Origin and diversification of the genera Aratinga, Eupsittula and Psittacara (Aves: Psittacidae)

doi:10.21203/rs.3.rs-2629125/v2

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Origin and diversification of the genera Aratinga, Eupsittula and Psittacara (Aves: Psittacidae)

https://doi.org/10.21203/rs.3.rs-2629125/v2

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The arrival of psittacines 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 psittacines, 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 the ancestral areas of the genera Aratinga, Eupsittula and Psittacara and related genera were estimated to propose hypotheses of origin, diversification, and dispersal of groups under a Bayesian inference framework based on mitochondrial molecular markers. 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 were integrated by different genera. The genera Aratinga and Eupsittula originated during the Miocene, and the genus Psittacara originated at the Miocene-Pliocene boundary. Aratinga is the oldest, followed by Eupsittula and the youngest is Psittacara. Biogeographic reconstruction suggests that the most likely origin of these genera is the Amazonian or Chaco regions. The diversification of these groups is 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 dispersion routes from south to north in the Neotropics and the use of the Greater and Lesser Antilles as a northward path.

Psittaciformes

Arini

Bayesian inference

phylogeny

historical biogeography

Neotropics

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 (Berkunsky et al., 2017; Cantú-Guzmán et al., 2007). Consequently, all neotropical psittaciform species are listed in the CITES protected species appendices (CITES, 2022).

In the Neotropics, parrots are exceptionally rich in species, and there are approximately 158 species distributed from northern Mexico to southern South America (Clements et al., 2021; Forshaw, 1989). 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 (Collar, 1997; Darlington, 1957; Forshaw, 1989; Joseph et al., 2012; Schweizer et al., 2011). The records for the northernmost distribution of psittacines in America are for Rhynchopsitta pachyrhyncha, which was recorded from the mountains of southern Arizona, and the extinct Conuropsis carolinensis, which inhabited large areas throughout the eastern United States (Forshaw, 1989; Wetmore, 1935).

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 (Eberhard and Bermingham, 2005; Eberhard et al., 2004; Ribas et al., 2005, 2006; Ribas and Miyaki, 2004; Tavares et al., 2006). 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 roosts, topographic complexity, and geographic position promote bird biodiversity in Mexico (Escalante-Pliego et al., 1993). In this sense, Weir et al. (2009) recognized the role of events such as the Great American Biota Exchange in promoting the exchange of bird species between North and South America. Furthermore, they proposed that the direction of bird traffic across the land bridge was primarily from south to north (Weir et al., 2009). In this exchange, the arrival of psittacines from the south to the north is intuited; however, for North American parrots, there are no publications on the influence of events such as the great exchange of American biota or proposals on the time of divergence.

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, which to date has not been considered under this approach. In addition, these genera are widely distributed with species present in northern Mexico, Central America, the Caribbean islands and South America (Forshaw, 1989, 2010; Howell and Webb, 1995). Therefore, they are a good example for inferring 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 (Peters, 1937; Salvadori, 1891; Vigors, 1825), and for more than eighty years, this genus was considered a monophyletic group (Peters, 1937; Remsen et al., 2013) (Table 1). 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 (BLI, 2015; Chesser et al., 2014; Clements et al., 2021; del Hoyo et al., 2014; Remsen et al., 2013) (Table 1). 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 (BLI, 2015; Chesser et al., 2014; Clements et al., 2021; del Hoyo et al., 2014; Remsen et al., 2013) (Table 1). Although there are independent studies where relationships have been established between some species of these genera, there is no consensus on the relationships between them and with other related ones, mainly because these relationships have been established independently and with a limited number of species. To show the scope of the proposals made on relationships between genera, according to different authors, the related genera are Diopsittaca, Guaruba, Pyrrhura, Anodorhynchus, Nandayus, Cyanopsitta, Primolius, Ara, Orthopsittaca, and Leptosittaca (Kirchman et al., 2012; Ribas and Miyaki, 2004; Tavares et al., 2006, 2004).

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 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.

Sequence samples

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 (2004), Tavares et al. (2006, 2004), Kirchman et al. (2012), and the proposed Arini tribe of Joseph et al. (2012). In detail, a total of 76 terminal taxa were included in the analyses, of which 54 belonged to the Arini tribe. According to the classification of Remsen et al. (2013) and Clements et al. (2021), we included all species of the genera Aratinga (6 species) and Eupsittula (5 species). Additionally, according to the classification by Clements et al. (2021), we included 9 of 10 living species of Psittacara (and the subspecies P. h. rubritorquis), 7 of 9 species from Forpus, 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. (2021), 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) (Table 2). We analyzed the sequences of two molecular markers of mitochondrial DNA (mtDNA): cytochrome c oxidase subunit I (COI) and NADH dehydrogenase subunit 2 (ND2) (Table 2).

Phylogenetic analysis

Sequence editing, alignments, and the construction of the data matrices were carried out with Sequencher v.4.1 (Gene Codes Corporation, 2015) and PhyDE (Müller et al., 2005). To estimate genetic distances (uncorrected p distance) among closely related species we used MEGA 5.05 software (Tamura et al., 2011). 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 2.1.1 (Posada, 2008) and selected using the corrected Akaike Information Criterion (cAIC) (Alfaro and Huelsenbeck, 2006). 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 - Hasegawa et al., 1985), for ND2, GTR+G+I (General Time Reversible + Gamma distribution of rates among sites + Invariant sites - Tavaré, 1986), 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) (Zwickl, 2006) and MrBayes v3.2 (Ronquist and Huelsenbeck, 2003) software, respectively. The branch support values were estimated by bootstrap probability (BP) of 500 replicates and by posterior probability (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 v1.4.0 (Rambaut, 2012).

Inference of divergence time

To estimate divergence times, we considered data from previous calibrations performed by Jarvis et al. (2014), who proposed estimates made under Bayesian inference with genomic sequences from 45 bird species. Based on nineteen fossil age calibrations, they proposed that the most basal divergences within Neoaves (Columbea-Passerea) occurred before the Cretaceous-Paleogene transition (67 to 69 million years ago -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 (Drummond and Rambaut, 2007). 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 (Aldous, 2001; Yule, 1924). 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 (Drummond and Rambaut, 2007). The results were summarized using TreeAnnotator v1.7.4 (Drummond and Rambaut, 2007). 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 v1.4.0 (Rambaut, 2012).

Reconstruction of ancestral areas

Reconstruction of ancestral areas was performed using 10,001 trees generated by BEAST (Drummond and Rambaut, 2007). Dispersal-vicariance analysis was performed using the S-DIVA tool in RASP v 3.0 (Yu et al., 2014). S-DIVA analyses are advantageous because they provide statistical support for ancestral area reconstructions (Yu et al., 2010). To run S-DIVA, we follow the recommendations of the authors of the program (Yu et al., 2014), taking into account binary trees = 10,001, discard trees = 1000, and random trees = 100. In this analysis, six geographic zones were considered: A) Central/North American, B) Northwestern/South American, C) Amazonian, D) Chaco, E) Parana and F) South American transition (Fig. 2A). 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 south and east Brazil. The South American transition region (F) comprises the Highlands of the Andes between western Venezuela and northern Chile and central western Argentina (Fig. 2A). The distributions of the genera were established in geographic maps according to records produced by different authors and summarized in del Hoyo et al. (2014) (Table 3).

Phylogenetic analyses

To the best of our knowledge, our study is the most complete presented to date on the Arini tribe; 94.4% of the genera recognized in the Arini tribe were covered. In particular, for the genus Psittacara, 90% of the recognized species were considered, and for the Aratinga and Eupsittula genera, 100% of the species within each genus were included (Table 2). The alignments contained 1610 bp 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.

BI and ML analyses produced trees with similar topologies. Overall, PP and BP values provided sufficient support for the phylogenetic relationships established within each group (Fig. 1). 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 consisted of different genera as follows: Clade 1 (C1) was formed by the genera Ara, Primolius and Orthopsittaca, which was retrieved as the basal genus in the clade; Clade 2 (C2) was formed by the genera Aratinga, Conuropsis and Cyanopsitta; and Clade 3 (C3) was formed by the genera Thectocercus, Diopsittaca, Guaruba, Leptosittaca, Enicognathus, Anodorhynchus, and Cyanoliseus (Fig. 1).

Regarding the genera (Aratinga, Eupsittula and Psittacara) that were the main objective of this work, our results show that clade C2 containing the genus Aratinga is sister to clade C1 and that the genus Eupsittula is a sister clade to the Psittacara clade. Clade C2 contains eight taxa, including six species from the genera Aratinga, the extinct Conuropsis carolinensis and Cyanopsitta spixii. In this clade, the position of Cyanopsitta spixii as a basal genus is weakly supported; therefore, more analyses are recommended. Additionally, in a well-supported node, A. weddellii is the ancestor of C. carolinensis and the rest of the Aratinga species. Within the Eupsittula clade, 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.

Within the Psittacara clade is subclade 1 (Sc1), which includes P. finschi, P. brevipes, P. holochlorus, P. h. rubritorquis, and P. erythrogenys (Fig. 1). The topologies of the BI and ML trees show P. holochlorus and P. h. rubritorquis (P. rubritorquis in the tree) as sister taxa, which also have a low genetic distance (Table 4). P. brevipes was found to be closely related to P. finschi. The genetic distance between P. holochlorus and P. brevipes was greater than that between P. brevipes and P. finschi (Table 4). We found P. chloropterus and P. euops to be sister species closely related to Sc1 (Fig. 1). In addition, P. leucophthalmus, P. wagleri and P. mitratus indicate an early divergence within the Psittacara clade, where P. leucophthalmus can be observed as a basal species. The greatest genetic distance between the closely related species in this genus was 0.071 (with ND2) between P. leucophthalmus and P. h. rubritorquis, and the shortest distance was 0.006 (with COI) between P. brevipes and P. finschi (Table 4).

Inference of divergence times and reconstruction of ancestral areas

The estimated age of the nodes and the biogeographic reconstruction are shown in Table 5 and Figure 2. In convergence testing for Bayesian analyses (Kass et al., 1998), the ESS values 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 5, Fig. 2), and their split was estimated to have occurred approximately 11.32-17.41 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 5, Fig. 2). Here, the genus Ara diverges during the Miocene, approximately 5.76-9.82 Mya, in the Amazonian region (node 1a, Table 5, Fig. 2).

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 5, Fig. 2). Within C2, the subsequent diversification of the genus Aratinga (including C. carolinensis) occurred approximately 8.23-14.02 Mya; the biogeographic reconstruction obtained with S-DIVA shows this clade with an origin in the Amazonian or Chaco regions (regions C or D) (node 2a, Table 5, Figs. 2 and 3). 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 5, Figs. 2 and 3); A. jandaya, A. auricapillus, A. maculata, and A. solstitialis are the youngest group with a time of the most recent common ancestor (TMRCA) estimated to be approximately 0.74-1.78 Mya (node 2c, Table 5, Figs. 2 and 3). In this group, the S-DIVA results suggested three dispersal events and two vicariance events.

The divergence of the clade C3 lineages began at approximately 11.46-17.86 Mya, although the ancestral area of C3 could not be determined (node 3, Table 5, Fig. 2). 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 5, Fig. 2). Furthermore, TMRCA estimates for 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 5, Fig. 2).

According to the results, the sister genera Psittacara and Eupsittula are proposed to have diverged around the Langhian stage, and TMRCA was estimated to have occurred at approximately 11.66-18.87 Mya. The origins of these genera can be assigned to the Amazonian region (region C) (node 9, Table 5, Fig. 2). The genus Eupsittula was estimated to have originated 5.59-10.85 Mya (node 5, Table 5, Figs. 2 and 4). In this group, E. canicularis is the youngest 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, Figs. 2 and 4). 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 5, Figs. 2 and 5). Within this group, the species P. finschi, P. brevipes, P. rubritorquis, P. holochlorus, P. erythrogenys, P. euops, and P. chloropterus shared an ancestor dating to approximately 1.36-2.58 Mya and diversified in the Central-North American region (region A) (node 4a, Table 5, Figs. 2 and 5). In this clade, the S-DIVA suggested three dispersal events and three vicariance events.

On the other hand, the genus Pyrrhura diverges during the Pliocene epoch, originating at approximately 3.5-7.01 Mya in the Amazonian region (region C) (node 6, Table 5, Fig. 2). In this clade, the sister species P. rupicola and P. molinae (node 6b, Table 5, Fig. 2) and P. picta and P. leucotis (node 6a, Table 5, Fig. 2) 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 of 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 5, Fig. 2). The TMRCA between R. pachyrhyncha and R. terrisi was estimated to have occurred approximately 0.04-0.42 Mya. S-DIVA results showed no dispersal or vicariance events in Rhynchopsitta.

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 (Fig. 1). 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. (2012). However, the relationship of Cyanopsitta is questionable; here, it is retrieved as the basal genus of Aratinga, and in Kirchman et al. (2012), their inference shows Cyanopsitta as basal to 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 (del Hoyo et al., 2017; Kirchman et al., 2012); however, in our results, C. carolinensis was integrated into clade C2 with the genus Aratinga.

Regarding the genus Eupsittula, our analysis recovered the relationship of E. aurea and E. nana as sister species, as observed by Kirchman et al. (2012) (Fig. 1). Our results also corroborate those of Remsen et al. (2013), who placed E. aurea and E. cactorum in this genus. However, our results contrast those of Kirchman et al. (2012), who proposed R. pachyrhyncha as a sister group to Eupsittula.

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 (Collar et al., 2016; Collar and Sharpe, 2016). However, in our results, the phylogenetic trees and genetic distance demonstrate that P. leucophthalmus is basal and distant from P. finschi and P. chloropterus (Fig. 1). Similar to what was observed by Kirchman et al. (2012), in this study, P. euops and P. chloropterus are sister species. Additionally, P. holochlorus is conspecific with P. rubritorquis (Fig. 1, Table 4). We found that P. brevipes (restricted to the Revillagigedo Islands of Mexico) is clearly not a subspecies of P. holochlorus (distributed from the eastern and southern of Mexico to northern Nicaragua), as has traditionally been considered (BLI, 2015; del Hoyo et al., 2014). The genetic distance of P. brevipes is greater with P. holochlorus than with P. finschi (distributed in Nicaragua, Costa Rica, and Panama) (Table 4). In trees, P. finschi and P. brevipes are placed in an unresolved subclade. However, the inclusion of another taxon and character could resolve this uncertainty.

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 only a few taxa diverged more recently in the Pleistocene epoch (Fig. 2). 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 (Antonelli et al., 2009; Barker, 2007; Brumfield and Edwards, 2007; Brumfield et al., 2007; Burns and Naoki, 2004; Cheviron et al., 2005; Cortés-Ortiz et al., 2003; García-Moreno and Fjeldså, 2000; Lim, 2007; Lovette, 2004; Miller et al., 2008; Santos et al., 2009).

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 (Leigh et al., 2013; O’Dea et al., 2016; Woodburne, 2010). 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 (Weir et al., 2009).

Our results on the genera Aratinga, Eupsittula and Psittacara show that among the three, the genus Aratinga is the oldest, followed by Eupsittula and the youngest is Psittacara (Fig. 2B). These genera originated in South America, most likely in the Amazon region (Fig. 2A). For the genus Aratinga (8.23-14.02 Mya) with A. weddellii as their ancestor, 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 (Fig. 3). The northernmost species of all American parrots, C. carolinensis (6.43-12.32 Mya), would have originated through a vicariance event during 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 (Fig. 3).

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 (Fig. 4). Range expansion occurred mainly to southeastern and northeastern South America and westward 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) (Fig. 4). 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 (Hoorn et al., 2010). 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 until the Isthmus of Panama was well established (last closed 3.5 Mya (Leigh et al., 2013), with range expansion and subsequent speciation in situ (Fig. 4). We propose that populations from northern Mexico expanded their range northwestward, perhaps following the tropical dry forest (Pacific slope) with which it is strongly associated (Forshaw, 1989).

Age estimates for species of the genus Psittacara are presented here for the first time. According to our results, Psittacara is a recent genus whose divergence began at the Miocene-Pliocene limits (Fig. 5). 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, coinciding with the disappearance of the Acre system and the establishment of modern drainage in the Amazon basin (Hoorn et al., 2010). Additionally, it has been proposed that the Andes are an important geographic barrier that has promoted diversification in various bird species (Burns and Naoki, 2004; Cheviron et al., 2005; Weir, 2009). Considering the geographic range of P. leucophthalmus and P. wagleri and our results, we propose that the northern Andes (Venezuela and Colombia) are the geographic barrier that promoted diversification (Fig. 5). The uplift of the Andes of Colombia and Venezuela occurred approximately 5-3 Mya (Audemard, 2003; Dhont et al., 2005; Gregory-Wodzicki, 2000), which coincides with the origin of P. wagleri at 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 (Fig. 5). For the species distributed in Central and North America and in the Antilles, we propose that diversification most likely occurred in Central America, where 85.71% of its species are found (Fig. 5). Diversification of this subgroup occurred after the establishment of the Isthmus of Panama 3.5 Mya (Leigh et al., 2013), suggesting range expansion and subsequent in situ speciation, particularly for P. finschi, P. rubritorquis and P. holochlorus, which reached northwestern and eastern Mexico (del Hoyo et al., 2014; Howell and Webb, 1995).

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 (Coates et al., 2004; Fritz et al., 2012; Parada et al., 2013; Prothero et al., 2014; Weir et al., 2008). Subsequently, the genus recently diversified (TMRCA = 0.04-0.42 Mya) in Mexico during the Pleistocene epoch.

To the best of our knowledge, this report includes analyses of the largest number of species of the Arini tribe. 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 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). We propose that the genera Rynchopsitta and C. carolinensis 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 species and subspecies within each group and expand the number of characters to refine the proposed results.

Acknowledgements

We appreciate the funding from the Consejo Nacional de Ciencia y Tecnología (CONACYT, Graduate Studies Scholarship No. 359650 to GPJ, research project CONACYT-2002-C01-00021 to TCMR, and Fondos Mixtos CONACYT-Michoacán, research project Clave 41168 to MGZP, HCC and TCMR), and the Coordinación de la Investigación Científica de la Universidad Michoacana de San Nicolás de Hidalgo (CIC-UMSNH, research projects 2014-2015, 2016-2017 to MGZP).

Author´s contribution

MGZP, GPJ, TCMR, and HCC conceived and designed the study. GPJ carried out the experiments. GPJ and MGZP carried out the bioinformatics analyses. GPJ, MGZP, TCMR, and HCC drafted the manuscript. All authors read and approved the final manuscript.

Data availability

The datasets supporting the conclusions of this article are available in the GenBank repository [https://www.ncbi.nml.gov/] under the accession numbers listed in Table 2.

Conflict of interest

The authors declare that they have no conflicts of interest.

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No competing interests reported.

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Origin and diversification of the genera Aratinga, Eupsittula and Psittacara (Aves: Psittacidae)

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