Eastern North America As an Independent Center of Plant Domestication

PERSPECTIVE

Eastern North America as an independent center of plant domestication

Bruce D. Smith* Archaeobiology Program, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560

Edited by Joyce Marcus, University of Michigan, Ann Arbor, MI, June 30, 2006 (received for review June 21, 2006)

The status of eastern North America as an independent center of plant domestication has recently been called into question by a number of genetic and archaeological studies, which suggest that the region may not have witnessed the independent domestication of local crop plants, but rather may have been on the receiving end of domesticated crop plants introduced from Mexico. Here, I provide a synthesis of the currently available archaeological and genetic evidence from both eastern North America and Mexico regarding the spatial and temporal context of initial domestication of the four plant species identified as potential eastern North American domesticates: marshelder (Iva annua), chenopod (Chenopodium berlandieri), squash (Cucurbita pepo), and sunflower (Heli- anthus annuus). Genetic and archaeological evidence provides strong support for the independent domestication of all four of these plant species in the eastern United States and reconfirms the region as one of the world’s independent centers of domestication.

etween approximately 11,000 Here, I reconsider eastern North by human groups for several thousand and 5,000 years ago, human so- America’s status as an independent cen- years leading up to its initial domesti- cieties in many different regions ter of plant domestication and provide a cation (8). of the world brought a wide new synthesis of the currently available The earliest evidence for domesti- B archaeological and genetic evidence cated marshelder in the eastern United range of different species of plants and animals under domestication, marking from both eastern North America and States comes from a shallow Tittering- the initial emergence of food production Mexico regarding the spatial and tempo- ton Phase pit (Feature 20) at the economies and the beginning of one of ral context of initial domestication of Napoleon Hollow site in west-central the major transitions in human history. the four plant species identified as po- Illinois, which yielded an assemblage of This transition, often described as the tential eastern North American domesti- 79 carbonized marshelder achenes and ‘‘Neolithic Revolution’’ or the ‘‘Origins cates: marshelder (Iva annua), chenopod seeds, including 44 that were complete of Agriculture’’ has been an enduring (Chenopodium berlandieri), squash (Cu- enough to be measured (Fig. 2) (15). area of inquiry in both archaeology and curbita pepo), and sunflower (Helianthus When achene measurements were ad- biology for more than a century. By annuus). Genetic and archaeological justed to correct for shrinkage due to 1940, Nikolai Vavilov had identified a evidence summarized here provides carbonization, this Napoleon Hollow total of seven primary centers of plant strong support for the independent assemblage of 44 I. annua specimens domestication, worldwide, based on ar- domestication of all four of these plant exhibited a 31% increase in mean eas of maximum genetic diversity in species in the eastern United States length when compared with a refer- crop plants (1). Vavilov’s seven centers and reconfirms the region as one of ence class of 11 modern wild I. annua of origin have been subjected to consid- the world’s independent centers of populations, providing clear evidence erable rethinking as a constant stream domestication. that they represent domesticated plants. An indirect date obtained on of genetic and archaeological studies, Marshelder (Iva annua) fueled by new approaches and techno- dispersed charcoal within Feature 20 Although marshelder is mentioned only Ϯ logical advances, have substantially ex- indicated an age of 3,920 90 B.P. in briefly in passing (9) or described as panded and refined our understanding radiocarbon years B.P., consistent with an ‘‘extinct minor cultigen’’ (14) in sev- of the spatial and temporal contexts of the age of the Titterington cultural eral recent studies suggesting that do- initial plant and animal domestication phase as documented elsewhere in Illi- mesticates first entered eastern North nois (15). A recent direct accelerator (2–4). In just the last 5–10 years, several America from Mexico, this crop plant new independent centers of plant do- mass spectrometry (AMS) radiocarbon in fact plays an important role in es- date obtained on one of the marsh- mestication have been identified in trop- tablishing whether the eastern wood- elder achenes yielded the identical age ical forest regions of South America and lands was an independent center of in radiocarbon years (3,920 Ϯ 40 B.P.) Southeast Asia (5–7) (Fig. 1). At the plant domestication. No longer culti- (Table 1), providing confirmation that same time that these Southeast Asian vated as a domesticated crop, I. annua had been brought under do- and South American centers have been marshelder grows today as a wild plant mestication in the eastern United recognized, however, the status of an- across much of the eastern and central States by ca. 4,400 B.P. The presence other, previously identified independent United States, and its range extends in eastern North America, by 4,400 center of plant domestication has been south into Tamaulipas, Mexico. No B.P., of an indigenous domesticated called into question. A number of recent remains of marshelder, however, have genetic and archaeological studies have ever been reported from archaeological led to suggestions that eastern North contexts in Mexico. In contrast, small Conflict of interest statement: No conflicts declared. † America, identified as a center of plant achenes and seeds representing wild I. This paper was submitted directly (Track II) to the PNAS domestication 20 years ago (8), may not annua plants have been recovered in office. have witnessed the independent domes- abundance from numerous archaeolog- Abbreviation: AMS, accelerator mass spectrometry. tication of local crop plants but rather ical contexts across the eastern United *E-mail: [email protected]. may have been on the receiving end of states dating back as early as ca. 8,000 †Marshelder and sunflower fruits (achenes) consist of a domesticated crop plants introduced B.P., indicating that wild populations single seed enclosed in a dry indehiscent pericarp. from Mexico (9–14). of marshelder were widely harvested © 2006 by The National Academy of Sciences of the USA

www.pnas.org͞cgi͞doi͞10.1073͞pnas.0604335103 PNAS ͉ August 15, 2006 ͉ vol. 103 ͉ no. 33 ͉ 12223–12228 Downloaded by guest on September 30, 2021 Pepo Squash 5,000 B.P. Broomcorn Millet, Sunflower 4,800 B.P. Pepo Squash 10,000 B.P. Foxtail Millet - Marshelder 4,400 B.P. 8,000 B.P. Maize 9,000 - 7,000 B.P. Chenopod 4,000 B.P. Common Bean 4,000 B.P. Rice 8,000 B.P. Foxnut 8,000 B.P. Arrowroot 8,000 B.P. Yam (D. trifida) 6,000 B.P Emmer wheat 10,000 B.P Cotton 5,000 B.P. Einkorn wheat 10,000 B.P. Sweet potato 4,500 B.P. Barley 10,000 B.P. African rice 2,000 B.P. Pearl millet 3,000 B.P. Sorghum 4,000 B.P. Potato 7,000 B.P.? Quinoa 5,000 B.P. Peanut? Yam (D. alata) 7,000 B.P.? Manioc 8,000 B.P.? Banana 7,000 B.P. Chile Peppers 6,000 B.P. Taro 7,000 B.P.?

Fig. 1. Currently recognized independent centers of plant and animal domestication.

crop plant provides a solid temporal soamerican exotics would, of necessity, grow today in eastern North America boundary line for the arrival of any ex- have to have arrived in the eastern and as a group are referred to by a otic outside domesticates if they are to United States before 4,400 B.P. Each of variety of common names, including be cast in a causal role. If the introduc- the other three plant species identified ‘‘lambsquarter’’ and ‘‘goosefoot.’’ One tion of crop plants and associated food as indigenous eastern domesticates (che- of these species of chenopod, Ch. ber- nopod, squash, and sunflower) have in production technologies from Me- landieri, is of interest here because it is fact recently been proposed as repre- soamerica is to be identified as the senting early introductions from Mexico. both currently grown as a domesticated source and ‘‘trigger’’ for a subsequent crop plant in Mexico and was present domestication of marshelder or any Chenopod (Chenopodium berlandieri) as a pre-Columbian domesticate in other ‘‘minor indigenous crop’’ (14) of A number of different wild species eastern North America (8). Wild popu- eastern North America, then the Me- belonging to the genus Chenopodium lations of Ch. berlandieri grow today

NAPOLEON NEWT KASH HOLLOW CLOUDSPLITTER ATLANTIC PHILLIPS SPRING HAYES OCEAN var. ozarkana

var. texana

Gulf Of Mexico ssp. fraterna

OCAMPO

N SAN ANDRÉS Caribbean Sea

Fig. 2. Location of archaeological sites discussed in the text and the present-day geographical range of the three wild Cucurbita gourds identiﬁed as potential progenitors of pepo squash (Cucurbita pepo ssp. ovifera).

12224 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0604335103 Smith Downloaded by guest on September 30, 2021 Table 1. Direct AMS radiocarbon age determinations for the earliest occurrence of indigenous domesticated seed crops in eastern North America Age, AMS-calibrated calendar years B.P.

Age, radiocarbon Laboratory Archaeological site and Domesticated plant species Intercept 1␴ age range years B.P. sample no. provenience

Pepo squash (C. pepo ssp. ovifera) 5,025 5,290–4,870 4,440 Ϯ 75 ß 47293 Phillips Spring (Unit K2) Sunﬂower (H. annuus) 4,840 4,860–4,830 4,265 Ϯ 60 ß 45050 Hayes (Level 14) Marshelder (I. annua) 4,400 4,420–4,290 3,920 Ϯ 40 ß 216463 Napoleon Hollow (Feature 20) Chenopod (Ch. berlandieri) 3,700 3,900–3,490 3,450 Ϯ 150 ß 11348 Cloudsplitter (F.S. 1361 3,640 3,840–3,460 3,400 Ϯ 150 ß 11347 Newt Kash (El 1114)

Calendar calibrations are based on the Pretoria Calibration Procedure and the Intcal 98 Calibration database.

over much of the United Sates and being grown as a domesticated crop comparison of the modern Mexican do- northern Mexico, as far south as Mi- plant in the East (8). mesticate and the ancient domesticate choaca´n (16). At the southern end of The archaeological record of Mexico and modern wild populations of Ch. ber- its geographical range, three varieties also offers clear evidence of human har- landieri from eastern North American of a domesticated subspecies of this vesting of wild stands of Ch. berlandieri, would be worthwhile. I expect that when plant (Ch. berlandieri ssp. nuttalliae) along with a variety of other plants pro- such a comparison is carried out it will are still cultivated today (Fig. 2) (16), ducing similarly sized small seeds, for provide further evidence that Ch. ber- and their small indehiscent fruits can thousands of years before the arrival of landieri was initially domesticated in be distinguished from those of wild the Spanish.‡ Despite careful and com- eastern North America by 3,700 B.P., plants on the basis of a substantial re- prehensive analysis of extant collections, with a second independent domestica- duction in the thickness of their testa however, thin-testa fruits representing tion occurring in Mexico in the 16th or seed coat (8). domesticated chenopod have yet to be century, Ͼ3,000 years later. Based on observed similarities in fruit found in any archaeological contexts in Squash (Cucurbita pepo) morphology between two of the modern Mexico, leading McClung de Tapia and Mexican cultivated varieties of domesti- Rios-Fuentes‡ to recently conclude that Of the five species of squash (Cucurbita) cated Ch. berlandieri ssp. nuttalliae on Ch. berlandieri was not present as a do- that were domesticated from different the one hand (the chia variety, with a mesticated plant in Mexico before the progenitor species of wild Cucurbita 10- 20-␮m-thick testa, and the ‘‘naked’’ 16th century. Interestingly, recent re- gourds throughout the Americas (12, huauzontle variety, with a 2- to 7-␮m- search in the south-central Andes has 20), only C. pepo is known at the thick testa) and archaeological speci- documented the independent domestica- present time to have been independently mens recovered from across eastern tion of a species of Chenopodium closely domesticated more than once (12, 21, North America on the other, it was sug- related to Ch. berlandieri, based on a 22), resulting in two present-day domes- gested in 1990 that Ch. berlandieri was reduction in testa thickness, beginning ticate lineages, now classed as distinct subspecies. The first of these, C. pepo initially domesticated in Mexico and at approximately the same time that do- ssp. pepo, which includes cultivated subsequently introduced as a domesti- mesticated Ch. berlandieri first appears pumpkins and marrows, was developed cate into eastern North America (16). in the archaeological record of the from an as yet undocumented wild pro- The suggestion that domesticated cheno- eastern United States (18). This docu- genitor in Mexico 10,000 years ago (12, pod may have been initially introduced mentation of a second developmental 23, 24). The second subspecies (C. pepo into the eastern United States from sequence of domestication for the genus Chenopodium in South America under- ssp. ovifera, which includes cultivated Mexico was recently reiterated (9), even crooknecks, acorn, and scallop squashes) though archaeological research in the scores the absence of any archaeological record of domesticated Ch. berlandieri in has long been identified as a potential last 15 years has provided compelling eastern North American domesticate (8). evidence to the contrary. Mexico. A recent genetic study employing Over the past two decades, a number In eastern North America, archaeo- of genetic studies have focused on iden- random amplified polymorphic DNA logical evidence indicates that Ch. ber- tifying the wild ancestor (and location of fragment analysis to identify genetic landieri was harvested as a wild plant as domestication) of this proposed ‘‘east- relationships among six Chenopodium early as 8,500 B.P. (15) and was an im- ern’’ lineage of pepo squash. Of the taxa, including the Mexican domesticate portant domesticated crop plant in the three taxa of wild Cucurbita gourds that Ͼ Ch. berlandieri ssp. nuttalliae and a col- region for 3,500 years (from ca. 1850 have been considered as possible pro- lection of wild Ch. berlandieri from B.C. to A.D. 1750) (8), with a number genitors of ssp. ovifera, two have contig- Madison, Wisconsin, suggests a consid- of regionally distinct cultivar varieties uous present-day geographical ranges erable amount of genetic separation be- now recognized (17). AMS radiocarbon north of Mexico (C. pepo ssp. ovifera dating of uncarbonized thin-testa Ch. tween the modern Mexican domesticate var. texana and C. pepo ssp. ovifera var. berlandieri fruits from Cloudsplitter and and eastern North American wild sam- ozarkana), whereas the third (C. pepo Newt Kash rockshelters in eastern Ken- ples (19). Given this apparent degree of ssp. fraterna) occurs today in northeast- tucky (Fig. 2) indicated conventional genetic separation and recent advances ern Mexico (Fig. 2). radiocarbon ages of 3,450 Ϯ 150 and in ancient DNA analyses, a three-way In an initial molecular study focused 3,400 Ϯ 150 B.P., respectively (inter- on these progenitor candidates, the cepts with the calibration curve of 3,700 isozyme alleles of the cultivar members ‡McClung de Tapia, E. & Rios-Fuentes, J., 71st Annual Meet- and 3,640) (Table 1), providing the ear- ing of the Society for American Archaeology, April 26, of C. pepo ssp. ovifera (C. pepo ssp. ovif- liest available evidence for this species 2006, San Juan, Puerto Rico, Session 158. era var. ovifera) were shown to be a sub-

Smith PNAS ͉ August 15, 2006 ͉ vol. 103 ͉ no. 33 ͉ 12225 Downloaded by guest on September 30, 2021 set of those in var. ozarkana, whereas and thin rind fragments recovered from squash in Tamaulipas at 6,000 B.P. pro- the other two progenitor candidates archaeological sites across eastern North vides further evidence against the do- (var. texana and ssp. fraterna) were both America indicate the widespread use of mestication of the ‘‘eastern’’ lineage (C. found to lack common alleles of the do- wild gourds of this species as early as pepo ssp. ovifera) from C. pepo ssp. fra- mesticates. As a result, var. ozarkana 8,000 B.P. The earliest evidence of do- terna in northeast Mexico. If this large was designated the best candidate to be mesticated C. pepo squash in the East 6,000 B.P. C. pepo squash of Tamaulipas the wild ancestor of the ‘‘eastern’’ C. was recovered from water-saturated represents domesticated C. pepo spp. pepo lineage (25), and eastern North habitation layers of the Phillips Spring ovifera locally derived from a wild ssp. America was identified as the region of site in south-central Missouri, within the fraterna progenitor, then it would have domestication. present day geographical range of the had to have undergone substantial sub- A subsequent genetic study using an wild gourd C. pepo ssp. ovifera var. ozar- sequent size reduction as it diffused intron region from the mitochondrial kana (Fig. 2). Along with rind fragments north to arrive in the eastern United nad1 gene as a marker, however, found and fruit stems, a total of 125 whole States at 5,000 B.P. as a much-smaller- that all three of the progenitor candi- seeds and fragments identified as C. fruited, smaller-seeded domesticate. If, dates (ssp. fraterna, var. texana, and var. pepo were recovered from Unit K2 (the on the other hand, the large-seeded, ozarkana) shared identical mtDNA se- ‘‘squash and gourd zone’’) at the site. Of large-fruited C. pepo squash represents a quences at the nad1 locus and con- these, 62 provided both length and long-extant domesticate of the other C. cluded that each should therefore be width measurements (mean length, 10.5 pepo lineage (C. pepo ssp. pepo), then considered to have equal likelihood of mm; range, 8.3–12.2 mm), and 12 ex- the local wild gourd, C. fraterna, would being the wild ancestor of the ssp. ovif- ceeded the 11.0-mm seed-length ceiling have had to have been brought under era lineage of domesticated C. pepo (12). established for wild Cucurbita, providing domestication in northeast Mexico even In addition, if ssp. fraterna turned out to clear evidence of domestication (28). though an already long-domesticated in fact be the wild ancestor the C. pepo Direct AMS dating of one of the Phil- pepo squash (as well as another domesti- ssp. ovifera lineage, rather than either of lips Spring squash seeds yielded a con- cated squash, C. argyrosperma) was al- the north of the border wild gourds, ventional radiocarbon age of 4,440 Ϯ 75 ready being cultivated in the region. In then initial domestication could have B.P. and a calibration curve intercept of addition, once domesticated, the newly taken place in northeastern Mexico, 5,025 B.P. (Table 1). In contrast to the domesticated fraterna-derived squash with the domesticate subsequently being Unit K2 C. pepo seed assemblage, how- would have had to have been carried introduced into eastern North America. ever, the thin rind fragments and four northward into the eastern United In contrast to the mitochondrial nad1 fruit-end peduncle scars from the States without leaving any trace in the study, which could not distinguish be- squash and gourd zone at Phillips Spring archaeological record of Tamaulipas, tween the three potential progenitor show no indication of morphological and this new domesticate would have gourds, a higher-resolution approach changes beyond the parameters of the had to have made the journey north un- involving phenetic analysis of random wild morphotype. They compare closely accompanied by either of the other do- amplified polymorphic DNA fragment with var. ozarkana in both diameter and mesticated squashes that were being data was able to separate ssp. fraterna circular outline, indicating that the Phil- grown in Northeast Mexico at 6,000– from var. texana and var. ozarkana, and lips Spring C. pepo assemblage was at an 5,000 B.P. C. argyrosperma, for example, effectively excluded ssp. fraterna from early stage of domestication. Over the does not appear in the East until after the cluster that includes all cultivated next 4,000 years, there is a well docu- A.D. 1,000 (31). Both molecular and and wild varieties of ssp. ovifera (24). mented gradual increase in seed size, archaeological evidence now provides Further support for excluding ssp. fra- fruit size, peduncle size, and rind thick- compelling support for the independent terna from contention as a potential ness of C. pepo in the archaeological domestication of C. pepo ssp. ovifera in progenitor is provided by a recent ge- record of eastern North America (29), eastern North America from an indige- netic study employing amplified frag- providing a clear developmental trajectory nous eastern North American Cucurbita ment-length polymorphism, inter-simple from an early, large-seeded, small-fruited gourd. sequence repeat, and simple sequence domesticate to later larger-fruited forms. repeat markers, in which ssp. fraterna By the time domesticated C. pepo first Sunflower (Helianthus annuus) was again placed at a greater genetic appears in the archaeological record of As is the case with Ch. berlandieri, wild distance from the domesticates of ssp. eastern North America 5,000 years B.P., forms of sunflower (H. annuus) have a ovifera than the eastern North American a domesticated pepo squash had already broad present-day distribution in North wild gourds (26). Molecular evidence been undergoing human selection in America that encompasses much of the thus now supports the Ozark wild gourd Mexico for five millennia. A domesti- central and western continental United (C. pepo ssp. ovifera var. ozarkana)as cated variety of C. pepo. ssp. pepo was States and southern Canada, along with the best candidate to be the progenitor being grown in the south-central high- northern Mexico. Its pre-Columbian dis- of the domesticated squashes of the C. lands of Mexico at 10,000 B.P. (23), and tribution, however, is less well under- pepo ssp. ovifera lineage (22, 27). In ad- by 8,500 B.P. its seeds and peduncles stood (27). The geographical range of dition, the archaeological sequences of were already substantially larger than wild sunflower probably did not extend both northeastern Mexico and eastern those recovered from 5,000 B.P. depos- very far to the east of the Plains before North America also provide substantial its at the Phillips Spring site (28). A do- the mid-Holocene, when it appears parallel evidence that ssp. ovifera was mesticated C. pepo squash with large to have experienced a bison- and͞or domesticated in eastern North America fruits, large peduncles, and large seeds human-mediated range extension into from an indigenous wild Cucurbita was also being grown as far north as the eastern woodlands before being gourd. Tamaulipas, in northeast Mexico, by brought under domestication (8, 27). In In the eastern United States, a de- 6,000 B.P. (30), in close proximity to the the early 1950s, Charles Heiser (32) hy- tailed archaeological record exists for modern-day range of the wild Cucurbita pothesized that sunflower was initially the initial domestication and subsequent gourd C. fraterna. domesticated in the east-central United human selection, over time, for desired The presence of this large-seeded, States, and subsequent archaeological traits in C. pepo. Small C. pepo seeds large-fruited domesticated C. pepo research in eastern North America has

12226 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0604335103 Smith Downloaded by guest on September 30, 2021 provided considerable support for his early interpretation. The earliest evidence for domesticated sunflower in the eastern woodlands of the United States consists of six complete carbonized seeds recovered from Level 14 of the Hayes site in Tennessee (33). When established correction ratios were used to estimate uncarbonized achene length measurements from these carbonized seeds, three of the specimens, with length estimates of 7.3, 7.3, and 7.4 mm, exceeded the 7-mm individual-achene-length baseline proposed for domesticated sunflower, and the mean length of all six seeds (x ϭ 6.9 mm) exceeded the 6-mm baseline mean for identifying domesticated sunflower seed assemblages (8). Direct AMS dating of one of these seeds yielded a conventional radiocarbon age of 4,265 Ϯ 60 B.P. and a calibration curve intercept of 4,840 B.P. (33) Fig. 3. Comparison of an archaeological sunflower achene from eastern North America with the San (Table 1). Andre´s specimen. (Left) Scanning electron micrograph of a sunflower achene from Cloudsplitter Rock- A recent study, however, questioned shelter in eastern Kentucky, exhibiting distinctive parallel longitudinal strands or bundles of sclerenchyma fibers (achene length, 9.2 mm). (Right) San Andre´s achene (achene length, 8.2 mm). (Photograph of San the accuracy and applicability of the Andre´s achene courtesy of David Lentz, Chicago Botanic Garden, Glencoe, IL.) correction ratios used for estimating precarbonization achene length values from carbonized sunflower seeds and than length and width measurements the parenchyma cell boundaries between argued that the Hayes-site sunflower and low-resolution photographs, and sclerenchyma bundles, and as a result this specimens did not meet the threshold unfortunately, no morphological or distinctive and diagnostic morphological for domesticated status (9). This pro- other basis for their identification as H. marker of H. annuus is retained even in posed reclassification of the Hayes-site annuus is offered. Their taxonomic iden- very fragmented and highly eroded speci- sunflower specimens as wild rather than tification is based on expert authentica- mens. The San Andre´s achene specimen domesticated, however, was itself based tion rather than on explicit recognition lacks this morphology, and its identifica- on a misapplication of ceiling standards and documentation of any taxonomically tion as H. annuus is not supported (Fig. developed for individual seeds vs. seed diagnostic morphology. When the San 3). The identification of the San Andre´s assemblages (8). When compared with Andre´s site specimens are considered site seed as sunflower can also be called the modern wild reference class sun- within the context of documented mor- into question. Although appearing to be flower samples used to establish the phological attributes of sunflower comparable with sunflower seeds in wild–domesticated boundary, the Hayes- achenes and seeds, they cannot be iden- general outline, the San Andre´s speci- site specimens are clearly larger than tified as H. annuus with any degree of men exhibits evidence of edge damage, those collected from modern wild confidence. and given the absence of any detailed populations. The shell or pericarp of a sunflower morphological description or high reso- In the same study that incorrectly achene gains its mechanical structure, lution images, it cannot be assigned to questioned the domesticated status of strength, and distinctive appearance H. annuus without additional documen- the Hayes-site sunflower specimens, two specimens of about the same age as the from a sclerenchymatous endocarp, tation. Domesticated sunflower may well Hayes-site seeds, recovered from a site which underlies thin outer epidermis, be present in the archaeological record on the Gulf coast of Tabasco, in Mexico, hypodermis, and carbon layers. Rather of Mexico, but as is the case for any are identified as representing domesti- than being continuous and uniform in discussion of early domesticates, sup- cated sunflower. A partially carbonized structure, the endocarp layer of sun- porting arguments should be based on achene measuring 8.2 ϫ 4.5 mm and a flower achenes is comprised of a large description and documentation of diag- carbonized seed measuring 7.8 ϫ 4.4 number of parallel isolated strands or nostic morphology (36). mm were recovered from Late Archaic bundles of sclerenchyma fibers arranged Given this reassessment of the Hayes- horizon contexts in different excavation longitudinally through the pericarp and site sunflower seed assemblage and the units of the San Andre´s site (Fig. 2). separated by parenchyma cells, forming San Andre´s-site specimens, the assertion Direct AMS dates obtained on the long-axis ropelike ridges (34, 35). These that the San Andre´s sunflower speci- achene and seed yielded conventional parallel strands are evident even when mens represented ‘‘a challenge to the radiocarbon ages of 4,498 Ϯ 50 B.P. and covered by an achene’s epidermis, hy- hypothesis that eastern North America 4,617 B.P., respectively (9, 10). Both drodermis, and carbon layers, and intact was a center of domestication indepen- specimens are larger than achenes pro- sunflower achenes are often described dent of such centers in other parts of duced by modern wild sunflowers and as exhibiting longitudinal surface lines, the hemisphere’’ (9) cannot be sus- are presented as evidence for the earli- ridges, or striations. The endocarp tained. At the same time that currently est domesticated sunflower in the ridges become even more distinct if available archaeological evidence offers Americas. overlying layers are absent (Fig. 3). strong support for the initial domestica- No description of the two San Andre´s When sunflower achenes erode and tion of sunflower in the eastern United specimens is provided, however, other fragment, they split longitudinally along States, recent comprehensive genetic

Smith PNAS ͉ August 15, 2006 ͉ vol. 103 ͉ no. 33 ͉ 12227 Downloaded by guest on September 30, 2021 studies of modern populations of wild Conclusions record of this major transition in human and domesticated sunflower provides As briefly outlined above, all four of the history (37). conclusive confirmation. seed plants proposed two decades ago Such well documented regional In a landmark genetic study of H. an- as having been initially brought under records of the timing, sequence, and nuus involving 18 microsatellite loci dis- domestication in eastern North America spatial, temporal, cultural, and envi- tributed across the sunflower genome can be confidently confirmed as indige- ronmental contexts of initial domesti- that included 21 present-day wild popu- nous eastern domesticates, based on cation of different species are the key lations of wild H. annuus from through- to gaining a better overall understand- substantial archaeological evidence and out its geographical range, along with ing of the transition from a hunting recent genetic studies. Research of the eight Native American landraces and and gathering way of life to human re- past two decades has thus substantially two modern cultivars, Harter et al. (14) liance on food-production economies. showed that all extant domesticated sun- strengthened the case for the eastern Over the next several decades, genetic flowers resulted from a single domesti- United States being an independent and archaeological research on the do- cation event. This single domestication center of plant domestication. Maize mestication of plants and animals event, which involved a substantial ge- (Zea mays), the earliest documented should substantially increase the num- netic bottleneck, occurred in eastern Mesoamerican domesticate to reach the ber of comparably well documented North America (14, 27), confirming East, does not arrive until ca. 2,200 B.P., primary centers of domestication. This Heiser’s 1951 hypothesis. As a result, if almost 2,500 years after the local do- improved and expanded set of region- domesticated sunflower is at some point mestication of marshelder, squash, and al-scale developmental sequences, in documented in the archaeological sunflower (8). turn, will allow much more informed record of Mexico, it will represent ei- Domestication of crop plants and the comparative analyses and better oppor- ther the southward dispersal of domesti- transition to food production occurs tunities for the recognition of general cated sunflower from eastern North much more recently in Eastern North shared patterns of developmental vari- America or a second independent do- America than in most other parts of the ation and commonality in the transi- mestication of sunflower in Mexico. If tion to agriculture, worldwide. sunflower was in fact domesticated a world, and the region certainly does not second time in Mexico, it left little trace compare with a number of the other Marcia Bakry produced Figs. 1 and 2. Eve in the archaeological or early historical centers of domestication in terms of having produced any of today’s most Emshwiller, Kristin Gremillion, Charles record of Mexico, contributed nothing Heiser, Joyce Marcus, Lee Newsom, Dolores to the present-day domesticated sun- important crop plants (Fig. 1). But the Piperno, Loren Rieseberg, and Melinda flower genome, and was, at most, a eastern woodlands of North America Zeder commented on early drafts of this arti- short-lived, peripheral, now-extinct mi- does represent, along with the Near cle, and their suggestions for improvement nor cultigen. East, the best-documented regional are greatly appreciated.

1. Vavilov, N. I. (1992) The Origin and Geography of 14. Harter, A. V., Gardner, K. A., Falush, D., Lentz, 26. Paris, H. S., Yonash, N., Portnoy, V., Mozes- Cultivated Plants (Cambridge Univ. Press, Cam- D. L., Bye, R. A. & Rieseberg, L. (2004) Nature Daube, N., Tzuri, G. & Katzir, N. (2003) Theor. bridge, U.K.). 430, 201–205. Appl. Genet. 106, 971–978. 2. Smith, B. D. (1998) The Emergence of Agriculture 15. Asch, D. & Asch, N. (1985) in Prehistoric Food 27. Rieseberg, L. H. & Harter, A. V. (2006) in (Freeman, New York). Production in Eastern North America, ed. Ford, Darwin’s Harvest—New Approaches to the Ori- 3. Smith, B. D. (2001) Proc. Natl. Acad. Sci. USA 98, R. I. (Museum of Anthropology, Univ. of Michi- gins, Evolution, and Conservation of Crops: A 1324–1326. gan, Ann Arbor), Anthropological Papers No. 75, Broad Taxonomic and Geographic Survey, ed. 4. Zeder, M. A., Bradley, D. G., Emshwiller, E. & pp. 149–203. Motley, T. (Columbia Univ. Press, New York), Smith, B. D. (2006) Documenting Domestication 16. Wilson, H. D. (1990) Econ. Bot. Suppl. 44, 92–110. pp. 31–48. (Univ. of California Press, Berkeley). 17. Gremillion, K. J. (1993) J. Ethnobiol. 13, 149–169. 28. Smith, B. (2006) in Documenting Domestication: 5. Piperno, D. R. & Pearsall, D. (1998) The Origins 18. Bruno, M. C. (2006) in Documenting Domestica- New Archaeological and Genetic Paradigms, eds. of Agriculture in the Lowland Neotropics (Aca- tion: New Archaeological and Genetic Paradigms, Zeder, M., Bradley, D., Emshwiller, E. & Smith, B. demic, New York). eds. Zeder, M., Bradley, D., Emshwiller, E. & (Univ. of California Press, Berkeley), pp. 25–31. 6. Denham, T. P., Haberle, S. G., Lentfer, C., Full- Smith, B. (Univ. of California Press, Berkeley), pp. 29. Cowan, C. W. (1997) in People, Plants, and Land- agar, R., Field, J., Therin, M., Porch, N. & Wins- 32–45. scapes, ed. Gremillion, K. (Univ. of Alabama borough, B. (2003) Science 301, 189–193. 19. Ruas, P. M., Bonifacio, A., Ruas, C., Fairbanks, D. Press, Tuscaloosa), pp. 63–85. 7. Olsen, K. & Schall, B. A. (1999) Proc. Natl. Acad. & Anderson, W. R. (1999) Euphytica 105, 25–32. 30. Smith, B. D. (1997) Lat. Am. Antiquity 8, 342– Sci. USA 96, 5586–5591. 20. Robinson, R. W. & Decker-Walters, D. S. (1997) 383. 8. Smith, B. D. (2006) Rivers of Change (Univ. of Cucurbits (CAB International, New York). 31. Fritz, G. (2006) in Handbook of North American Alabama Press, Tuscaloosa), 3rd Ed. 21. Decker-Walters, D. (1990) in Biology and Utiliza- Indians, ed. Ubelaker, D. (Government Printing 9. Lentz, D. L., Pohl, M. E. D., Pope, K. O. & Wyatt, tion of the Cucurbitaceae, eds. Bates, D. & Jeffrey, A. R. (2000) Econ. Bot. 55, 370–376. C. (Cornell Univ. Press, Ithaca, New York), pp. Office, Washington, DC), Vol. 3, pp. 437–446. 10. Pope, K. O., Pohl, M. E. D., Jones, J. G., Lentz, 96–101. 32. Heiser, C. B. (1951) Proc. Am. Philos. Soc. 95, D. L., von Nagy, C., Vega, F. J. & Quitmyer, I. R. 22. Emshwiller, E. (2006) in Documenting Domestica- 432–448. (2001) Science 292, 1370–1373. tion: New Archaeological and Genetic Paradigms, 33. Crites, G. (1993) Am. Antiquity 58, 146–148. 11. Piperno, D. R. (2001) Science 292, 2260–2261. eds. Zeder, M. A., Bradley, D., Emshwiller, E. & 34. Roth, I. (1977) Fruits of Angiosperms (Gebru¨der 12. Sanjur, O. J., Piperno, D. R., Andres, T. C. & Smith, B. D. (Univ. of California Press, Berkeley), Borntraeger, Berlin, Germany). Wessel-Beaver, L. (2002) Proc. Natl. Acad. Sci. pp. 99–122. 35. Saenz, A. A. (1981) Darwiniana 23, 37.117. USA 99, 535–540. 23. Smith, B. D. (1997) Science 276, 932–934. 36. Smith, B. D. (2001) in Archaeology at the Millen- 13. Sanjur, O. J., Piperno, D. R., Andres, T. C. & 24. Decker-Walters, D. S., Staub, J. E., Chung, S.-M., nium, eds. Feinman, G. M. & Price, T. D. (Kluwer, Wessel-Beaver, L. (2005) in Biomolecular Archae- Nakata, E. & Quemada, H. (2002) Syst. Bot. 27, New York), pp. 199–230. ology, ed. Reed, D. M. (Center for Archaeological 19–28. 37. Bellwood, P. & Renfrew, C., eds. (2002) Examin- Investigations, Southern Illinois Univ., Carbon- 25. Decker-Walters, D., Walters, T., Cowan, C. W. & ing the Farming/Language Dispersal Hypothesis dale), Occasional Paper No. 32, pp. 128–150. Smith, B. D. (1993) J. Ethnobiol. 13, 55–72. (Oxbow Books, Oxford).

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