Bridging Evolutionary History and Conservation of New World Vultures

Abstract

Simple Summary
This study focuses on New World Vultures, a group of seven scavenger bird species with ecological significance. Despite their importance, there is limited knowledge about their evolutionary history and conservation needs. Recent advances in understanding their evolutionary relationships have paved the way for addressing these gaps using phylogenetic methods. By analyzing the species’ ancestral distribution in the Americas, we employed two techniques to identify historical dispersion patterns. This study pinpointed South America as their original area, with subsequent recolonization of North America by certain species. To guide conservation efforts, we used two indices. The Evolutionary Distinctiveness (ED) index measured species’ uniqueness according to their phylogeny, while the Global Endangerment (GE) index mapped phylogenetic diversity. The findings highlighted the Black Vulture, California Condor and Andean Condor as priority species based on their uniqueness and evolutionary significance. Additionally, we identified crucial regions for conservation, including the lowlands of the Amazon River basin, the Orinoco basin and various areas along the Guiana Shield’s tributaries. This research underscores the importance of combining evolutionary and ecological insights and tools to fill knowledge gaps about species of concern. By doing so, we can formulate effective strategies to protect these species in the face of ongoing biodiversity loss.

Abstract
The New World Vultures (Cathartidae) include seven species of obligate scavengers that, despite their ecological relevance, present critical information gaps around their evolutionary history and conservation. Insights into their phylogenetic relationships in recent years has enabled the addressing of such information gaps through approaches based on phylogeny. We reconstructed the ancestral area in America of the current species using two regionalization schemes and methods: Biogeography with Bayesian Evolutionary Analysis (BioGeoBears) and Bayesian Binary Model–Monte Carlo Markov Chains (BBM–MCMC). Then, we identified the priority species and areas for conservation by means of the Evolutionary Distinctiveness index (ED), as a proxy of the uniqueness of species according to phylogeny, and the Global Endangerment index (GE), mapping phylogenetic diversity. We found that the ancestral area of New World Vultures in America corresponds to South America, with dispersal processes that led to a recolonization of North America by Coragyps atratus, Gymnogyps californianus and Cathartes aura. We identified the Black Vulture, G. californianus and Vultur gryphus as priority species based on ED and “Evolutionary Distinct Globally Endangered” (EDGE) indexes, and the lowlands of Amazon River basin and the Orinoco basin and some tributaries areas of the Guiana Shield were identified as the priority areas when mapping the phylogenetic diversity. This study highlights the importance of filling knowledge gaps of species of conservation concern through the integration of evolutionary and ecological information and tools and, thus, developing adequate strategies to enhance the preservation of these species in the face of the current loss of biodiversity.

Full text

Citation: Cortés-Díaz, D.;
Buitrago-Torres, D.L.;
Restrepo-Cardona, J.S.;
Estellés-Domingo, I.; López-López, P.
Bridging Evolutionary History and
Conservation of New World Vultures.
Animals 2023,13, 3175. https://
doi.org/10.3390/ani13203175
Academic Editor: Brian L. Cypher
Received: 20 August 2023
Revised: 7 October 2023
Accepted: 8 October 2023
Published: 11 October 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
animals
Article
Bridging Evolutionary History and Conservation of
New World Vultures
Daniela Cortés-Díaz 1, Diana L. Buitrago-Torres 2, Juan Sebastián Restrepo-Cardona 3,4 ,
Irene Estellés-Domingo 5and Pascual López-López 5, *
1Semillero de Investigación en Ecología y Conservación, Universidad de La Salle, Bogotá110151, Colombia;
cortesdd9@gmail.com
2Programa de Biología, Universidad del Quindío, Carrera 15 #12N, Quindío 630004, Colombia;
dialu1989@gmail.com
3
Wildlife Ecology and Conservation, University of Florida, Gainesville, FL 32611, USA; jsrestrepoc@gmail.com
4Fundación Cóndor Andino—Ecuador, Quito 170143, Ecuador
5Movement Ecology Laboratory, Cavanilles Institute of Biodiversity and Evolutionary Biology,
University of Valencia, C/Catedrático JoséBeltrán 2, 46980 Paterna, Valencia, Spain; irene.estelles@uv.es
*Correspondence: pascual.lopez@uv.es
Simple Summary:
This study focuses on New World Vultures, a group of seven scavenger bird
species with ecological significance. Despite their importance, there is limited knowledge about
their evolutionary history and conservation needs. Recent advances in understanding their evolu-
tionary relationships have paved the way for addressing these gaps using phylogenetic methods.
By analyzing the species’ ancestral distribution in the Americas, we employed two techniques to
identify historical dispersion patterns. This study pinpointed South America as their original area,
with subsequent recolonization of North America by certain species. To guide conservation efforts,
we used two indices. The Evolutionary Distinctiveness (ED) index measured species’ uniqueness
according to their phylogeny, while the Global Endangerment (GE) index mapped phylogenetic
diversity. The findings highlighted the Black Vulture, California Condor and Andean Condor as
priority species based on their uniqueness and evolutionary significance. Additionally, we identified
crucial regions for conservation, including the lowlands of the Amazon River basin, the Orinoco basin
and various areas along the Guiana Shield’s tributaries. This research underscores the importance
of combining evolutionary and ecological insights and tools to fill knowledge gaps about species
of concern. By doing so, we can formulate effective strategies to protect these species in the face of
ongoing biodiversity loss.
Abstract:
The New World Vultures (Cathartidae) include seven species of obligate scavengers that,
despite their ecological relevance, present critical information gaps around their evolutionary history
and conservation. Insights into their phylogenetic relationships in recent years has enabled the
addressing of such information gaps through approaches based on phylogeny. We reconstructed
the ancestral area in America of the current species using two regionalization schemes and methods:
Biogeography with Bayesian Evolutionary Analysis (BioGeoBears) and Bayesian Binary Model–
Monte Carlo Markov Chains (BBM–MCMC). Then, we identified the priority species and areas for
conservation by means of the Evolutionary Distinctiveness index (ED), as a proxy of the uniqueness
of species according to phylogeny, and the Global Endangerment index (GE), mapping phylogenetic
diversity. We found that the ancestral area of New World Vultures in America corresponds to South
America, with dispersal processes that led to a recolonization of North America by Coragyps atratus,
Gymnogyps californianus and Cathartes aura. We identified the Black Vulture, G. californianus and Vultur
gryphus as priority species based on ED and “Evolutionary Distinct Globally Endangered” (EDGE)
indexes, and the lowlands of Amazon River basin and the Orinoco basin and some tributaries areas of
the Guiana Shield were identified as the priority areas when mapping the phylogenetic diversity. This
study highlights the importance of filling knowledge gaps of species of conservation concern through
the integration of evolutionary and ecological information and tools and, thus, developing adequate
strategies to enhance the preservation of these species in the face of the current loss of biodiversity.
Animals 2023,13, 3175. https://doi.org/10.3390/ani13203175 https://www.mdpi.com/journal/animals

Animals 2023,13, 3175 2 of 13
Keywords:
extinction; evolutionary distinctiveness; foraging strategies; phylogenetic comparative
methods; biogeography; Cathartidae; evolutionary distinctiveness; EDGE; raptors
1. Introduction
The New World Vultures (Family: Cathartidae) comprise an emblematic group of raptors
that includes seven species of obligate scavenging birds: the Andean Condor (Vulture gryphus),
Black Vulture (Coragyps atratus), California Condor (Gymnogyps californianus), Greater yellow-
headed Vulture (Cathartes melambrotus), King Vulture (Sarcoramphus papa), Lesser yellow-
headed Vulture (Cathartes burrovianus) and Turkey Vulture (Cathartes aura) [1–3].
Although this family has an undisputed monophyletic status, historically, the phy-
logenetic position of New World Vultures in avian phylogeny varies among different
studies [
4
–
8
]. However, more recent studies indicate that Cathartidae may be closely re-
lated to the families Accipitridae and Sagittariidae [
8
,
9
]. Furthermore, the phylogenetic
relationships within the family, mainly between the Andean Condor, California Condor,
King Vulture and Black Vulture, have been a focus of discussion. Some analyses with nu-
cleotide sequences show that the Andean Condor is related to the King Vulture, while the
Black Vulture is a sister species of the California Condor [
9
–
11
]. However, Johnson et al. [
12
]
have a different proposal: the family can be divided into two monophyletic groups: in the
first one, the Andean Condor, King Vulture and California Condor are related, while in the
second one, the Black Vulture is more related to species of the genus Cathartes.
Currently, the New World Vultures are restricted to the Americas and reach their
highest diversity in the Neotropical region ([
1
]; see species’ distribution and IUCN status
in http://datazone.birdlife.org/species/search accessed on 10 October 2023). There, the
Lesser yellow-headed Vulture is distributed from western Mexico to northern Argentina in
areas associated with water bodies, secondary forests and forest edges [
13
]. The Greater
yellow-headed Vulture habits moderately altered and unaltered Amazonian forest and
forest–grassland ecotones [
13
]. The King Vulture is distributed from Mexico to Argentina
in dense and open forests, savannahs and coastal meadows [
14
] and the Andean Condor
is distributed throughout the Andes mountain range in primary and secondary forests,
“páramos”, open grasslands and coastal areas [
15
]. In the Nearctic region, the California
Condor is restricted to the coastal mountain ranges of Southern California and Northern
Baja California in the USA [
16
]. In contrast, the Black Vulture and the Turkey Vulture are
distributed both in the Neotropical and Nearctic regions in a wide variety of both natural
and anthropogenic habitats [17].
New World Vultures are among the world’s most threatened birds due to habitat
loss and the consequent decrease in food sources as well as the high incidence of poi-
soning and hunting as a consequence of human–wildlife conflicts [
18
–
21
]. These threats
have severely affected populations, mainly of the California Condor and the Andean Con-
dor [
22
]. Estimates indicate that the California Condor has a global population of less than
500 individuals, so it is categorized as a Critically Endangered species [
23
], and the Andean
Condor has a global population of about 6700 individuals with a declining population
size and is classified as Vulnerable [
23
]. The other New World Vultures are species of
Least Concern and wide distribution [
24
–
28
]. However, the King Vulture and the Greater
yellow-headed Vulture present declining populations [
25
,
28
] and trends indicate that New
World Vultures could face critical future scenarios if adequate conservation measures are
not rapidly implemented [29,30].
The New World Vultures play a critical role within birds’ communities and provide
essential ecosystem services, since carrion consumption plays a key role in nutrient flow
and mitigates the potential transmission of infectious diseases [
31
–
33
]. In fact, it has been
shown that the decrease in scavengers has caused an increase in the stray dog population
and, thus, in human exposure to rabies [34]. In addition, disposal of livestock and human
waste by these scavengers has contributed to reducing water pollution [
35
]. Therefore,

Animals 2023,13, 3175 3 of 13
these species are able to structure biological communities in ecosystems and are indicators
of environmental and human health [
36
]. Due to their ecological importance and the risk
of extinction of some of these species, this group offers an interesting model to evaluate
different metrics for the conservation of birds and their habitats.
Thanks to the most recent contributions to the reconstruction of the tree of life
in the last two decades (e.g., [
37
–
41
], conservation biology has begun to include ele-
ments of species evolutionary history in assessments of entire groups of species (see, e.g.,
https://birdtree.org/;https://earlybird.biology.ufl.edu/,https://b10k.genomics.cn/; all
accessed on 10 October 2023). Among these measures, the evolutionary distinctiveness (ED)
captures the evolutionary uniqueness of the species, shedding light on more detailed as-
pects of phylogenetic diversity. Also, when the ED is weighted with the extinction risk, this
provides an index known as EDGE, which becomes a useful variable tool in identifying and
prioritizing irreplaceable key species in clades and ecosystems [
42
–
44
] since phylogenetic
diversity can also play as a proxy of functional and morphological diversity [45–47].
Given their complex evolutionary history, ecological importance and conservation
status, the New World Vultures are an interesting group in which to address some infor-
mation gaps, implementing emerging integrative analyses. Thus, the aims of this study
are: (i) to infer the most likely ancestral area of the most common recent ancestor (MCRA)
of extant species of New World Vultures; and (ii) to estimate the phylogenetic diversity,
evolutionary distinctiveness and EDGE values for this group of birds.
2. Methods
We used the most complete and robust molecular phylogeny of the New World
Vultures inferred by Johnson et al. [
12
] for all analyses in this study. This phylogeny corre-
sponds to a maximum clade credibility tree (MCC), reconstructed with Bayesian inference
from two mtDNA genes (Cyt-b and ND2) and five sets of nuclear introns (EEF2, GAPDH,
HMGN2, RHOD and TGFb2). Johnson’s [
12
] phylogenetic tree provides an estimate of
divergence times and is supported by posterior probabilities of nodes mostly greater than
0.8. It includes representative species of the most related families (e.g., Pandionidae, Sagit-
tariidae and Accipitridae). However, we keep apart the clade corresponding to the New
World Vultures species in order to perform the subsequent analyses (Figure 1).
2.1. Biogeography
We used a sample of 151 trees by Johnson et al. [
12
] sourced from a GitHub repository
(https://github.com/FePhyFoFum/phyx accessed on 10 October 2023) in combination
with the MCC. For the inference of the MRCA of the New World Vultures, we performed
biogeographic reconstructions by setting two large-scale regionalization schemes: a first
biogeographic reconstruction in which we used the Neotropical and Nearctic regions and a
second biogeographic reconstruction in which we used three more specific areas, namely
(i) North America (including the United States and northern Mexico), (ii) Central America
(from the tropical belt of Mexico to the Isthmus of Panama) and (iii) South America. We
did not increase the spatial resolution of the analyses to include more areas, since the
probabilities of the ancestral areas calculated by the algorithm (<15%) were very low
relative to the uncertainty (20%).
We tested two methods implemented in Reconstruct Ancestral State in Phylogenies
(RASP): Biogeography with Bayesian Evolutionary Analysis (BioGeoBears) and Bayesian Bi-
nary Model–Monte Carlo Markov Chains (BBM–MCMC) [
48
]. BioGeoBears is an R package
incorporated in RASP that allows one to infer ancestral areas by probabilistically comparing
several models, namely Dispersal–Extinction–Cladogenesis (DEC), a likelihood interpreta-
tion of Statistical Dispersal–Vicariance Analysis (DIVALIKE), a likelihood interpretation
of the Bayesian inference of historical biogeography for many discrete areas method (BA-
YAREALIKE) and a version of each of these models including the “J” parameter [
49
]. We
computed the Akaike Information Criterion corrected for small samples (AICc) for model
ranking. The BBM explains the phylogenetic uncertainty when estimating the probability

Animals 2023,13, 3175 4 of 13
of an ancestral range in an averaged node on a posterior set of trees [
50
]. In this analysis, we
implemented the F81 Gamma model and ran 10 MCMC for 1,000,000 generations, sampling
every 100 generations, with 25% of the initial samples discarded as burn-in [
50
,
51
]. In BBM
analysis, the maximum number of areas in both biogeographical reconstructions was set to
one, in order to override combinations of areas, so that the probability of each individual
area on the nodes could be determined.
Animals 2023, 13, x FOR PEER REVIEW 4 of 14
Figure 1. Illustration of the maximum clade credibility tree (MCC) of New World Vultures inferred
by Johnson et al. [12].
2.1. Biogeography
We used a sample of 151 trees by Johnson et al. [12] sourced from a GitHub repository
(hps://github.com/FePhyFoFum/phyx accessed on 10 October 2023) in combination with
the MCC. For the inference of the MRCA of the New World Vultures, we performed bio-
geographic reconstructions by seing two large-scale regionalization schemes: a first bio-
geographic reconstruction in which we used the Neotropical and Nearctic regions and a
second biogeographic reconstruction in which we used three more specific areas, namely
(i) North America (including the United States and northern Mexico), (ii) Central America
(from the tropical belt of Mexico to the Isthmus of Panama) and (iii) South America. We
did not increase the spatial resolution of the analyses to include more areas, since the
probabilities of the ancestral areas calculated by the algorithm (<15%) were very low rel-
ative to the uncertainty (20%).
We tested two methods implemented in Reconstruct Ancestral State in Phylogenies
(RASP): Biogeography with Bayesian Evolutionary Analysis (BioGeoBears) and Bayesian
Binary Model–Monte Carlo Markov Chains (BBM–MCMC) [48]. BioGeoBears is an R pack-
age incorporated in RASP that allows one to infer ancestral areas by probabilistically com-
paring several models, namely Dispersal–Extinction–Cladogenesis (DEC), a likelihood in-
terpretation of Statistical Dispersal–Vicariance Analysis (DIVALIKE), a likelihood inter-
pretation of the Bayesian inference of historical biogeography for many discrete areas
method (BAYAREALIKE) and a version of each of these models including the “J” param-
eter [49]. We computed the Akaike Information Criterion corrected for small samples
(AICc) for model ranking. The BBM explains the phylogenetic uncertainty when estimat-
ing the probability of an ancestral range in an averaged node on a posterior set of trees
[50]. In this analysis, we implemented the F81 Gamma model and ran 10 MCMC for
1,000,000 generations, sampling every 100 generations, with 25% of the initial samples
Figure 1.
Illustration of the maximum clade credibility tree (MCC) of New World Vultures inferred
by Johnson et al. [12].
2.2. Phylogenetic Diversity, Evolutionary Distinctiveness and EDGE Species
The identification of EDGE species requires the analysis of two components: Evolu-
tionary Distinctiveness (ED) and Globally Endangered (GE) scores, based on the IUCN Red
List categories. To this end, firstly, we calculated the Evolutionary Distinctiveness (ED)
by “Fair proportion” of each species using the evol.distinc function implemented in the pi-
cante R package [
52
]. The “Fair proportion” measure consists of the sum of branch lengths
from root to each tip divided by the number of species descending from each branch [
53
].
Then, to obtain the Globally Endangered (GE) scores, we turned the current IUCN Red List
categories of species [
23
] into numerical values as proposed by Isaac et al. [
42
] as follows:
Least Concern (LC) = 0, Near Threatened (NT) and Conservation Dependent (LR/cd) = 1,
Vulnerable (VU) = 2, Endangered (EN) = 3 and Critically Endangered (CR) = 4. With the ED
and GE values, we identified the EDGE species by applying the following formula proposed

Animals 2023,13, 3175 5 of 13
by Isaac et al. [
42
]: EDGE = ln (1 + ED) + (GE
×
ln (2)). To optimize these calculations, we
compiled this formula into a function called edge.species (S1).
In order to quantify the loss of the phylogenetic diversity of New World Vultures, we
tested for hypothetical scenarios of extinction of species that reached the highest ED and
EDGE values. First, we calculated the phylogenetic diversity on the phylogeny of the whole
clade with the pd function in the picante R package [
52
]. This function computes the total
sum of phylogenetic branch lengths for any given dataset with an associated phylogeny. It
should be noted that phylogenetic diversity (PD) is not statistically independent of species
richness but rather shows a positive correlation with species richness. Then, we performed
the same calculation on phylogenetic trees excluding each of the identified priority species.
Finally, we mapped the phylogenetic diversity of New World Vultures to identify the
areas of highest biodiversity score in terms of each group’s evolutionary history using the
distribution polygons of each species from IUCN spatial data and mapping [
23
] and the
phyloregion R package [
54
]. We converted the polygons into a community matrix using the
polys2comm function with a resolution of 1
×
1 degree grid cells. Then, we calculated the
phylogenetic diversity with the pd function and, finally, we projected the results onto a map
of America using the plot_swatch function. In both analyses, phylogenetic diversity was
calculated as the total length of all branches of a set of taxa in a phylogenetic tree [55].
3. Results
3.1. Biogeography
According to model ranking, the BioGeoBears model that best fits the data in both
regionalization schemes is DEC (tables 1and 2). Reconstruction with this model suggested
that the most likely ancestral area of the MCRA of extant New World Vulture species
was the Neotropical region, particularly South America (Figure 2A,B). Although ancestral
area estimation using the DEC model did not provide high resolution, the exclusion of
combined areas in BBM analysis supports with a high probability (>75%) a neotropical–
South American origin (Figure 2A,B). Reconstruction of ancestral areas indicated that
dispersal was a key element in the speciation processes that shaped the current distribution
patterns of New World Vultures in America. Our results suggest that a first dispersal
event in the neotropics during the Miocene split the ancestral lineage into the clade of
vultures (Black Vulture, Turkey Vulture, Lesser yellow-headed Vulture and Greater yellow-
headed Vulture) and the clade of the condors (California Condor, King Vulture and Andean
Condor). Later, during this same period, a second dispersal event triggered the divergence
of the genus Cathartes and the Black Vulture. The Andean Condor then separated from the
California Condor and King Vulture lineage by a third process of dispersal that allowed
the former species to colonize the Andes. The divergence of the California Condor and the
King Vulture has a dispersion component, which probably promoted the establishment of
the California Condor in the Nearctic region, and a vicariant one, which is reflected in the
disjunction between the current distributions of both species.
Table 1.
Comparison of the six models evaluated with BioGeoBears for the regionalization scheme
of two areas (Neotropical and Nearctic) and their respective parameters and scores: Dispersion (d),
Extinction (e), Founder (j) and Akaike information criterion corrected for sample size (AICc).
Rank Model Parameters d e J AICc
1 DEC 2 0.071 0.0084 0 22.07
2 DIVALIKE 2 0.084 0.0062 0 22.72
3 BAYAREALIKE 2 0.081 0.039 0 24.91
4 DEC + J 3 0.044 1.0 ×10−12 0.38 26.49
5 DIVALIKE + J 3 0.056 1.0 ×10−12 0.36 27.49
6 BAYAREALIKE + J 3 0.037 1.0 ×10−70.29 29.89

Animals 2023,13, 3175 6 of 13
Table 2.
Comparison of the six models evaluated with BioGeoBears for the regionalization scheme of
three areas (North America, Central America and South America) and their respective parameters
and scores: Dispersion (d), Extinction (e), Founder (j) and Akaike information criterion corrected for
sample size (AICc).
Rank Model Parameters d e J AICc
1 DEC 2 0.078 0.0089 0 31.73
2 DIVALIKE 2 0.088 1.0 ×10−12 0 31.93
3 BAYAREALIKE 2 0.10 0.078 0 33.76
4 DEC + J 3 0.061 1.0 ×10−12 0.56 36.6
5 DIVALIKE + J 3 0.071 1.0 ×10−12 0.50 37.57
6 BAYAREALIKE + J 3 0.011 0.079 1.0 ×10−540.76
Animals 2023, 13, x FOR PEER REVIEW 7 of 14
Figure 2. Reconstruction of the ancestral areas inferred from the BBM analysis and the DEC model
using two regionalization schemes: (A) Nearctic and Neotropical region; (B) North America, Central
America and South America. The pie charts in the nodes represent the marginal probabilities of each
area and the areas combined. The biogeographic events associated with the diversification and dis-
tributions of the seven species of New World Vultures in America are indicated by arrows and as-
terisks. The leers in each reconstruction refer to the chosen areas; in the reconstruction of the first
regionalization scheme (above), we have the Nearctic area (A), the Neotropical area (B) and the com-
bination of both areas (AB), while in the reconstruction of the second regionalization scheme (be-
low), we have the area of North America (A), the area of Central America (B and area of South
America (C) and the rest of the leers are the combination of the main areas mentioned.
Figure 2.
Reconstruction of the ancestral areas inferred from the BBM analysis and the DEC model
using two regionalization schemes: (
A
) Nearctic and Neotropical region; (
B
) North America, Central
America and South America. The pie charts in the nodes represent the marginal probabilities of
each area and the areas combined. The biogeographic events associated with the diversification and
distributions of the seven species of New World Vultures in America are indicated by arrows and
asterisks. The letters in each reconstruction refer to the chosen areas; in the reconstruction of the
first regionalization scheme (above), we have the Nearctic area (A), the Neotropical area (B) and the
combination of both areas (AB), while in the reconstruction of the second regionalization scheme
(below), we have the area of North America (A), the area of Central America (B and area of South
America (C) and the rest of the letters are the combination of the main areas mentioned.

Animals 2023,13, 3175 7 of 13
3.2. Phylogenetic Diversity, ED and EDGE Species
The mean evolutionary distinctiveness (ED) score for New World Vulture species was
8.83 Ma, with the Black Vulture (ED—12.32 Ma) and the Andean Condor (ED—10.90 Ma)
reaching the highest values (Figure 3A). Linking ED scores to GE, the two species with the
highest risk of extinction were the California Condor (CR) and the Andean Condor (VU).
Overall, this indicates that the Black Vulture, California Condor and Andean Condor are pri-
ority species for conservation, given their distinctive evolutionary history (Figure 3A). The
phylogenetic diversity (PD) for New World Vulture species was 62 Ma. When comparing
the three hypothetical scenarios of extinction of the ED and EDGE species, the magnitude of
the loss of phylogenetic diversity given the extinction of the Black Vulture, Andean Condor
and California Condor would be 19%, 16% and 13%, respectively. Finally, by mapping the
phylogenetic diversity of New World Vultures, we found that the greatest richness and
phylogenetic diversity of this group of species are located in the Neotropics and tend to
decrease towards temperate areas. In fact, the maximum values are concentrated in the
Amazon, mainly in the lowlands close to the Amazon basin and the Orinoco basin and
other tributaries of the Guiana Shield (Figure 3B). In this area, five of the seven species
are distributed: the Black Vulture, Turkey Vulture, Lesser yellow-headed Vulture, Greater
yellow-headed Vulture and King Vulture, which together represent 44.2 Ma of evolutionary
history of the New World Vultures.
Animals 2023, 13, x FOR PEER REVIEW 8 of 14
3.2. Phylogenetic Diversity, ED and EDGE Species
The mean evolutionary distinctiveness (ED) score for New World Vulture species
was 8.83 Ma, with the Black Vulture (ED—12.32 Ma) and the Andean Condor (ED—10.90
Ma) reaching the highest values (Figure 3A). Linking ED scores to GE, the two species
with the highest risk of extinction were the California Condor (CR) and the Andean Con-
dor (VU). Overall, this indicates that the Black Vulture, California Condor and Andean
Condor are priority species for conservation, given their distinctive evolutionary history
(Figure 3A). The phylogenetic diversity (PD) for New World Vulture species was 62 Ma.
When comparing the three hypothetical scenarios of extinction of the ED and EDGE spe-
cies, the magnitude of the loss of phylogenetic diversity given the extinction of the Black
Vulture, Andean Condor and California Condor would be 19%, 16% and 13%, respec-
tively. Finally, by mapping the phylogenetic diversity of New World Vultures, we found
that the greatest richness and phylogenetic diversity of this group of species are located
in the Neotropics and tend to decrease towards temperate areas. In fact, the maximum
values are concentrated in the Amazon, mainly in the lowlands close to the Amazon basin
and the Orinoco basin and other tributaries of the Guiana Shield (Figure 3B). In this area,
five of the seven species are distributed: the Black Vulture, Turkey Vulture, Lesser yellow-
headed Vulture, Greater yellow-headed Vulture and King Vulture, which together repre-
sent 44.2 Ma of evolutionary history of the New World Vultures.
Figure 3. (A) Evolutionary distinctiveness (ED) and Evolutionary Distinct and Globally Endangered
(EDGE) scores. (B) Map of phylogenetic diversity (PD) of New World Vultures in America based on
distribution maps of species according to the IUCN. Geographic coordinates are expressed in deci-
mal degrees.
4. Discussion
Multiple hypotheses about the center of origin of the New World Vultures have
arisen. On the one hand, a North American origin was proposed [56] based on a fossil
from the late Eocene recorded in the United States [57] and, on the other hand, fossil rec-
ords in Europe dated from the transition Eocene/Oligocene support an Old World origin
[7,58]. Thus, this issue remains the focus of a controversial debate that is still in place and
requires more fossil evidence to be solved. In spite of this, advances in molecular
Figure 3.
(
A
) Evolutionary distinctiveness (ED) and Evolutionary Distinct and Globally Endangered
(EDGE) scores. (
B
) Map of phylogenetic diversity (PD) of New World Vultures in America based
on distribution maps of species according to the IUCN. Geographic coordinates are expressed in
decimal degrees.
4. Discussion
Multiple hypotheses about the center of origin of the New World Vultures have arisen.
On the one hand, a North American origin was proposed [
56
] based on a fossil from the late
Eocene recorded in the United States [
57
] and, on the other hand, fossil records in Europe
dated from the transition Eocene/Oligocene support an Old World origin [
7
,
58
]. Thus, this
issue remains the focus of a controversial debate that is still in place and requires more
fossil evidence to be solved. In spite of this, advances in molecular phylogenetics allow us

Animals 2023,13, 3175 8 of 13
to account for the dated phylogeny of the current species of New World Vultures, and with
this resource now available, we are able to infer the most recent biogeographic history of
the group, that is, from its arrival into the New World.
Our results suggest that the radiation of the seven current species of New World Vul-
tures took place in South America (Figure 2A,B). This hypothesis is supported by the record
of a Brazilian fossil morphologically similar to Coragyps dated from Late Oligocene/Early
Miocene [
59
,
60
] that is considered the oldest and best documented fossil of the family in
New World [
61
]. Then, two major events took place during the Middle Miocene: on the
one hand, speciation processes within the Condor clade gave rise to the Andean Condor
that colonized the Andes ~9 Ma ago [
12
], a period that coincides with the period after the
rampant orogenic processes of the region during the Early—Middle Miocene (as mentioned
by Blandin and Purser [
62
] and references therein). On the other hand, dispersal events
allowed the colonization of North America by the Black Vulture and the California Condor.
After their arrival, it is presumed that the genus Gymnogyps reached a wide distribution,
even outside North America, during the Pleistocene [
63
]. Regarding the whole clade of the
condors, based on two fossils assigned to this group recorded in the United States dated
~ 15–13 Ma, it has been suggested that the clade originated in North America and radiated
in South America [
60
] as a result of a dispersal process facilitated by the coastal winds
of the Western Andes [
64
]. Although this idea has been sustained for years, according to
our results, there is no likely reason to consider North America as the ancestral area of
the clade of condors, since this hypothesis implies a second recolonization event of South
America by the King Vulture and the Andean Condor, a less cost-effective and parsimo-
nious process than a South-American radiation with a single recolonization northward.
The genus Cathartes radiated during the Pliocene in South America, and then a process of
expansion of the distribution of the Turkey Vulture could have allowed this species to reach
North America.
It has been suggested that the radiation of megafauna in South America after the
Middle Miocene and the consequent increase in carrion availability [
65
,
66
] are related to the
diversification of scavengers in the New World. In particular, the increase in species richness
of the New World Vultures in the Plio-Pleistocene is strongly supported by numerous fossil
records in several localities across South America [
61
,
67
–
75
]. In consequence, a presumable
increase in interspecific competition could have triggered the development of distinctive
traits and behaviors to optimize the exploitation of resources, as the differential capacity in
the olfactory system [
76
–
78
] thus, decreasing the overlap between sympatric species [
77
,
78
].
Our findings indicate that the Black Vulture, Andean Condor and California Condor
must be considered conservation-priority species based on their uniqueness and evolu-
tionary significance (Figure 3A). The Black Vulture is a resilient species that adapts to
different types of habitats [
79
] and is listed as a species of Least Concern according to
IUCN criteria [
27
]. Studies have shown that in some geographic areas, Black Vultures are
constantly threatened by high levels of lead contamination and conflicts over wildlife that
could be detrimental to their populations [
20
,
80
,
81
]. Species conventionally considered at
low risk of extinction and marginalized from conservation plans can reach high ED values,
so traditional prioritization systems could be masking their real importance [
44
]. In this
sense, we highlight the importance of increasing efforts for the conservation of the Black
Vulture, since its extinction would represent the loss of a significant amount of unique
evolutionary history (~12 Ma), corresponding to 19% of the total phylogenetic diversity of
the family.
Due to anthropogenic threats such as habitat degradation, poisoning with pesticides,
lead intoxication, illegal capture, free-ranging dogs and shooting [
21
,
82
–
84
], Andean
Condors and California Condors, listed as Vulnerable and Critically Endangered [
23
],
respectively, have suffered considerable population declines and geographic range contrac-
tions [
85
–
88
]. Furthermore, it is also expected that climate change will cause Black Vultures
to move to higher altitudes and this will consequently increase overlap and competition
with Andean Condors [
89
]. In this scenario, the risk of extinction of the Andean Condor

Animals 2023,13, 3175 9 of 13
would increase, since its populations are competitively excluded by Black Vultures [
90
,
91
].
It is fundamental to develop conservation strategies focused on Andean Condors and Cali-
fornia Condors, as well as on Black Vultures [
84
,
92
]. The protection of these three species
could allow the preservation of unique phenotypic and ecological traits that may lead to
more stable biological systems [
93
,
94
]. If adequate management actions are not taken, the
ecological, economic and evolutionary impact generated by the reduction in the geographic
range and the subsequent extinction of scavengers will be critical [
34
,
42
,
95
,
96
]. In order to
reduce anthropogenic threats on New World Vultures and their direct consequences, the
selection of strategic areas for conservation, an approach that has also been suggested for
groups of scavengers in the Old World (see [97]), becomes essential.
We emphasize the Amazon basin as a key area for the protection of ~70% of the
phylogenetic diversity of New World Vultures (Figure 3B). The Amazon basin is one of the
main sources of biodiversity, mainly due to the major speciation events that have taken
place since the Cenozoic, giving rise to several Neotropical lineages [
98
]. Several areas of
the Amazon region have been highlighted as priorities for the conservation of evolutionary
history because they host high levels of phylogenetic diversity of different taxonomic
groups such as lizards, snakes, turtles and plants [
99
–
101
]. Faced with the global crisis of
biodiversity loss, identifying phylogenetic diversity hotspots, as a result of the integration
of spatial data and evolutionary analysis, is an ideal proxy for the conservation of genetic
diversity, an aspect that has become crucial for international cooperation initiatives such as
the Aichi Biodiversity Targets established by The Convention on Biological Diversity (CBD)
and the UN Sustainable Development Goals (SDGs).
5. Conclusions
In this study, we underscore the critical significance of harnessing available resources
to employ a diverse array of analytical phylogenetic methods. These approaches serve
as powerful tools not only for bridging information gaps but also for advancing our
understanding not just of the evolutionary trajectories of organisms but also of their
conservation and management strategies. It is essential, however, to acknowledge and
address certain inherent limitations within this study. One such limitation stems from
the use of a phylogeny constructed based on a restricted set of genes. Additionally, the
exclusion of closely related extinct taxa from our phylogeny is, regrettably, a consequence
of the limited availability of suitable information. These limitations, namely the reliance
on a gene-limited phylogeny and the omission of extinct taxa due to data constraints,
inevitably constrain the resolution of our analytical approaches and, consequently, the
depth of our inferences.
In conclusion, our research not only highlights the invaluable role of comprehensive
phylogenetic investigations but also underscores the need for continued efforts to address
these limitations. For groups of species that have received minimal scientific attention,
we advocate for dedicated research endeavors aimed at reconstructing dated molecular
phylogenies that encompass all relevant species. By doing so, we can potentially illuminate
previously uncharted facets of their biology, offering invaluable insights derived from a
more comprehensive understanding of their evolutionary relationships.
Author Contributions:
Conceptualization, D.C.-D. and D.L.B.-T.; Formal analysis, D.C.-D. and
D.L.B.-T.; Methodology, D.C.-D. and D.L.B.-T.; Supervision, P.L.-L. and J.S.R.-C.; Writing—original
draft, D.C.-D. and D.L.B.-T.; Writing—review and editing, P.L.-L., J.S.R.-C. and I.E.-D. All authors
have read and agreed to the published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.

Animals 2023,13, 3175 10 of 13
Data Availability Statement:
The data on the molecular phylogeny of the New World Vultures
inferred by Johnson et al. [
12
] are publicly available at the GitHub repository (https://github.com/
FePhyFoFum/phyx, accessed on 10 October 2023).
Acknowledgments: We thank P.G.P. Ericson for his comments during the conception of the project.
Conflicts of Interest: The authors declare no conflict of interest.
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