Archaeogenomic evidence from the southwestern US points to a pre-Hispanic scarlet macaw breeding colony
Edited by James A. Brown, Northwestern University, Evanston, IL, and approved July 13, 2018 (received for review April 4, 2018)
Significance
Archaeogenomic analysis of scarlet macaw bones demonstrates that the genetic diversity of these birds acquired by people in the southwestern United States (SW) between 900 and 1200 CE was exceedingly low. Only one mitochondrial DNA haplogroup (Haplo6) is present of the five historically known haplogroups in the lowland forests of Mexico and Central America. Phylogenetic analyses indicate the ancient macaw lineage in the SW shared genetic affinities with this wild lineage. These data support the hypothesis that a translocated breeding colony of scarlet macaws belonging to only one haplogroup existed some distance north of their endemic range, and SW peoples continuously acquired these birds from this unknown location for nearly 3 centuries, as no evidence currently exists for macaw breeding in SW.
Abstract
Hundreds of scarlet macaw (Ara macao cyanoptera) skeletons have been recovered from archaeological contexts in the southwestern United States and northwestern Mexico (SW/NW). The location of these skeletons, >1,000 km outside their Neotropical endemic range, has suggested a far-reaching pre-Hispanic acquisition network. Clear evidence for scarlet macaw breeding within this network is only known from the settlement of Paquimé in NW dating between 1250 and 1450 CE. Although some scholars have speculated on the probable existence of earlier breeding centers in the SW/NW region, there has been no supporting evidence. In this study, we performed an ancient DNA analysis of scarlet macaws recovered from archaeological sites in Chaco Canyon and the contemporaneous Mimbres area of New Mexico. All samples were directly radiocarbon dated between 900 and 1200 CE. We reconstructed complete or near-complete mitochondrial genome sequences of 14 scarlet macaws from five different sites. We observed remarkably low genetic diversity in this sample, consistent with breeding of a small founder population translocated outside their natural range. Phylogeographic comparisons of our ancient DNA mitogenomes with mitochondrial sequences from macaws collected during the last 200 years from their endemic Neotropical range identified genetic affinity between the ancient macaws and a single rare haplogroup (Haplo6) observed only among wild macaws in Mexico and northern Guatemala. Our results suggest that people at an undiscovered pre-Hispanic settlement dating between 900 and 1200 CE managed a macaw breeding colony outside their endemic range and distributed these symbolically important birds through the SW.
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Archaeogenomic research is revolutionizing our understanding of the past, including the origin, structure, and movement of human populations (1–3), the processes of plant and animal domestication (4–13), our biological adaptation to novel environments (1, 14–16), and sociopolitical systems among ancient people (17). Here, we expand the use of these techniques to examine the acquisition of exotic birds in two pre-Hispanic Native American societies, specifically, the translocation of scarlet macaws from their northern endemic range in Neotropical Mexico to the southwestern United States between 900 and 1200 CE and their apparent breeding by people at intermediate locations through this ∼300-y period.
The appearance of scarlet macaws (Ara macao cyanoptera) in some parts of the southwestern United States and northwestern Mexico (SW/NW) between 900 and 1200 CE co-occurs with the emergence of larger settlements in Chaco and in the Mimbres region than was typical in the broader SW (excluding the Hohokam region; Fig. 1), increased interaction with Mesoamerica and California (18), and the emergence of more complex societies in parts of the SW (17, 19–23). The immense costs involved in procuring macaws over long geographical and social distances, along with other exogenous items and products including cacao, copper bells, marine shell/bracelets, and distinct ceramic vessels, may have both contributed to and were products of emergent sociopolitical complexity in Chaco Canyon (19, 21).
Fig. 1.
Some scholars have hypothesized that scarlet macaws were directly acquired from lowland tropical regions between 900 and 1200 CE via long-distance treks to the northern extent of their range in the Mexican Gulf Coast state of Tamaulipas, and possibly to more distant ranges in the Isthmus of Tehuantepec and Central America (24). Others have suggested that these birds passed from one community to the next from Mesoamerica to the SW/NW (e.g., refs. 25–27). Alternatively, here we test the hypothesis proposed by Crown (28), that lengthy trips were mitigated by the presence of intermediate breeding centers in the area between the northern endemic range of scarlet macaws and the SW/NW.
Such centers may have raised generations of captive macaws and maintained a stock of age-specific macaws for transport throughout the SW/NW, as occurred at the later (1250–1450 CE) settlement of Paquimé in the Mexican state of Chihuahua. Paquimé was an unusually large settlement with some characteristics (e.g., pueblos of contiguous rooms) of the SW and other attributes (e.g., ball courts) that were more typical of Mesoamerica (29, 30). Also present were macaw pens in public plazas, eggshells, and skeletal remains of >300 scarlet macaws ranging in age between nestlings and breeding age individuals. Oxygen isotopes support the conclusion that a majority of the scarlet macaws at Paquimé were bred in northern Mexico outside their endemic range (31).
The highest concentrations of scarlet macaws in the SW before the 13th century and before the construction of Paquimé have been recovered from archaeological contexts in Chaco Canyon (n = 35) in northwestern New Mexico, the Mimbres region (n > 10) of southwestern New Mexico, Wupatki in north-central Arizona (n > 22, see ref. 28), and the Hohokam region of southern Arizona (21, 23). Directly radiocarbon-dated scarlet macaw bones from Chaco Canyon and the Mimbres region indicate an increased rate of the acquisition of these birds in the SW between 900 and 1200 CE compared with sparse evidence between 200 and 900 CE in the Hohokam region (23) (Fig. 2). However, archaeological excavations have not revealed pre-Paquimé breeding centers (e.g., egg shells, possible nesting boxes, nestlings and breeding age birds all recovered from the same settlement) in the SW/NW. At both Pueblo Bonito in Chaco Canyon and Wupatki, for example, which have relatively large numbers of scarlet macaws, analysis revealed only one bird at each site that was possibly of breeding age. We should emphasize, however, that the intensity of archaeological research has been more limited in northern Mexico compared with adjacent areas of the SW and central Mexico. Archaeologists thus have generally assumed that during this period, wild scarlet macaws were acquired directly or passed from community to community from their endemic range to the SW/NW.
Fig. 2.
The presence of scarlet macaw skeletons at archaeological sites in Mesoamerica and the SW/NW is not surprising. The significance of macaws as metaphorical markers of human social identities is widespread among living and historic Amerindians of the tropics, perhaps most famously the Amazonian Bororo (e.g., refs. 32 and 33), and in some other parts of the New World. In the Late Preclassic period (400 BCE–200 CE) in southern Mesoamerica, depictions of high-status individuals adorned with scarlet macaw feathers suggest they were markers of prestige (34). Imagery of macaws and macaw feathers on carved stone monuments, painted murals, and polychrome pottery showing, for example, macaws resting on elite headdresses continued into the Classic period (250–900 CE) among the Maya and suggests the importance of scarlet macaws in cosmology and religion (34).
Among historic Pueblo groups in the SW, European explorers in the 16th century and later ethnographers commented on the significance of scarlet macaws and their feathers in Pueblo society (e.g., refs. 21 and 28). The long-term presence of a high-status Parrot/Macaw clan among the Hopi, the prominent role of macaws and their eggs in mythology and ritual representations at Acoma and Isleta pueblos (e.g., ref. 35), and the continuing, widespread use of macaw feathers in ritual dress in contemporary Pueblo ceremonies demonstrate the significance of macaws. The importance of macaw feathers also is demonstrated by contemporary efforts to supply Pueblos with bird feathers, including macaws (36). In current, historic, and likely pre-Hispanic Pueblo cosmology, color-direction symbolism is very important. Macaws are the bird equivalent to reddish Spondylus (spp.) shell and the color red, often marking the southern cardinal point, just as western bluebirds (Sialia mexicana) and turquoise mark the opposing cardinal direction (e.g., ref. 37). It is thus almost certainly no coincidence that both scarlet macaws and turquoise are unusually abundant in Chaco Canyon.
Throughout much of the SW/NW, the occurrence of scarlet macaws is both temporally and geographically discontinuous, with unusual frequencies in areas such as Chaco Canyon or Mimbres that are also characterized by other rare features (e.g., the remarkable representational images on Mimbres pottery and the unusually large great houses of Chaco). A previous study suggested that scarlet macaws served a central role in creating and maintaining the sociopolitical economic foundations of Chacoan society (21). Macaw plumes fade and lose their vivid colors quickly, and the effort required to obtain macaws is consistent with other luxury items sought after as markers of status in pre-Hispanic times (38).
To infer the geographic source of scarlet macaws and to explore the character of acquisition networks before the 13th century, we examined the mitogenomic variability and population structure of 14 scarlet macaws from five archaeological sites located in either Chaco Canyon (n = 11) or the Mimbres area (n = 3) of New Mexico (SI Appendix, Table S1 and Dataset S1). We compare our results with phylogeographic data available for wild scarlet macaws collected within the last 200 y from their endemic range in Mexico and Central America (39) to describe genetic relationships among the archaeological macaws and to investigate the geographic extent of socioeconomic interaction and possible long-distance acquisition in the SW/NW.
Archaeogenomic Analysis
We initially extracted ancient DNA from the bones of 20 scarlet macaws excavated from two sites in Chaco Canyon (n = 14 macaws), three sites in the Mimbres region (n = 5 macaws), and to add some spatial and temporal variation, one site (Arroyo Hondo; n = 1 macaw) in north central New Mexico (SI Appendix, Table S1 and Dataset S1). None of the scarlet macaws studied was associated with human burials. We prepared massively parallel sequencing libraries from each extract, but before sequencing we used a DNA capture approach (40) to enrich our libraries for scarlet macaw mitochondrial DNA fragments, using biotinylated RNA baits complementary to the reference scarlet macaw mitochondrial genome sequence (GenBank accession: CM002021.1; ref. 41). Postcapture libraries were then sequenced using the Illumina HiSeq 2500 and Illumina NextSeq 500 platforms (SI Appendix, Table S2). Three of the 20 samples yielded no recoverable endogenous DNA.
For 17 of the 20 ancient macaws included in this study, we recovered 133–32,607 nonredundant sequence reads that mapped to the reference scarlet macaw mitochondrial genome from South America (A. m. macao; GenBank accession: CM002021.1; ref. 41). We were able to reconstruct complete or nearly complete mitogenome sequences from 14 of these individuals. After masking nucleotides at the end of reads subject to ancient DNA damage, we assembled consensus sequences using a minimum of 2× nonredundant reads covering each nucleotide position and 80% site identity (91–99.94% of the reference mitogenome represented: sevenfold to 218-fold average sequence coverage per nucleotide). The observed misincorporation pattern for each sample was consistent with that expected from ancient DNA damage (refs. 42 and 43 and SI Appendix, Fig. S1), serving as a strong marker of authenticity. The three remaining mitogenomes were considerably less complete and were only included in subsequent analyses to ascertain whether the partial mitogenomes are assignable to a reference haplogroup (9.15–65% of the reference mitogenome; see SI Appendix). All 14 samples with complete or near-complete mitogenomes were directly radiocarbon dated to between 900 and 1200 CE (Fig. 2, SI Appendix, Table S1, and Dataset S2).
All the complete and nearly complete mitogenome sequences belonged to haplogroup 6 (Haplo6) and were assigned by comparing 23 unique modern A. m. cyanoptera reference haplotypes consisting of multiple mtDNA gene segments from Schmidt (39) (SI Appendix, Fig. S3; base pairs analyzed = 3,128 from the 12S, 16S, COI, cytb, control region). Samples collected from wild scarlet macaws in Mexico and Central America clustered within the evolutionarily distinct cyanoptera lineage consisting of five haplogroups (Haplo1, Haplo2, Haplo3, Haplo5, Haplo6; Dataset S3). Ranging further south in Costa Rica, Panama, and South America, the A. m. macao lineage consists of two haplogroups (Haplo4 and Haplo7; see refs. 39 and 44). We did not include A. m. macao haplotypes in the majority of our analyses, given evidence of geographic isolation between lineages in lower Central America. However, the complete mitogenome reference sample used here from an exemplar of A. m. macao originating from South America is Haplo4 (39). There are currently no published modern or historically collected A. m. cyanoptera complete mitogenomes available.
The nucleotide sequences of our 14 complete or near-complete ancient macaw mitogenomes are remarkably similar to each other and belong to four separate haplotypes (Haplo6a1, Haplo6a2, Haplo6a3, Haplo6a4). The primary haplotype (Haplo6a1) includes 10 of the 14 individuals, and each sequence is identical across all base pairs, whereas the remaining four mitogenomes differ from the primary haplotype and each other at only two to five nucleotides across 15,584 and 16,982 positions (99.9–100% similarity; Fig. 3A). In contrast, the ancient mitogenome haplotypes differ from the South American reference scarlet macaw mitogenome at 102–105 positions (98.8% similarity). The 10 Haplo6a1 sequences were recovered across four archaeological sites — Pueblo Bonito (n = 6), Pueblo del Arroyo (n = 2), the Mitchell Site (n = 1), and the Wind Mountain site (n = 1) — and they represent the entire time span of our sample based on the radiocarbon dates, including the earliest and latest dated individuals and multiple other individuals within the ∼300-y span (Fig. 3B and SI Appendix, Table S2). Haplo6a2 (n = 1) and Haplo6a3 (n = 2) were only recovered at Pueblo Bonito after 1045 CE, and Haplo6a4 (n = 1) was found only in the Mimbres area at Old Town 1020 CE.
Fig. 3.
We separately aligned the three additional specimens (PB74 and PB80A from Chaco Canyon, and BA660 from Arroyo Hondo) with partial mitogenomes to the 14 complete or near-complete sequences to determine the degree of haplotype similarity among these samples (SI Appendix, Fig. S2). Although the two partial sequences from Pueblo Bonito (PB74 and PB80A) were 100% identical to Haplo6a1 across 3,580 and 11,006 alignable positions, only three of the five positions used to distinguish the ancient haplotypes were present in PB80A, and only one of the five positions was present in PB74. None of these positions was present in the BA660 sequence found at Arroyo Hondo across 1,523 alignable positions. We then aligned 16 ancient macaws (14 complete or near-complete and two partial mitogenomes) to the 23 unique modern A. m. cyanoptera reference haplotypes. We found that two of the three partial mitogenomes cluster within the Haplo6 clade across all alignable reference mtDNA gene segments (base pairs analyzed = 3,128; SI Appendix, Fig. S3 and Table S2). Although coverage was too low to accurately define the ancient haplotype, the two partial mitogenome sequences from Pueblo Bonito share identical segments across conserved genes used to identify the A. m. cyanoptera lineage and known variable positions used to define Haplo6. These data indicate that these two partial mitogenomes share a high degree of genetic similarity with our 14 complete or nearly complete ancient scarlet macaw mitogenomes.
There has been one previously published ancient DNA study of scarlet macaws from three archaeological sites in the SW (45). In that study, sequence data from a 396-bp fragment of the mitochondrial genome (12s gene) of four scarlet macaws were reconstructed using PCR-based ancient DNA amplification and Sanger sequencing methods (45). We aligned each of these sequences and modern references to our 14 complete or near-complete mitogenomes (SI Appendix, Table S4 and Dataset S4). The 12s gene mtDNA sequences of two ancient macaws (Grasshopper Ruin 2 in Arizona and Cameron Creek in the Mimbres region) are identical to those from our study across all alignable positions. One of the previously studied ancient macaws (Grasshopper Ruin 1 in Arizona) differs by a single nucleotide from our sequences, and the fourth macaw (Salmon Ruins, a site related to those in Chaco Canyon) has differences at four positions (SI Appendix, Fig. S5A). Importantly, all but one of these differences could potentially be explained by unmasked C to T or G to A mismatches attributed to ancient DNA damage (SI Appendix, Fig. S5B). After masking for potential DNA degradation, three of the four ancient macaws from the previous study cluster within a region of the 12s gene consistent with Haplo6. However, Haplo3 cannot be ruled out when examining the 12s region alone.
After assigning the ancient scarlet macaws to the cyanoptera lineage, we next investigated the potential source populations by comparing the 14 complete or near-complete ancient mitogenomes alongside previously published sequence data from the mitochondrial control region (885 bp) of 84 modern A. m. cyanoptera samples collected from across its distribution in Mexico and upper Central America; Fig. 4 and Dataset S4). Among the 98 total (n = 14 ancient; n = 84 modern) macaw control region sequences, there were 24 unique haplotypes. A previous study of scarlet macaw genetic diversity and population substructure recovered two populations within the cyanoptera lineage (39). The northern population extends across Mexico, Guatemala, and Belize (Haplo1, Haplo2, Haplo5, and Haplo6; Fig. 4A), whereas the southern population is found in Honduras, Nicaragua, El Salvador, and northern Costa Rica (Haplo2, Haplo3, Haplo5). The 14 ancient macaws with complete mitochondrial control regions group together in Haplo6 with three exemplars from the northern population: Isthmus of Tehuantepec in Mexico (n = 2) and northern Guatemala (n = 1; see SI Appendix, Fig. S4 for network analysis).
Fig. 4.
To estimate the probability that the complete or nearly complete mitochondrial coverages of the 14 macaws could have been independently captured from the wild and individually transported directly to the SW/NW, we performed a permutation analysis with the modern/historic wild macaw haplogroup data. Specifically, we considered the wild scarlet macaw haplogroups from the Gulf coast region of the Isthmus of Tehuantepec, Mexico, the closest region to the SW/NW in our current dataset with Haplo6 wild macaws (Fig. 4B). We then drew with replacement an artificial sample of 14 individual sequences from three wild macaw haplogroups in this region known during the last 200 y and recorded how many times an individual with Haplo6 was in the artificial sample. We repeated this artificial sampling 10,000 times and then compared the frequency distribution of the number of individuals with Haplo6 per permutation to the observed result for the ancient macaws (in which all 14 individuals have Haplo6) as an empirical P value. Of 10,000 permutations, there was a maximum of 11 individuals with Haplo6 (mean = 4.67; SD = 1.75; P < 0.001; Fig. 4C), indicating very low probability that the archaeological macaws could represent a population sample drawn randomly from the tested wild location. We repeated this permutation analysis using various modern/historic sampling regions, always obtaining equivalent results (SI Appendix, Fig. S6 and Table S5).
Discussion and Conclusions
Archaeogenomic analyses of scarlet macaws were used to help resolve long-standing questions regarding the origins and acquisition of these exotic birds at SW archaeological sites. The early 900–1200 CE presence of these macaws, far outside of their endemic Neotropical range, along with studies demonstrating the exchange of cacao, marine shell, and copper bells (20, 22, 46–48) over similar periods, indicate significant and long-standing interactions between Mesoamerican societies and the native peoples of the SW/NW.
Wild scarlet macaws have occurred historically over vast portions of the lowland Neotropics of Mexico, Central America, and South America. Archaeologists working in the SW/NW have previously hypothesized that the birds in archaeological sites originated in the northernmost extent of this range, along the Gulf Coast of Mexico (21). Our archaeogenomic results indicate that the original breeding stock came from this general region. Specifically, only a single mitochondrial haplogroup, Haplo6, was identified among our archaeological samples from Chaco Canyon and the Mimbres region. Meanwhile, Haplo6 was observed in only three of 84 modern macaws (39): two individuals from the Gulf Coast/Isthmus of Tehuantepec region and a third individual from northern Guatemala. Haplo6 co-occurs with other haplogroups in both these areas.
We currently do not have comparative wild scarlet macaw samples from the very northernmost extent of their range in northern Veracruz/southern Tamaulipas. However, given the species behavior, it is highly unlikely that northern Veracruz/southern Tamaulipas represents an isolated subpopulation with a disproportionately high abundance of Haplo6. Scarlet macaws, similar to other large parrots, exhibit a high capacity for dispersal, with known long-distance seasonal migrations. Although exact distances traveled by individual macaws are not well understood because of the logistical challenges of radio/satellite telemetry, documented changes in relative abundances suggest movements up to several hundred kilometers (49, 50).
It is also important to note that Haplo6 occurs at a low frequency within the modern dataset — three of 84 cyanoptera samples cluster within Haplo6 — whereas all ancient scarlet macaws cluster within this haplogroup. Our permutation analysis suggests that the low diversity observed in the ancient SW macaw sample was unlikely to represent a random sampling of individual wild macaws. Moreover, 71% of the SW macaws shared the exact same mitogenome sequence, increasing the likelihood these ancient macaws share a matrilineal pedigree. These observations are inconsistent with models proposing direct acquisition or the passing of individual macaws from community to community from multiple distant source areas in Mexico and Central America (27). The logistical challenges of transporting scarlet macaws (eggs, chicks, juveniles, or adults) also lends support to the need of human-mediated propagation of this animal population.
All the SW scarlet macaws we sequenced predate the well-attested scarlet macaw breeding activities evident at Paquimé, which was an important socioeconomic center from 1250 to 1450 CE in northern Mexico (29–31, 51). We argue that the low haplotypic diversity shown here resulted from a pre-Hispanic captive breeding program of a small founder population, with fledglings and immature birds being transported to other communities in the SW/NW throughout a period perhaps as long as 300 y. The radiocarbon results from the SW scarlet macaws predate the breeding activities at Paquimé, thus suggesting the existence of a previously unobserved captive breeding population being managed between 900 and 1200 CE that served as the source for macaws in Chaco Canyon and the Mimbres region. Our results are consistent with the hypothesis proposed by Crown (28), that lengthy trips were mitigated by the presence of intermediate breeding centers in the area between the northern endemic range of scarlet macaws and the SW/NW. The location of this hypothesized early breeding colony is unknown, although additional research in the SW/NW may uncover the archaeological remains of this site.
Methods
Details for all ancient scarlet macaw radiocarbon dating and genomic methods used in this study are provided in SI Appendix. Ancient scarlet macaw samples from Chaco Canyon were accessed through a submitted research proposal to the Smithsonian Institution for accelerator mass spectrometer (AMS) 14C radiocarbon dating and ancient mitogenomic DNA analysis (SI Appendix, Table S1). Additional scarlet macaw samples from the Mimbres area at the Mitchell, Old Town, and Wind Mountain sites and the Arroyo Hondo macaw were sampled from existing collections. Schmidt (39) provided genetic data from wild and historic scarlet macaw (A. m. cyanoptera) specimens. Detailed information about ancient and reference macaw sequences are provided in SI Appendix and Datasets S1–S4.
Mitochondrial DNA from 20 ancient macaw samples were extracted and processed in the ancient DNA facility at Pennsylvania State University (SI Appendix, Table S2). Detailed information about laboratory procedures, sequencing, and bioinformatics are provided in the SI Appendix. In a dedicated clean facility, DNA extraction of bone samples followed a modified version of ref. 52 and/or ref. 53 (detailed in SI Appendix). Double-stranded DNA libraries were constructed from DNA extracts following a published protocol (54), and were then enriched for mitochondrial DNA fragments by bead capture in-solution biotinylated RNA bait hybridization (40), using the Mycroarray MyBaits system (probe design: 140429 and 150610). Postcapture libraries were sequenced at the Clinical Microarray Core, University of California, Los Angeles. All computational methods and damage profiles are detailed in the SI Appendix, Fig. S1 and Dataset S2. Sequencing data are available from the National Center for Biotechnology Information’s Sequence Read Archive (BioProject ID: PRJNA477839), merged DNA assemblies are available from Dryad Digital Repository at https://doi.org/10.5061/dryad.sv74pj2, and mitogenome consensus sequences are available from GenBank (accession nos. MH400234–MH400248; Dataset S2).
Data Availability
Data deposition: The sequences reported in this paper have been deposited in the NCBI Sequence Read Archive (BioProject ID: PRJNA477839), Dryad Digital Repository (https://doi.org/10.5061/dryad.sv74pj2), and GenBank database (accession nos. MH400234–MH400248).
Acknowledgments
We thank the Smithsonian Institution Department of Anthropology for granting us permission to sample scarlet macaws from Pueblo Bonito and Pueblo del Arroyo, and we are grateful for the assistance of Torben Rick and Esther Rimer. Thomas Holcomb of the Bureau of Land Management in Las Cruces gave permission to sample the Old Town macaws. Darrell Creel provided those samples, and Michael Cannon sent the Mitchell site sample. Christine Szuter and Eric Kaldahl at the Amerind Foundation provided the Wind Mountain sample. Many thanks to George Perry for his important contributions in designing and writing up this work. Patricia Crown, Dick Drennan, John Kantner, and Joyce Marcus, and two anonymous reviewers provided valuable feedback on the manuscript. We also thank members of the Human Paleoecology & Isotope Geochemistry Lab for their assistance processing AMS 14C radiocarbon samples: Laurie Eccles, Margaret Davis, Lindsay Simmins, and Matthew Veres. AMS 14C radiocarbon dates from this project were analyzed at the Penn State AMS 14C facility and the W. M. Keck Carbon Cycle Accelerator Mass Spectrometry Laboratory. We acknowledge and thank Ximin Li and Janice Yoshizawa at the University of California, Los Angeles, Clinical Microarray. Data from this project were processed using the high-performance computing infrastructure at the Pennsylvania State University Institute for Cyber Science Advanced Cyber Infrastructure. This project was supported through grants from the National Science Foundation (Archaeometry Program, BCS-1460367), research support from the Dean of Arts & Sciences, University of Virginia, and the Pennsylvania State University.
Supporting Information
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References
1
R Nielsen, et al., Tracing the peopling of the world through genomics. Nature 541, 302–310 (2017).
2
JV Moreno-Mayar, et al., Terminal Pleistocene Alaskan genome reveals first founding population of Native Americans. Nature 553, 203–207 (2018).
3
P Skoglund, et al., Reconstructing prehistoric African population structure. Cell 171, 59–71.e21 (2017).
4
K Swarts, et al., Genomic estimation of complex traits reveals ancient maize adaptation to temperate North America. Science 357, 512–515 (2017).
5
CF Speller, et al., Ancient mitochondrial DNA analysis reveals complexity of indigenous North American Turkey domestication. Proc Natl Acad Sci USA 107, 2807–2812 (2010).
6
FB Marshall, K Dobney, T Denham, JM Capriles, Evaluating the roles of directed breeding and gene flow in animal domestication. Proc Natl Acad Sci USA 111, 6153–6158 (2014).
7
G Larson, et al., Current perspectives and the future of domestication studies. Proc Natl Acad Sci USA 111, 6139–6146 (2014).
8
A Manin, et al., Diversity of management strategies in Mesoamerican turkeys: Archaeological, isotopic and genetic evidence. R Soc Open Sci 5, 171613 (2018).
9
L Kistler, et al., Gourds and squashes (Cucurbita spp.) adapted to megafaunal extinction and ecological anachronism through domestication. Proc Natl Acad Sci USA 112, 15107–15112 (2015).
10
P Librado, et al., Ancient genomic changes associated with domestication of the horse. Science 356, 442–445 (2017).
11
RR da Fonseca, et al., The origin and evolution of maize in the Southwestern United States. Nat Plants 1, 14003 (2015).
12
J Ramos-Madrigal, et al., Genome sequence of a 5,310-year-old maize cob provides insights into the early stages of maize domestication. Curr Biol 26, 3195–3201 (2016).
13
G Larson, et al., Patterns of East Asian pig domestication, migration, and turnover revealed by modern and ancient DNA. Proc Natl Acad Sci USA 107, 7686–7691 (2010).
14
S Marciniak, GH Perry, Harnessing ancient genomes to study the history of human adaptation. Nat Rev Genet 18, 659–674 (2017).
15
L Fehren-Schmitz, L Georges, Ancient DNA reveals selection acting on genes associated with hypoxia response in pre-Columbian Peruvian highlanders in the last 8500 years. Sci Rep 6, 23485 (2016).
16
C Jeong, et al., Long-term genetic stability and a high-altitude East Asian origin for the peoples of the high valleys of the Himalayan arc. Proc Natl Acad Sci USA 113, 7485–7490 (2016).
17
DJ Kennett, et al., Archaeogenomic evidence reveals prehistoric matrilineal dynasty. Nat Commun 8, 14115 (2017).
18
DJ Kennett The Island Chumash: Behavioral Ecology of a Maritime Society (Univ California Press, Berkeley, CA, 2005).
19
S Plog, C Heitman, Hierarchy and social inequality in the American Southwest, A.D. 800-1200. Proc Natl Acad Sci USA 107, 19619–19626 (2010).
20
PL Crown, WJ Hurst, Evidence of cacao use in the prehispanic American Southwest. Proc Natl Acad Sci USA 106, 2110–2113 (2009).
21
AS Watson, et al., Early procurement of scarlet macaws and the emergence of social complexity in Chaco Canyon, NM. Proc Natl Acad Sci USA 112, 8238–8243 (2015).
22
EM Smith, M Fauvelle, Regional interactions between California and the Southwest: The Western Edge of the North American Continental system. Am Anthropol 117, 710–721 (2015).
23
CR McKusick, Southwest Birds of Sacrifice (WorldCat lists, Tucson, AZ), No. 31. (2001).
24
PA Gilman, M Thompson, KC Wyckoff, Ritual change and the distant: Mesoamerican iconography, scarlet macaws, and great kivas in the Mimbres region of Southwestern New Mexico. Am Antiq 79, 90–107 (2014).
25
HW Toll, Material distributions and exchange in the Chaco system. Chaco and Hohokam: Prehistoric Regional Systems in the American Southwest, eds PL Crown, WJ Judge (School of Am Res, Santa Fe, NM), pp. 77–107 (1991).
26
FJ Mathien Culture and Ecology of Chaco Canyon and the San Juan Basin (Natl Park Service, Santa Fe, NM, 2005).
27
D Creel, C McKusick, Prehistoric macaws and parrots in the Mimbres area, New Mexico. Am Antiq 59, 510–524 (1994).
28
PL Crown, Just macaws: A review for the US Southwest/Mexican Northwest. KIVA 82, 331–363 (2016).
29
CC Di Peso Casas Grandes: A Fallen Trading Center of the Gran Chichimeca (Amerind Foundation, Dragoon, AZ) Vol 1–3 (1974).
30
ME Whalen, PE Minnis, The Casas Grandes regional system: A late prehistoric polity of northwestern Mexico. J World Prehist 15, 313–364 (2001).
31
AD Somerville, BA Nelson, KJ Knudson, Isotopic investigation of pre-hispanic macaw breeding in Northwest Mexico. J Anthropol Archaeol 29, 125–135 (2010).
32
C Lévi-Strauss, The Raw and the Cooked: Introduction to a Science of Mythology, trans Weightman J, Weightman D (Harper and Row, New York), Vol 1. (1969).
33
JC Crocker, My brother the parrot. The Social Use of Metaphor, eds DJ Sapir, JC Crocker (Univ of Pennsylvania Press, Philadelphia), pp. 164–192 (1977).
34
J Guernsey Ritual and Power in Stone: The Political and Cosmological Significance of Late Preclassic Izapan-Style Monuments (Univ Texas Press, Austin, TX, 2006).
35
HA Tyler, Pueblo Birds and Myths (Northland, Flagstaff, AZ), 1979. (1991).
36
JE Reyman, Feathers and ceremonialism in the American southwest, past and present. J West 47, 16–22 (2008).
37
PM Whiteley, Turquoise and squash blossom. Turquoise in Mexico and North America, eds JCH King, M Carocci, C Cartwright, C McEwan, R Stacey (Archetype/British Museum, London), pp. 145–154 (2012).
38
S Houston, C Brittenham, C Mesick, A Tokovinine, CG Warinner Veiled Brightness: A History of Ancient Maya Color (Univ Texas Press, Austin, TX, 2009).
39
K Schmidt, Spatial and temporal patterns of genetic variation in scarlet macaws (Ara macao): Implications for population management in La Selva Maya, Central America PhD dissertation (Proquest Dissertations Publishing, Columbia University, New York). (2013).
40
A Gnirke, et al., Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing. Nat Biotechnol 27, 182–189 (2009).
41
CM Seabury, et al., A multi-platform draft de novo genome assembly and comparative analysis for the scarlet macaw (Ara macao). PLoS One 8, e62415 (2013).
42
AW Briggs, et al., Patterns of damage in genomic DNA sequences from a Neandertal. Proc Natl Acad Sci USA 104, 14616–14621 (2007).
43
S Sawyer, J Krause, K Guschanski, V Savolainen, S Pääbo, Temporal patterns of nucleotide misincorporations and DNA fragmentation in ancient DNA. PLoS One 7, e34131 (2012).
44
DA Wiedenfeld, A new subspecies of scarlet macaw and its status and conservation [Una nueva subespecie de la lapa roja y su estado de conservación]. Ornitol Neotrop 5, 99–104 (1994).
45
PY Bullock, A Cooper, Ancient DNA and macaw identification in the American Southwest: A progress report. Artifact 40, 1–10 (2002).
46
AW Vokes, DA Gregory, Exchange networks for exotic goods in the Southwest and Zuni’s place in them. Zuni Origins: Toward a New Synthesis of Southwestern Archaeology, eds DA Gregory, DR Wilcox (Univ Arizona Press, Tucson, AZ), pp. 318–357 (2007).
47
J Neitzel, The Chacoan regional system: Interpreting the evidence for sociopolitical complexity. The Sociopolitical Structure of Prehistoric Southwestern Societies, eds S Upham, K Lightfoot, R Jewett (Westview, Boulder, CO), pp. 509–556 (1989).
48
VD Vargas, Copper Bell Trade Patterns in the Prehispanic US Southwest and Northwest Mexico (Arizona State Museum, Univ Arizona, Tucson, AZ), No. 187. (1995).
49
K Renton, Seasonal variation in occurrence of macaws along a rainforest river. J Field Ornithol 73, 15–19 (2002).
50
J Karubian, et al., Temporal and spatial patterns of macaw abundance in the Ecuadorian Amazon. Condor 107, 617–626 (2005).
51
AY Morales‐Arce, MH Snow, JH Kelley, M Anne Katzenberg, Ancient mitochondrial DNA and ancestry of Paquimé inhabitants, Casas Grandes (AD 1200–1450). Am J Phys Anthropol 163, 616–626 (2017).
52
N Rohland, DNA extraction of ancient animal hard tissue samples via adsorption to silica particles. Methods Mol Biol 840, 21–28 (2012).
53
J Dabney, et al., Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc Natl Acad Sci USA 110, 15758–15763 (2013).
54
M Meyer, M Kircher, Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb Protoc 2010, pdb.prot5448 (2010).
55
R Bouckaert, et al., BEAST 2: A software platform for Bayesian evolutionary analysis. PLOS Comput Biol 10, e1003537 (2014).
Information & Authors
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© 2018. Published under the PNAS license.
Data Availability
Data deposition: The sequences reported in this paper have been deposited in the NCBI Sequence Read Archive (BioProject ID: PRJNA477839), Dryad Digital Repository (https://doi.org/10.5061/dryad.sv74pj2), and GenBank database (accession nos. MH400234–MH400248).
Submission history
Published online: August 13, 2018
Published in issue: August 28, 2018
Keywords
Acknowledgments
We thank the Smithsonian Institution Department of Anthropology for granting us permission to sample scarlet macaws from Pueblo Bonito and Pueblo del Arroyo, and we are grateful for the assistance of Torben Rick and Esther Rimer. Thomas Holcomb of the Bureau of Land Management in Las Cruces gave permission to sample the Old Town macaws. Darrell Creel provided those samples, and Michael Cannon sent the Mitchell site sample. Christine Szuter and Eric Kaldahl at the Amerind Foundation provided the Wind Mountain sample. Many thanks to George Perry for his important contributions in designing and writing up this work. Patricia Crown, Dick Drennan, John Kantner, and Joyce Marcus, and two anonymous reviewers provided valuable feedback on the manuscript. We also thank members of the Human Paleoecology & Isotope Geochemistry Lab for their assistance processing AMS 14C radiocarbon samples: Laurie Eccles, Margaret Davis, Lindsay Simmins, and Matthew Veres. AMS 14C radiocarbon dates from this project were analyzed at the Penn State AMS 14C facility and the W. M. Keck Carbon Cycle Accelerator Mass Spectrometry Laboratory. We acknowledge and thank Ximin Li and Janice Yoshizawa at the University of California, Los Angeles, Clinical Microarray. Data from this project were processed using the high-performance computing infrastructure at the Pennsylvania State University Institute for Cyber Science Advanced Cyber Infrastructure. This project was supported through grants from the National Science Foundation (Archaeometry Program, BCS-1460367), research support from the Dean of Arts & Sciences, University of Virginia, and the Pennsylvania State University.
Notes
This article is a PNAS Direct Submission.
Authors
Competing Interests
The authors declare no conflict of interest.
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