words distinguish them from other birds. Unfortunately, this group is also notable for being among the most endangered birds globally. In the neotropical region, the main threats they face and that have caused their populations to decrease are human activities, such as agriculture, logging, and capture for the pet trade, among others [1,2]. Consequently, all neotropical Psittaciformes species are listed in the CITES protected species appendices [3].
In the Neotropics, parrots are exceptionally rich in species, and there are approximately 158 species distributed from northern Mexico to southern South America [4,5]. South America in particular shows considerable radiative speciation, and in North America, only 21 currently living species have reached the northernmost distribution in Mexico and the USA [4,6,7,8,9]. The records for the northernmost distribution of psittacines in America are for Rhynchopsitta pachyrhyncha, which was recorded in the mountains of southern Arizona, and the extinct Conuropsis carolinensis, which inhabited large areas throughout the eastern United States [4,10]. In Mexico, the distribution of the Psittacidae family has been recorded in specific areas. Its distribution is mainly limited to areas on the Pacific and Gulf of Mexico Slopes, and in the Yucatan Peninsula, being rare towards the interior of the territory [4,7,11]. It is worth mentioning that, for the family in Mexico, there is a general tendency towards a reduction in the distribution and populations of these species caused by habitat loss and extraction for the illegal pet trade [12,13].
Through phylogeographic analyses and phylogenetic reconstructions with molecular data of some species of parrots in South America, it has been established that the triggers of speciation were geotectonic events such as the uplift of the Andes, marine incursions, fluvial dynamics, and the influence of the Pleistocene glacial cycles [14,15,16,17,18,19]. However, analyses of this type for parrots in their northernmost distribution (Mexico) are scarce, and it is unknown how and when the psittacines arrived in North America.
It has previously been suggested that factors such as climatic oscillations, Pleistocene refugia, topographic complexity, and geographic position promote bird biodiversity in Mexico [20]. In this sense, the role of events such as the Great American Biotic Interchange in promoting the exchange of bird species between North and South America is recognized [21]. Furthermore, it has been proposed that the direction of bird traffic across the land bridge was primarily from south to north [21,22]. In this exchange, it has been proposed that the arrival of psittacines from the south to the north occurred multiple times in the late Miocene [22]; however, for North American parrots, there are no publications on the influence of spatiotemporal events on their diversification.
The tools developed for phylogeographic analysis and the gradual increase in information available for reviewing taxonomic relationships, particularly those based on DNA sequences, have allowed the generation of hypotheses that explain the origin and diversification of natural groups. In this sense, the genera Aratinga, Eupsittula, and Psittacara have information that can be analyzed together. In addition, these genera are widely distributed with species present in northern Mexico, Central America, the Caribbean islands, and South America [4,11,23]. Therefore, they are a good example to infer ancestral areas, patterns of diversification, and divergence times of psittacines from south to north in the neotropical region.
Some changes have been proposed for the classification and nomenclature of the species of the genus Aratinga based on morphological data [24,25,26], and for more than eighty years, this genus was considered a monophyletic group [26,27] (Supplementary Table S1). However, based on evidence demonstrated by phylogenetic reconstructions from molecular data, some species were reclassified and recognized in the genera Aratinga, Eupsittula, Thectocercus, and Psittacara [5,22,27,28,29,30] (Supplementary Table S1).
Currently, according to different authors, six or seven species are recognized in the genus Aratinga, five or six in the genus Eupsittula, and twelve species in the genus Psittacara [5,27,28,29,30] (Supplementary Table S1). Although there are independent studies where relationships have been established between species of these genera, there is no consensus on the relationships between them and with other related ones. In the proposals made by different authors on the relationships between psittacines of the Arini tribe, the related genera are Anodorhynchus, Ara, Aratinga, Conuropsis, Cyanoliseus, Cyanopsitta, Diopsittaca, Enicognathus, Eupsittula, Guaruba, Leptosittaca, Nandayus, Orthopsittaca, Psittacara, Pyrrhura, Primolius, Rhynchopsitta, and Thectocercus [15,19,22,31,32].
In this study, we present a phylogenetic hypothesis on the relationships between the genera Aratinga, Eupsittula, and Psittacara using molecular data from the mitochondrial genes for cytochrome oxidase subunit I (COI) and NADH dehydrogenase subunit 2 (ND2). We also propose about the time of divergence, probable ancestral areas, and possible dispersal routes of these groups, with emphasis on their arrival at the extreme north of their distribution. This study increases knowledge about the presence of parrots in Mexico and helps build a broader view of the processes that could influence the presence and diversity of neotropical birds in their northernmost distribution.

2. Materials and Methods

2.1. Biological Samples, DNA Extraction, PCR Amplification, and Sequencing

Two biological samples of E. canicularis used in the present study were collected in 2005, under collection permit SGPA/DGVS/06387. The samples came from specimens found in 2 locations in the north and center of the Pacific Slope in Mexico (Sinaloa and Michoacan states). The geographic coordinates of each collection location were recorded. Biological samples of feathers were collected from nests without harming the individuals. The samples were preserved by using the method described by Padilla-Jacobo et al. [33] and were deposited in the wildlife samples collection at Centro Multidisciplinario de Estudios en Biotecnología (CMEB), at the Universidad Michoacana de San Nicolás de Hidalgo (UMSNH), in Morelia, Michoacan, Mexico.
DNA was extracted by using the phenol-free method described by FitzSimmons [34]. DNA quality and concentration were verified by agarose gel electrophoresis and on a Nanodrop (Thermo Scientific, Waltham, MA, USA). Fragments of COI and ND2 mitochondrial genes were amplified. The COI fragment was amplified by using the primers and PCR conditions described by Palumbi et al. [35], and the ND2 fragment was amplified by using the PCR conditions and primers described by Hackett [36]. PCR product quality and concentration were revised by agarose gel electrophoresis and on a Nanodrop (Thermo Scientific, Waltham, MA, USA). The concentrations of the PCR products were adjusted to 30 ng/μL (total volume of 20 μL). DNA sequencing was performed by using the Sanger method on both strands [37] by using the commercial service Psomagen (Psomagen Inc., Rockville, MD, USA). The obtained sequences were reviewed using the Sequencher v.5.4.6 [38] software. Four sequences were deposited in GenBank-NCBI (Access numbers: KJ612381, KJ612385, KJ612390, KJ612394).

2.2. Sequence Samples

The sequences used in the analyses were obtained from the National Center for Biotechnology Information (NCBI) GenBank database. To establish the relationships of the Aratinga, Eupsittula, and Psittacara genera, we analyzed the Arini tribe, including 17 of the 18 genera that compose it. The out-group comprises species representing the tribes Incertae sedis (8 of 10 genera), Androglossini (Amazona ochrocephala), Melopsittacini (Melopsittacus undulatus), and Cacatuini (Cacatua sulphurea), and the species Coracopsis vasa, Nestor notabilis, Falco peregrinus, and Columba livia. The taxa included in these analyses were chosen according to results previously reported by Ribas and Miyaki [15], Tavares et al. [19,31], and Kirchman et al. [32], and the Arini tribe proposed by Joseph et al. [9]. In detail, a total of 76 terminal taxa were included in the analyses, of which 54 belonged to the Arini tribe (Supplementary Table S2). According to the classification of Remsen et al. [27] and Clements et al. [5], we included all species of the genera Aratinga (6 species) and Eupsittula (5 species). Additionally, according to the classification by Clements et al. [5], we included 9 of 11 living species of Psittacara (and the subspecies P. h. rubritorquis), 7 of 9 species from Forpus, and all the species of the genera Primolius (3 species), Pionites (2 species), and Rhynchopsitta (2 species). We also included the genera Deroptyus, Cyanoliseus, Conuropsis, Cyanopsitta, Orthopsittaca, Leptosittaca, Guaruba, Thectocercus, and Diopsittaca. Finally, according to Clements et al. [5], other genera and the proportion of species also included are described below: Ara (7 of 8 living species), Enicognathus (1 of 2 species), Anodorhynchus (2 of 3 species), and Pyrrhura (8 of 23 species) (Supplementary Table S2). We analyzed the sequences of two molecular markers of mitochondrial DNA (mtDNA): cytochrome c oxidase subunit I (COI) and NADH dehydrogenase subunit 2 (ND2) (Supplementry Table S2).

2.3. Phylogenetic Analysis

Sequence editing, alignments, and the construction of the data matrices were carried out with Sequencher v.5.4.6 [38] and PhyDE [39]. To estimate genetic distances (uncorrected p distance) among closely related species, we used MEGA 11 software [40]. Separate analyses were run for each genetic marker where the sequences with “N” were excluded, and the Kimura 2-Parameter model with gamma distribution of rates among sites was used. Molecular evolution models were obtained with jModelTest 2.1.10 [41] and selected using the corrected Akaike Information Criterion (cAIC) [42]. The best model obtained using this criterion for COI was HKY + G + I (Hasegawa, Kishino and Yano + Gamma distribution of rates among sites + Invariant sites [43]), for ND2, GTR + G + I (General Time Reversible + Gamma distribution of rates among sites + Invariant sites [44]), and GTR + G + I for all the sequence data after concatenation (COI + ND2).
Phylogenetic reconstructions were generated with concatenated sequences using maximum likelihood (ML) and Bayesian inference (BI) frameworks. The ML and BI reconstructions were performed using Genetic Algorithm for Rapid Likelihood Inference (GARLI) [45] and MrBayes v3.2 [46] software, respectively. The branch support values were estimated by the BP of 500 replicates and by PP. MrBayes runs were performed using the following parameters: four independent runs of four chains each (one cold chain and three hot chains) for 10 million generations with sampling one tree every 1000 generations. Trees and parameters were summarized after discarding 25% of the data (burn-in). The remaining trees were summarized as a majority consensus tree and visualized using FigTree v1.4.4 [47].

2.4. Inference of Divergence Time

To estimate divergence times, we considered data from previous calibrations performed by Jarvis et al. [48], who proposed estimates made under Bayesian inference with genomic sequences from 45 bird species. Based on 19 fossil age calibrations, they proposed that the most basal divergences within Neoaves (Columbea–Passerea) occurred before the Cretaceous–Paleogene transition (67 to 69 Mya). They also reported that Falconiformes and Psittaciformes share an ancestor of approximately 60 Mya.
In this analysis, divergence times with concatenated sequences (COI + ND2) were estimated under Bayesian inference using BEAST v1.7.4 [49]. To establish the divergence age, we used one calibration point using a normal distribution for the root of the tree (Columba livia, average = 69.5 Mya, SD = 1.0). The following specifications were used. An uncorrelated lognormal relaxed clock model was selected with a GTR+G+I selection model. We used a Yule-type speciation model because it is appropriate for the analysis of sequences obtained from different species [50,51]. Markov Chain Monte Carlo (MCMC) analyses were run for 10 million generations with sampling one tree every 1000 generations. To assess convergence, effective sample size (ESS) values were observed with MCMC Trace Analysis Tool v1.5.0 [49]. The results were summarized using TreeAnnotator v1.7.4 [49]. After 10% of the trees were discarded, the remaining trees were summarized as a maximum clade credibility tree, including the average divergence times and their associated 95% high posterior densities (HPDs). Trees were visualized using FigTree v1.4.4 [47].

2.5. Reconstruction of Ancestral Areas

Reconstruction of ancestral areas was performed using 10,001 trees generated by BEAST [49]. Dispersal–vicariance analysis was performed using the S-DIVA tool in RASP v 4.0 [52]. S-DIVA analyses are advantageous because they provide statistical support for ancestral area reconstructions [53]. To run S-DIVA, we followed the recommendations of the authors of the program [52], taking into account binary trees = 10,001, discard trees = 1000, and random trees = 100. In this analysis, six geographic zones were considered according to Morrone [54,55]: (A) Central/North American, (B) Northwestern/South American, (C) Amazonian, (D) Chaco, (E) Parana, and (F) South American transition (Figure 1).
The Central/North American region (A) comprises central and southern Mexico, Belize, Guatemala, El Salvador, Honduras, and the Antilles. The northwestern South American region (B) consists of Costa Rica, Panama, northwestern South America, Ecuador, Colombia, Venezuela, and Trinidad and Tobago. The Amazonian region (C) is the largest in the neotropical region and extends through most of Brazil and the Guyanas and parts of Venezuela, Colombia, Ecuador, Peru, Bolivia, Paraguay, and Argentina. The Chaco region (D) encompasses northern and central Argentina, southern Bolivia, western and central Paraguay, Uruguay, and central and northwestern Brazil. The Parana region (E) includes northwestern Argentina, the eastern region of Paraguay, and the areas of extreme southern and eastern Brazil. The South American transition region (F) comprises the Highlands of the Andes between western Venezuela and northern Chile and central western Argentina (Figure 1). The distributions of the genera were established in geographic maps according to records produced by different authors and summarized in del Hoyo et al. [29] (Table 1).

3. Results

3.1. Phylogenetic Analyses

Seventeen of the eighteen recognized genera in the tribe Arini were included. In particular, for the genus Psittacara, 9 of the 11 recognized species were considered, and for the genera Aratinga and Eupsittula, all species within each genus were included (Supplementary Table S2). The alignments contained 1610 characters corresponding to the concatenated sequences of COI and ND2 (570 + 1040 bp) of 76 taxa. In the alignment of COI, 338 invariable (monomorphic) characters, 198 parsimony informative sites, 14 singleton variable sites, and 212 variable (polymorphic) characters were identified. In the alignment of ND2, 357 invariable (monomorphic) characters, 542 parsimony informative sites, 83 singleton variable sites, and 625 variable (polymorphic) characters were identified. Bayesian inference (BI) and maximum likelihood (ML) analyses produced trees with similar topologies. Overall, the posterior probability (PP) and bootstrap probability (BP) values provided sufficient support for the phylogenetic relationships established within each group (Figure 2).
We found that of the seven monophyletic clades within the Arini tribe, four coincided with the genera Psittacara, Eupsittula, Rhynchopsitta, and Pyrrhura, and three clades each integrated different genera as follows: Clade 1 (C1) included Ara, as sister to Primolius, and Orthopsittaca, which was retrieved as the most ancestral in the clade; Clade 2 (C2) was formed by Aratinga, Conuropsis, and Cyanopsitta; and Clade 3 (C3) included Thectocercus, Diopsittaca, Guaruba, Leptosittaca, Enicognathus, Anodorhynchus, and Cyanoliseus (Figure 2).
Regarding the genera (Aratinga, Eupsittula, and Psittacara) that were the main objective of this work, our results show that clade C2, where Aratinga is included, is sister to clade C1, while Eupsittula is a sister clade to the Psittacara clade (Figure 2). Clade C2 contains eight taxa, including six species from the genera Aratinga, and the extinct Conuropsis carolinensis and Cyanopsitta spixii. In this clade, the position of Cyanopsitta spixii as the most ancestral genus is weakly supported. This indicates that the data set (considering taxa and characters) is insufficient to resolve the uncertainty. Therefore, analyses that consider a larger sample of taxa, molecular markers (nuclear and mitochondrial from other individuals of the species), and morphological, behavioral, ecological data, among others, are recommended. Additionally, in a well-supported node, A. weddellii is ancestral to C. carolinensis and the rest of the Aratinga species. Within the Eupsittula genus, E. aurea and E. nana form a sister clade to E. canicularis, and E. cactorum and E. pertinax form a polytomy together with the rest of the group (Figure 2).
Within the Psittacara clade, a subclade includes P. finschi, P. brevipes, P. holochlorus, P. h. rubritorquis, and P. erythrogenys, while P. chloropterus and P. euops were found to be sister species closely related to this subclade (Figure 2). In the subclade, the topologies of the BI and ML trees show P. holochlorus and P. h. rubritorquis (P. rubritorquis in the tree) as sister taxa. The genetic distance matrix in Table 2 shows the proportion of nucleotide sites where two sequences are different. A value close to zero indicates a lower genetic difference, and a value close to one implies a higher genetic difference between the sequences being compared. For example, in the context of the values obtained, a low genetic distance (0.016/0.006) is observed between P. holochlorus and P. h. rubritorquis, coinciding with their relationship as sister species.
In addition, P. brevipes was found to be closely related to P. finschi (0.011/0.006). The genetic distance between P. holochlorus and P. brevipes (0.024/0.008) was greater than that between P. brevipes and P. finschi (0.011/0.006) (Table 2). In addition, P. leucophthalmus, P. wagleri and P. mitratus indicate an early divergence within the Psittacara clade (Figure 2), where P. leucophthalmus can be observed as the most ancestral species, which is consistent with its genetic distance from the other two species (0.051/0.053 and 0.061/0.043, respectively) (Table 2).

3.2. Inference of Divergence Times and Reconstruction of Ancestral Areas

The estimated age of the nodes and the biogeographic reconstruction are shown in Table 3 and Figure 3. In convergence testing for Bayesian analyses [56], the effective sample size values (ESS) for different statistics were acceptable (all higher than 200). In general, the results show that most of the analyzed genera of interest began their diversification during the Miocene epoch; then, during the Pliocene, the diversification among species continued, within each genus.
Clades C1 and C2 shared a common ancestor that also originated during the Miocene, which may have inhabited the Amazonian or Chaco regions (node 8, Table 3, Figure 3), and their split was estimated to have occurred approximately 11.32–17.41 million years ago (Mya). In clade C1, the split of Orthopsittaca manilatus as an ancestral lineage was estimated to have occurred approximately 8.96–14.71 Mya, with the most likely ancestral area being the Amazonian region (region C) (node 1, Table 3, Figure 3). Here, the genus Ara diverges during the Miocene, approximately 5.76–9.82 Mya, in the Amazonian region (node 1a, Table 3, Figure 3).
The estimated age for the divergence of C2, with C. spixii as the basal lineage, is approximately 10.25–16.24 Mya, with a common ancestor that probably lived in the Chaco region (D) (node 2, Table 3, Figure 3). Within C2, the subsequent diversification of the genus Aratinga (including C. carolinensis) occurred approximately 8.23–14.02 Mya; the biogeographic reconstruction obtained with the dispersal–vicariance analysis (S-DIVA) shows this clade with an origin in the Amazonian or Chaco regions (regions C or D) (node 2a, Table 3, Figure 3 and Figure 4).
It should be noted that the divergence time between the species C. carolinensis and the rest of the group was estimated at approximately 6.43–12.32 Mya (node 2b, Table 3, Figure 3 and Figure 4) in the Central/North American region; A. jandaya, A. auricapillus, A. maculata, and A. solstitialis are the most recent group with a time of the most recent common ancestor (TMRCA) estimated to be approximately 0.74–1.78 Mya (node 2c, Table 3, Figure 3 and Figure 4). In this group, the S-DIVA results suggested three dispersal events and two vicariance events.
The divergence of the clade C3 lineages began approximately 11.46–17.86 Mya, although the ancestral area of C3 could not be determined (node 3, Table 3, Figure 3). However, it is clear that most of the genera that make up this clade diversified during the Miocene, with the following notable aspects: the TMRCA of Thectocercus and Diopsittaca was estimated to have originated approximately 3.13–6.72 Mya, and it was assigned to the Amazonian region (region C) (node 3a, Table 3, Figure 3). Furthermore, TMRCA estimates for the Anodorhynchus species indicate that the splits occurred approximately 2.03–5.28 Mya, and the ancestral area was possible in the Chaco region (region D) (node 3b, Table 3, Figure 3).
According to the results, the sister genera Psittacara and Eupsittula share a TMRCA estimated to have occurred approximately 11.66–18.87 Mya, around the Langhian stage. The origin of these genera and the beginning of their diversification can be assigned to the Amazonian region (region C) (nodes 9, 5 and 4, Table 3, Figure 3). It is estimated that the genus Eupsittula began its diversification aproximately 5.59–10.85 Mya (node 5, Table 3, Figure 3 and Figure 5).
In this group, E. pertinax and E. cactorum would be the most ancestral species considering their place in the clade topology; however, since they are found in a polytomy, caution should be taken. E. aurea and E. nana are sister species that share a TMRCA with a probable origin in the Amazonian region (Figure 3). E. canicularis would be the most recent species, with an origin of approximately 0.34–1.11 Mya in central and North America or in the northwestern regions of South America (regions A or B) (node 5a, Figure 3 and Figure 5). In this clade, the S-DIVA results suggested five dispersal events and one vicariance event.
The estimated age of divergence for the genus Psittacara is in the boundary of the Miocene–Pliocene epochs and constitutes one of the most diversified genera. This clade began its diversification with the separation of P. leucophthalmus approximately 3.76–7.36 Mya, and the Amazonian region was estimated as the ancestral area (region C) (node 4, Table 3, Figure 3 and Figure 6).
Next, P. wagleri originated approximately 2.45–4.7 Mya in the South American region and P. mitratus originated approximately 1.9–3.62 Mya in the Amazonian or Chaco regions (node 4, Table 3, Figure 3 and Figure 6). Within this group, the species P. finschi, P. brevipes, P. rubritorquis, P. holochlorus, P. erythrogenys, P. euops, and P. chloropterus shared a TMRCA dating to approximately 1.36–2.58 Mya, with a diversification in the Central/North American region (region A) (node 4a, Table 3, Figure 3 and Figure 6). In this clade, the S-DIVA suggested three dispersal events and three vicariance events.
On the other hand, the genus Pyrrhura diverged during the Pliocene epoch, originating approximately 3.5–7.01 Mya in the Amazonian region (region C) (node 6, Table 3, Figure 3). In this clade, the sister species P. rupicola and P. molinae (node 6b, Table 3, Figure 3) and P. picta and P. leucotis (node 6a, Table 3, Figure 3) are the most recent species.
Another interesting observation is the divergence of the genus Rhynchopsitta in the Langhian to Aquitanian stages. For the genus Rhynchopsitta, with an origin approximately 14.28–21.75 Mya, the region of origin was not determined, but the results suggested a possible origin in the Amazonian region (region C) (node 7, Table 3, Figure 3). The TMRCA between R. pachyrhyncha and R. terrisi was estimated to have occurred approximately 0.04–0.42 Mya. The S-DIVA results showed no dispersal or vicariance events in Rhynchopsitta.

4. Discussion

4.1. Phylogenetic Analyses

In the present study, we analyzed the mitochondrial sequences of taxa of the genera Aratinga, Eupsittula, and Psittacara to establish phylogenetic relationships as a first step required to estimate their divergence time and origin. The topology of the BI and ML trees revealed the Arini tribe as monophyletic and Pionites–Deroptyus as the sister group (Figure 2), similar to the observations of Selvatti et al. [22] and Smith et al. [57]. Clade C2 consisted of the genera Aratinga, Conuropsis, and Cyanopsitta and is sister to clade C1, comprising the genera Ara, Primolius, and Orthopsittaca, a relationship previously observed by Kirchman et al. [32] and Selvatti et al. [22]. However, the relationship of Cyanopsitta is questionable; here, it is retrieved as ancestral to Aratinga in clade C2, and in the inferences of Kirchman et al. [32] and Selvatti et al. [22] Cyanopsitta is included as the most ancestral in clade C1, although in both studies, the relationships are recovered with low support values. In previous studies, the extinct C. carolinensis was located as a sister genus of Aratinga [32,58]; however, consistent with the reports of Selvatti et al. [22] and Smith et al. [57], in our results, C. carolinensis was integrated into clade C2 with the genus Aratinga.
Regarding the genus Eupsittula, in contrast with the findings of Kirchman et al. [32] and Selvatti et al. [22], who proposed R. pachyrhyncha as sister to Eupsittula or sister to Cyanoliseus, respectively, in our results, Eupsittula is a sister clade to the Psittacara clade. Our analysis showed the relationship of E. aurea and E. nana as sister species, as observed by Kirchman et al. [32] and by Selvatti et al. [22] (Figure 2). Our results also corroborate those of Remsen et al. [24], who placed E. aurea and E. cactorum in this genus. Some uncertainties remain within the Psittacara genus; for some authors, P. finschi and P. chloropterus are conspecific with P. leucophthalmus, and it has been suggested that P. rubritorquis is conspecific with P. holochlorus [59,60]. However, in our results, the phylogenetic trees and genetic distance show that P. leucophthalmus could be the most ancestral in the Psittacara clade and distant from P. finschi and P. chloropterus (Figure 2, Table 3), consistent with the inference of Selvatti et al. [22]. Similar to what was observed by Kirchman et al. [32] and Selvatti et al. [22], in this study, P. euops and P. chloropterus are sister species. Additionally, P. holochlorus is sister to P. rubritorquis (Figure 2, Table 2), in contrast with Selvatti et al. [22], who propose P. holochlorus as sister to P. leucophthalmus. The genetic distance of P. brevipes is greater from P. holochlorus than from P. finschi (distributed in Nicaragua, Costa Rica, and Panama) (Table 2). In the trees, P. finschi and P. brevipes are placed in an unresolved subclade. However, the inclusion of other data could resolve this uncertainty.

4.2. Divergence Times and Reconstruction of Ancestral Areas

Overall, our results show that most of the taxa of the Arini tribe originated and diversified during the Miocene and Pliocene epochs, and some taxa diverged more recently in the Pleistocene epoch (Figure 3). This coincides with what was previously reported, where it is established that the diversification in neotropical birds and other taxa was continuous throughout the Miocene and up to the Pleistocene under the complex multifactorial conditions described for South America [61,62,63,64,65,66,67,68,69,70,71,72]. Furthermore, our results are consistent with those of plant and animal phylogenetic studies showing that many neotropical sister species diverged in the Pleistocene [73,74,75,76,77,78].
In Central America, the closure of the Isthmus of Panama facilitated the phenomenon known as “The Great American Biotic Interchange”, which allowed the dispersion of taxa from north to south and from south to north, with the subsequent diversification of some taxa in new areas [79,80,81]. For different bird species, it has been established that the closure of the Isthmus of Panama promoted the dispersion and invasion of South American lineages toward North America [21].
Our results on the genera Aratinga, Eupsittula, and Psittacara show that among the three, the genus Aratinga is the oldest, considering the divergence of A. weddellii at 8.23–14.02 Mya, followed by Eupsittula, with a first divergence at 5.59–10.85 Mya, and the most recent is Psittacara, with the first divergence at 3.76–7.36 Mya (Figure 3). These genera originated in South America, most likely in the Amazon region (Figure 3). For the genus Aratinga (8.23–14.02 Mya), with A. weddellii as the most ancestral species, the center of origin was the Amazonian or Chaco regions, from which a first dispersal event occurred, suggesting that it took place to the southeast, west and east of the Amazonian region and to the north (Figure 4). The northernmost species of all American parrots, C. carolinensis (6.43–12.32 Mya), could have originated in the Central/North American–Chaco (AD) regions through a vicariance event during the Miocene. The dated ML tree of Selvatti et al. [22] also shows C. carolinensis originating in the Miocene. However, given its ancient origin and distribution, we propose that the initial vicariance event was followed by dispersal events, where it may have used the Greater and Lesser Antilles as part of its northward route (Figure 4).
For Eupsittula (5.59–10.85 Mya), the most likely ancestral area was the Amazonian region, and dispersal events were the main promoters of diversification within the genus (Figure 5). Range expansion occurred mainly to southeastern and northeastern South America and western North America. Currently, species of the genus Eupsittula are found in the southern Amazonian region (E. aurea, E. cactorum, and E. pertinax), in North America (E. canicularis and E. nana), and in the Chaco and Parana regions (E. aurea and E. cactorum) (Figure 5). In South America, this group may have benefited from the biotic and abiotic changes that caused the disappearance of Lake Pebas and the establishment of the Acre system conditions [82]. The only mainland species in the group with a North American distribution is E. canicularis. Based on the estimated divergence time (0.34–1.11 Mya) and ancestral area (Central/North America) for this species, it is suggested that it crossed into North America after the Isthmus of Panama was well established (last closed 3.5 Mya [80]), with range expansion and subsequent speciation in situ (Figure 5). Populations from northern Mexico may have expanded their range northwestward, perhaps following the tropical dry forest (Pacific Slope), with which it is strongly associated [4].
According to our results, Psittacara is a recent genus whose divergence began at the Miocene–Pliocene limits (Figure 6). The genus Psittacara is widely distributed in the Neotropics, with species inhabiting areas from North America to South America. Furthermore, it is one of the largest and has experienced the fastest diversification within the Arini tribe (TMRCA 3.76–7.36 Mya). According to our results, the events that promoted within-group diversification are dispersion and vicariance, suggesting a complex evolutionary history. The diversification of the first split in Psittacara occurred in the Amazonian region approximately 3.76–7.36 Mya, coinciding with the disappearance of the Acre system (7 Mya) and the establishment of modern drainage in the Amazon basin (7 to 2.5 Mya) [82]. Additionally, it has been proposed that the Andes are an important geographic barrier that has promoted diversification in various bird species [63,65,83]. Considering the geographic range of P. leucophthalmus and P. wagleri and our results, the northern Andes (Venezuela and Colombia) are the geographic barrier that promoted diversification (Figure 6). The uplift of the Andes of Colombia and Venezuela occurred approximately 5–3 Mya [84,85,86], which coincides with the origin of P. wagleri approximately 3.48 Mya. P. mitratus also diverges by vicariance, but when observing the distribution of the species, there is no current geographical barrier related to its origin by vicariance. However, the most likely region of origin is the Amazon (2.69 Mya), where rivers or changes in vegetation could promote their separation (Figure 6). For the species distributed in Central and North America and in the Antilles, diversification probably occurred in Central America, where 85.71% of its species are found (Figure 6). Diversification of this subgroup occurred after the establishment of the Isthmus of Panama 3.5 Mya [80], suggesting range expansion and subsequent in situ speciation, particularly for P. finschi, P. rubritorquis, and P. holochlorus, which reached northwestern and eastern Mexico [11,29].
Other notable observations are that with respect to the genus Rhynchopsitta currently inhabiting North America, its area of origin in South America indicates a possible single event of ancestral arrival before the closure of the Isthmus of Panama. It is possible that the ancestor used the Neogene volcanic arc of Central America to reach North America, as has been reported for other taxa [87,88,89,90,91]. Subsequently, the genus recently diversified (TMRCA = 0.04–0.42 Mya) in Mexico during the Pleistocene epoch.

5. Conclusions

We identified seven well-supported clades, some of which coincided with recognized genera (Rhynchopsitta, Psittacara, Eupsittula, and Pyrrura). Some relationships between the clades are not widely supported, but they are constant under different analyses. Our analyses show a complex evolutionary history within the Arini tribe, with most of the analyzed genera originating during the Miocene (Ara, Orthopsittaca, Aratinga, Cyanopsitta, Guaruba, Leptosittaca, Enicognathus, Cyanoleus, Eupsittula, and Rhynchopsitta) and some around the Miocene–Pliocene (Psittacara and Pyrrhura). It is proposed that the genera Rynchopsitta and Conuropsis reached North America before the closure of the Isthmus of Panama by independent events. Additionally, the lineages that arrived in North America after the closure of the Isthmus of Panama are P. finschi, P. brevipes, P. holochlorus, and E. canicularis. Because the Arini tribe includes a great diversity of species with a wide distribution in the Neotropics, this study supports the need for further analyses for each of the seven identified clades. Additionally, it is recommended to consider the species and subspecies within each group and expand the number of data to refine the proposed results.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d17030155/s1, Table S1: Contrasting classifications of the genera Aratinga, Eupsittula, and Psittacara; Table S2: List of species (and/or subspecies) used in this study, including locality, identification and GenBank accession numbers.

Author Contributions

Conceptualization, G.P.-J., T.C.M.-R., and M.G.Z.-P.; Data curation, G.P.-J.; Formal analysis, G.P.-J. and M.G.Z.-P.; Funding acquisition, T.C.M.-R., H.C.-C., and M.G.Z.-P.; Investigation, G.P.-J.; Project administration, T.C.M.-R., H.C.-C., and M.G.Z.-P.; Resources, T.C.M.-R.; Supervision, M.G.Z.-P.; Visualization, G.P.-J.; Writing—original draft preparation G.P.-J. and M.G.Z.-P.; Writing—review and editing, G.P.-J., T.C.M.-R., H.C.-C., and M.G.Z.-P. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Fondos Mixtos, Consejo Nacional de Humanidades, Ciencias y Tecnologías-Michoacán, grant number 41168 to M.G.Z.-P., H.C.-C., and T.C.M.-R., and by Consejo Nacional de Humanidades, Ciencias y Tecnologías, grant number 2002-C01-00021 to T.C.M.-R. It was also funded by Coordinación de la Investigación Científica de la Universidad Michoacana de San Nicolás de Hidalgo, grant number Proyect-2016-2017 to M.G.Z.-P.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

All sequences were deposited in GenBank-NCBI.

Acknowledgments

The authors thank the collection permits granted by Secretaría del Medio Ambiente y Recursos Naturales de México (number SGPA/DGVS/06387 to T.C.M.-R.).

Conflicts of Interest

The authors declare no conflicts of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Figure 1. Map showing the six geographic zones that were considered according to Morrone [54,55].
Figure 1. Map showing the six geographic zones that were considered according to Morrone [54,55].
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Figure 2. Consensus tree showing the phylogenetic relationships between Aratinga, Eupsittula, and Psittacara and related genera obtained using BI and ML analyses. Estimates were made with 1610 characters corresponding to the concatenated sequences of COI and ND2 (570 + 1040 bp) of 76 taxa. Values on the branches represent posterior probabilities and bootstrap values (PP/BP). (*) Value inferior at PP = 0.5 or PB = 50. The scale bar under the tree represents the number of substitutions per site. Abbreviations: C1, C2, C3 = Clade 1, Clade 2, Clade 3; Sc1 = Subclade 1; InSe = Incertae sedis tribe; ISAn = Incertae sedis and Androglossini tribes.
Figure 2. Consensus tree showing the phylogenetic relationships between Aratinga, Eupsittula, and Psittacara and related genera obtained using BI and ML analyses. Estimates were made with 1610 characters corresponding to the concatenated sequences of COI and ND2 (570 + 1040 bp) of 76 taxa. Values on the branches represent posterior probabilities and bootstrap values (PP/BP). (*) Value inferior at PP = 0.5 or PB = 50. The scale bar under the tree represents the number of substitutions per site. Abbreviations: C1, C2, C3 = Clade 1, Clade 2, Clade 3; Sc1 = Subclade 1; InSe = Incertae sedis tribe; ISAn = Incertae sedis and Androglossini tribes.
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Figure 3. Chronogram with divergence times and ancestral distribution of the genera Aratinga, Eupsittula, and Psittacara and related genera. Bars indicate 95% confidence intervals (high posterior density, HPD) for node age estimates. The pie charts at the nodes represent the probabilities of the ancestral area at the respective nodes. The legend to the left summarizes the colors and codes that represent geographic zones associated with the following labels: The asterisk (*) indicates an undetermined zone, (A) Central/North American, (B) Northwestern South American, (C) Amazonian, (D) Chaco, (E) Parana, and (F) South American transition. The values of divergence times and ancestral areas can be found in Table 3. The green rings represent vicariance events, and the purple rings represent dispersal events.
Figure 3. Chronogram with divergence times and ancestral distribution of the genera Aratinga, Eupsittula, and Psittacara and related genera. Bars indicate 95% confidence intervals (high posterior density, HPD) for node age estimates. The pie charts at the nodes represent the probabilities of the ancestral area at the respective nodes. The legend to the left summarizes the colors and codes that represent geographic zones associated with the following labels: The asterisk (*) indicates an undetermined zone, (A) Central/North American, (B) Northwestern South American, (C) Amazonian, (D) Chaco, (E) Parana, and (F) South American transition. The values of divergence times and ancestral areas can be found in Table 3. The green rings represent vicariance events, and the purple rings represent dispersal events.
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Figure 4. Clade description and map of distribution areas for the genus Aratinga. The colored distribution areas on the map represent the current distribution of each species of the genus included in this analysis. The letters A, B, C, D, E, and F within the maps represent the six neotropical regions (see Figure 1).
Figure 4. Clade description and map of distribution areas for the genus Aratinga. The colored distribution areas on the map represent the current distribution of each species of the genus included in this analysis. The letters A, B, C, D, E, and F within the maps represent the six neotropical regions (see Figure 1).
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Figure 5. Clade description and map of distribution areas for the genus Eupsittula. The estimated values of the TMRCA (HPD 95%) and the most likely ancestral area are indicated. The colored distribution areas in the map represent the current distribution of each species of the genus included in this analysis. The letters A, B, C, D, E, and F within the maps represent the six neotropical regions (see Figure 1).
Figure 5. Clade description and map of distribution areas for the genus Eupsittula. The estimated values of the TMRCA (HPD 95%) and the most likely ancestral area are indicated. The colored distribution areas in the map represent the current distribution of each species of the genus included in this analysis. The letters A, B, C, D, E, and F within the maps represent the six neotropical regions (see Figure 1).
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Figure 6. Clade description and map of distribution areas for the genus Psittacara. The estimated values of the TMRCA (HPD 95%) and the most likely ancestral area are indicated. The colored distribution areas in the map represent the current distribution of each species of the genus included in this analysis. The letters A, B, C, D, E, and F within the maps represent the six neotropical regions (see Figure 1).
Figure 6. Clade description and map of distribution areas for the genus Psittacara. The estimated values of the TMRCA (HPD 95%) and the most likely ancestral area are indicated. The colored distribution areas in the map represent the current distribution of each species of the genus included in this analysis. The letters A, B, C, D, E, and F within the maps represent the six neotropical regions (see Figure 1).
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Table 1. Species distribution according to del Hoyo et al. [29] and codes assigned to the distribution areas. Common names of species are listed in Supplementary Table S2.
Table 1. Species distribution according to del Hoyo et al. [29] and codes assigned to the distribution areas. Common names of species are listed in Supplementary Table S2.
SpeciesDistributionArea Code
Amazona ochrocephalaPanama, Colombia, Venezuela, Guianas, Brazil, Ecuador, Peru, BoliviaBCD
Anodorhynchus hyacinthinusBrazil, Bolivia, ParaguayCD
Anodorhynchus leariBrazilD
Ara ambiguousHonduras, Nicaragua, Costa Rica, Panama, Colombia EcuadorAB
Ara araraunaPanama, Colombia, Venezuela, Guianas, Ecuador, Peru, Bolivia Brazil, Paraguay, Argentina, EcuadorBCDE
Ara chloropterusPanama, Colombia, Venezuela, Guianas, Brazil, Paraguay, Ecuador, Peru, Bolivia, Argentina.BCDE
Ara glaucogularisBoliviaC
Ara macaoMexico, Central America, Colombia, Venezuela, Guianas, Brazil, Ecuador, Peru, BoliviaABCD
Ara militarisMexico, Venezuela, Colombia, Ecuador, Peru, Bolivia, ArgentinaABCD
Ara severusPanama, Colombia, Ecuador, Venezuela, Guianas, Peru, Bolivia, BrazilBCD
Aratinga auricapillusBrazilDE
Aratinga jandayaBrazilCDE
Aratinga maculataBrazilC
Aratinga nendayBolivia, Brazil, Paraguay, ArgentinaCD
Aratinga solstitialisBrazil, GuianaC
Aratinga weddelliiColombia, Ecuador, Peru, Brazil, BoliviaCD
Bolborhynchus lineolaMexico, Panama, Venezuela, Colombia, BoliviaABC
Cacatua sulphurea-G
Columba livia-G
Conuropsis carolinensisUnited States of AmericaA
Coracopsis vasa-G
Cyanoliseus patagonusArgentina, Uruguay, ChileDF
Cyanopsitta spixiiBrazilD
Deroptyus accipitrinusColombia, Ecuador, Peru, Venezuela, Guianas, Brazil, BoliviaC
Diopsittaca nobilisVenezuela, Guianas, Brazil BC
Enicognathus leptorhynchusChile F
Eupsittula aureaSuriname, Brazil, Peru, Bolivia, Paraguay, ArgentinaCDE
Eupsittula cactorumBrazilCDE
Eupsittula canicularisMexico, Costa RicaAB
Eupsittula canicularisMexico, Costa RicaAB
Eupsittula canicularisMexico, Costa RicaAB
Eupsittula nanaMexico, JamaicaA
Eupsittula pertinaxPanama, Colombia, Venezuela, Antillas, Guiana, BrazilBC
Falco peregrinus-G
Forpus coelestisEcuador, Peru, ColombiaBF
Forpus conspicillatusPanama, Colombia, VenezuelaB
Forpus cyanopygiusMexicoA
Forpus modestusColombia, Venezuela, Brazil, Ecuador, Peru, BoliviaC
Forpus passerinusColombia, Venezuela, Trinidad, Guianas, BrazilBC
Forpus xanthopsPeruC
Forpus xanthopterygiusColombia, Ecuador, Peru, Brazil, Bolivia, Paraguay, ArgentinaCDE
Guaruba guaroubaBrazilC
Hapalopsittaca melanotisPeru, BoliviaC
Leptosittaca branickiiColombia, Ecuador, PeruBF
Melopsittacus undulatus-G
Myiopsitta monachusBolivia, Paraguay, Brazil, Argentina, UruguayCDEF
Nestor notabilis-G
Orthopsittaca manilatusColombia, Ecuador, Peru, Bolivia, Venezuela, Trinidad, Guianas, BrazilBCDE
Pionites leucogasterBrazil CD
Pionites melanocephalusColombia, Venezuela, Guianas, Brazil, Ecuador, Peru C
Primolius auricollisBolivia, Brazil, Paraguay, ArgentinaCD
Primolius couloniPeru, Brazil, BoliviaC
Primolius maracanaBrazil, Parana, Paraguay, ArgentinaCDE
Psilopsiagon aymaraBolivia, ArgentinaCDF
Psittacara brevipesMexicoA
Psittacara chloropterusHispaniola IslandA
Psittacara erythrogenysEcuador, PeruB
Psittacara euopsCubaA
Psittacara finschiNicaragua, Costa Rica, PanamaAB
Psittacara holochlorusMexico, NicaraguaA
Psittacara h. rubritorquisGuatemala, El Salvador, Honduras, NicaraguaA
Psittacara leucophthalmusColombia, Ecuador, Peru, Brazil, Guianas, Venezuela, Bolivia, Paraguay, Argentina, UruguayBCDE
Psittacara mitratusPeru, Bolivia, ArgentinaCD
Psittacara wagleriColombia, VenezuelaB
Pyrrhura albipectusEcuador, PeruC
Pyrrhura frontalisBrazil, Paraguay, Argentina, UruguayDE
Pyrrhura hoffmanniCosta Rica, PanamaB
Pyrrhura leucotisBrazilE
Pyrrhura molinaeBolivia, Brazil, Paraguay, ArgentinaCD
Pyrrhura perlataBrazil, BoliviaCD
Pyrrhura pictaVenezuela, Brazil C
Pyrrhura rupicolaPeru, Brazil, BoliviaC
Rhynchopsitta pachyrhynchaMexicoA
Rhynchopsitta terrisiMexicoA
Thectocercus acuticaudatusColombia, Venezuela, Brazil, Bolivia, Paraguay, ArgentinaBCD
Touit purpuratusVenezuela, Brazil, Colombia, Ecuador, PeruC
Table 2. Pairwise genetic distance between Psittacara species, estimated under K2P model using ND2 (above diagonal) and COI (below diagonal).
Table 2. Pairwise genetic distance between Psittacara species, estimated under K2P model using ND2 (above diagonal) and COI (below diagonal).
PleuPwagPmitPeuoPchlPeryPhruPholPfinPbre
Pleu 0.0510.0610.0600.0660.0670.0710.0700.0700.063
Pwag0.053 0.0300.0440.0450.0390.0430.0470.0410.045
Pmit0.0430.026 0.0290.0280.0270.0320.0400.0290.034
Peuo0.0530.0330.029 0.0220.0250.0330.0410.0250.029
Pchl0.0580.0360.0310.015 0.0270.0340.0420.0270.030
Pery----- 0.0180.0250.0150.020
Phru0.0630.0410.0360.0190.022- 0.0160.0130.019
Phol0.0660.0430.0380.0220.024-0.006 0.0210.024
Pfin0.0640.0410.0360.0190.022-0.0130.011 0.011
Pbre0.0610.0380.0290.0170.020-0.0110.0080.006
(Pleu) P. leucophthalmus; (Pwag) P. wagleri; (Pmit) P. mitratus; (Peuo) P. euops; (Pchl) P. chloropterus; (Pery) P. erythronegys; (Phru) P. h. rubritorquis; (Phol) P. holochlorus; (Pfin) P. finschi; (Pbre) P. brevipes. (-) No available data.
Table 3. Divergence times of the genera Aratinga, Eupsittula, and Psittacara.
Table 3. Divergence times of the genera Aratinga, Eupsittula, and Psittacara.
NodeMeanHPD 95%OriginProbability of Area
111.698.96–14.71Indeterminate (most probable C)0.37
1a7.665.76–9.82Amazonian (C)1
213.1510.25–16.24Most probable D/or CD0.52/0.47
2a10.988.23–14.02Most probable D/or C0.52/0.47
2b9.246.43–12.32Most probable AD/or AC0.53/0.46
2c1.20.74–1.78Indeterminate (most probable CD)0.35
314.511.46–17.86Indeterminate (most probable F)0.18
3a4.773.13–6.72Amazonian (C)1
3b3.452.03–5.28Chaco (D)1
45.383.76–7.36Amazonian (C)1
4a1.921.36–2.58North American (A)1
57.885.59–10.85Amazonian (C)1
5a0.660.34–1.11Most probable A/B 0.51/0.49
65.093.5–7.01Amazonian (C)1
6a0.820.33–1.48Indeterminate (CE)1
6b0.20.0–0.84Amazonian (C)1
717.814.28–21.75Indeterminate (most probable AC/ACD)0.63/0.37
814.2111.32–17.41Indeterminate (most probable CD)0.38
915.0811.66–18.87Amazonian (C)1
1015.9512.81–19.39Indeterminate (most probable D)0.22
1120.4116.25–24.86Amazonian (C)1
1213.49.47–17.82Amazonian (C)1
1329.9324.45–35.81Amazonian (C)1
1435.6529.21–42.52Indeterminate (CG)1
The mean and HPD 95% values are in millions of years. The nodes correspond to the chronogram in Figure 2; HPD (high posterior density) indicates 95% confidence intervals for the estimation of node age.
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Padilla-Jacobo, G.; Monterrubio-Rico, T.C.; Cano-Camacho, H.; Zavala-Páramo, M.G. Origin and Diversification of the Genera Aratinga, Eupsittula, and Psittacara (Aves: Psittacidae). Diversity 2025, 17, 155. https://doi.org/10.3390/d17030155

AMA Style

Padilla-Jacobo G, Monterrubio-Rico TC, Cano-Camacho H, Zavala-Páramo MG. Origin and Diversification of the Genera Aratinga, Eupsittula, and Psittacara (Aves: Psittacidae). Diversity. 2025; 17(3):155. https://doi.org/10.3390/d17030155

Chicago/Turabian Style

Padilla-Jacobo, Gabriela, Tiberio Cesar Monterrubio-Rico, Horacio Cano-Camacho, and María Guadalupe Zavala-Páramo. 2025. "Origin and Diversification of the Genera Aratinga, Eupsittula, and Psittacara (Aves: Psittacidae)" Diversity 17, no. 3: 155. https://doi.org/10.3390/d17030155

APA Style

Padilla-Jacobo, G., Monterrubio-Rico, T. C., Cano-Camacho, H., & Zavala-Páramo, M. G. (2025). Origin and Diversification of the Genera Aratinga, Eupsittula, and Psittacara (Aves: Psittacidae). Diversity, 17(3), 155. https://doi.org/10.3390/d17030155

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