REPORTS

tant role in locomotor propulsion than the fore- ⫺1.678 ⫹ 2.518 (1.80618), W ⫽ 741.1; anteropos- phylogeny place Lagostomus together with Chin-
limbs, which were probably important in food terior distal humerus diameter (APH): log W ⫽ chilla (22).
⫺1.467 ⫹ 2.484 (1.6532), W ⫽ 436.1 kg. 25. M. S. Springer et al., Proc. Natl. Acad. Sci. U.S.A. 98,
manipulation. Because of this, the body mass 17. A. R. Biknevicius, J. Mammal. 74, 95 (1993). 6241 (2001).
estimation based on the femur is more reliable: 18. The humerus/femur length ratio (H/F) and the (humer- 26. We thank J. Bocquentin, A. Ranci, A. Rincón, J. Reyes,
P. pattersoni probably weighed ⬃700 kg. With us ⫹ radius)/(femur ⫹ tibia) length ratio [(H ⫹ R)/(F ⫹ D. Rodrigues de Aguilera, and R. Sánchez for help with
T )] in P. pattersoni (0.76 and 0.78, respectively) are fieldwork; J. Reyes and E. Weston for laboratory work;
Phoberomys, the size range of the order is in- average compared with those of other caviomorphs. For E. Weston and three anonymous reviewers for com-
creased and Rodentia becomes one of the mam- a sample of 17 extant caviomorphs, the mean values ⫾ ments on the manuscript; O. Aguilera Jr. for assist-
malian orders with the widest size variation, SD were H/F ⫽ 0.80 ⫾ 0.08 and (H ⫹ R)/(F ⫹ T ) ⫽ ance with digital imaging; S. Melendrez for recon-
0.74 ⫾ 0.09. In the sample, there are no marked trends struction of the skeleton of Phoberomys in Fig. 2; D.
second only to the Diprotodontia (kangaroos, associated with growth or phylogeny (21). On the other Mörike (Stuttgart) and E. Weber ( Tübingen) for ac-
koalas, wombats, and possums) (fig. S1). hand, the ratios between femur versus humerus cross- cess to collections; and J. Bocquentin and A. Ranci for
The fossil record of Caviomorpha is exten- sectional diameters (APF/APH) (15) show that the hind- preliminary work on the identification of the giant
sive, with 140 fossil genera recognized in a limbs of P. pattersoni are robust. APF/APH is 1.42, rodent. Work in Venezuela by M.R.S.-V. was partially
whereas the average ⫾ SD for a sample of 19 cavi- supported by the National Geographic Society and
recent review (8), but no form competes with omorph species (21) is 1.27 ⫾ 0.18. Robust hindlimbs in the University of Tübingen. The Smithsonian Tropical
Phoberomys in terms of size. Artigasia magna comparison to forelimbs characterizes also the clade Research Institute and the Universidad Nacional Ex-
from the upper Pliocene of Uruguay is reported composed of Dinomys, Chinchilla, and Lagostomus perimental Francisco de Miranda (UNEFM) supported
(mean ⫾ SD 1.40 ⫾ 0.26), the closest relatives to the field and laboratory work of O.A. O.A. is a Re-
to be gigantic, but its lower teeth are only Phoberomys among extant caviomorphs. search Associate of the Smithsonian Tropical Re-
⬃60% the size of those of P. pattersoni (19). 19. J. C. Francis, A. Mones, Kraglieviana 1, 89 (1966). search Institute.
Artigasia, like most fossil rodents, is known 20. R. C. Wood, Breviora 436, 1 (1976).
21. M. R. Sánchez-Villagra, O. Aguilera, I. Horovitz, un- Supporting Online Material
based only on dental and mandibular parts. www.sciencemag.org/cgi/content/full/301/5640/1708/
published data.
The paleoenvironment in which P. patter- 22. R. M. Nowak, Walker’s Mammals of the World ( John DC1
soni was found and the associated fauna indi- Hopkins Univ. Press, Baltimore, ed. 6, 1999). SOM Text
cate that this rodent was either semiaquatic or 23. D. Huchon, J. P. Douzery, Mol. Phylogenet. Evol. 20, Fig. S1
238 (2001). Tables S1 to S3
foraged in or near water, as capybaras do. P.
24. We added Lagostomus to the tree to increase the References
pattersoni had a deep and massive horizontal relevant sampling in our scaffold analysis. All rel-
ramus of the mandible, correlated with a high evant treatments of caviomorph taxonomy and 6 May 2003; accepted 6 August 2003
degree of hypsodonty. Phoberomys clearly had
an abrasive diet, perhaps consisting of sea-
Amazonia 1492: Pristine Forest

Downloaded from https://www.science.org at FU Berlin/CBF on October 17, 2021

grasses. Potential predators could have been the
many crocodiles reported from Urumaco, in-
cluding some of the largest forms that ever or Cultural Parkland?
existed, such as Purussaurus spp. Contempo-
raries included Stupendemys geographicus, the Michael J. Heckenberger,1* Afukaka Kuikuro,4
world’s largest turtle (20). Urissapá Tabata Kuikuro,4 J. Christian Russell,2
Morgan Schmidt,3 Carlos Fausto,5 Bruna Franchetto5
References and Notes
1. D. Starck, Lehrbuch der Speziellen Zoologie. Wirbelt- Archaeology and indigenous history of Native Amazonian peoples in the Upper
iere. Teil 5: Säugetiere (Gustav Fischer Verlag, Jena,
Germany, 1995). Xingu region of Brazil reveal unexpectedly complex regional settlement pat-
2. J. J. Flynn, A. R. Wyss, Trends Ecol. Evol. 13, 449 terns and large-scale transformations of local landscapes over the past mil-
(1998). lennium. Mapping and excavation of archaeological structures document pro-
3. R. F. Kay, R. H. Madden, R. L. Cifelli, J. J. Flynn, Eds.,
Vertebrate Paleontology in the Neotropics. The Mio-
nounced human-induced alteration of the forest cover, particularly in relation
cene Fauna of La Venta, Colombia (Smithsonian In- to large, dense late-prehistoric settlements (circa 1200 to 1600 A.D.). The
stitution, Washington, DC, 1997). findings contribute to debates on human carrying capacity, population size and
4. Léxico Estratigráfico de Venezuela (Ministerio de En-
ergı́a y Minas, Boletı́n de Geologı́a, Caracas, ed. 3,
settlement patterns, anthropogenic impacts on the environment, and the im-
1997). portance of indigenous knowledge, as well as contributing to the pride of place
5. A. Mones, Ameghiniana 17, 277 (1980). of the native peoples in this part of the Amazon.
6. A. Mones, Comun. Paleontol. Mus. Hist. Nat. Montev.
2, 1 (1997).
7. F. R. Negri, J. Ferigolo, Bolet. Mus. Pare. Emı́lio Goeldi
Was the Amazon a natural forest in 1492, garding pre-Columbian cultural and ecologi-
11, 1 (1999). sparsely populated and essentially pristine, as cal variation in the region remain unresolved
8. M. C. McKenna, S. K. Bell, Classification of Mammals has been traditionally thought? Or, instead, due to a lack of well-documented case studies
Above the Species Level (Columbia Univ. Press, New were parts of it densely settled and better (7, 8). Here, we present clear evidence of
York, 1997).
9. S. O. Landry, Univ. Calif. Pub. Zool. 56, 1 (1957). viewed as cultural forests, including large large, regional social formations [circa (c.)
10. M. G. Vucetich, D. H. Verzi, J.-L. Hartenberger, C. R. agricultural areas, open parklands, and work- 1250 to 1600 A.D.] and their substantial in-
Acad. Sci. Ser. II Sci. Terre Planetes 329, 763 (1999). ing forests associated with large, regional fluence on the landscape, where they have
11. L. Kraglievich, An. Soc. Cient. Argent. 114, 155
(1932). polities (1–3). Despite growing popularity for altered much of the local forest cover. Spe-
12. C. de Paula Couto, Tratado de Paleomastozoologia the latter view (4–6), entrenched debates re- cifically, archaeological research in the Up-
(Academia Brasileira de Ciencias, Rı́o de Janeiro, per Xingu (Mato Grosso, Brazil), including
1979).
13. B. Demes, W. L. Jungers, Folia Primatol. 52, 58 1
Department of Anthropology, 2Land-Use and En- detailed mapping and excavations of exten-
(1989). vironmental Change Institute, 3Department of Ge- sive earthen features (such as moats, roads,
14. J. Bertram, A. A. Biewener, J. Morphol. 204, 157 ography, University of Florida, Gainesville, FL and bridges) in and around ancient settle-
(1990). 32611, USA. 4Associação Indı́gena Kuikuro do Alto
15. A. R. Biknevicius , D. A. McFarlane, R. D. E. MacPhee,
ments, reveals unexpectedly complex region-
Xingu, Parque Indı́gena do Xingu, Mato Grosso,
Am. Mus. Novit. 3079, 1 (1993). Brazil. 5Department of Anthropology, Museu Nacio-
al settlement patterns that created areas of
16. Predictive equations for body size (15): log W ⫽ log nal, Universidade Federal do Rio de Janeiro, Quinta acute forest alteration.
a ⫹ b (log AP), where W is body mass (in kilograms), da Boa Vista, Rio de Janeiro 20940 – 040, Brazil. The Upper Xingu is unique in the south-
log a is intercept, b is slope, and AP is the antero-
posterior diameter of the bone examined. Anteropos- *To whom correspondence should be addressed. E- ern peripheries of the Amazon as the larg-
terior proximal femur diameter (APF): log W ⫽ mail: [email protected]fl.edu est contiguous tract of tropical forest still

1710 19 SEPTEMBER 2003 VOL 301 SCIENCE www.sciencemag.org

 REPORTS
under indigenous resource management elaborate regional plan (14 ). The earth- tlements. In the case of the Kuhikugu (X11)
[Parque Indı́gena do Xingu (PIX)]. It re- works include (i) excavated ditches in and cluster, the largest residential center is the
mains little affected by 20th century mech- around ancient settlements (up to 2.5 km hub (Fig. 3B). The primary nodes of each
anized development (Fig. 1). The Upper long and 5 m deep); (ii) linear mounds or cluster are also linked by roads to smaller
Xingu is a long-standing case study of in- “curbs” positioned at the margins of major plaza settlements (fig. S1). On the basis of
digenous Amazonian agriculture and ecol- roads and circular plazas (averaging about artifact and dark-earth distributions, it has
ogy (9, 10) and one of the few places where 0.5 to 1.0 m in height); and (iii) a variety of been estimated that large sites, such as X6
contemporary observations about indige- wetland features, such as bridges, artificial and X11, had 15 to 25 ha of residential
nous agriculture, land use, and settlement river obstructions and ponds, raised cause- space, medium sites (X17, X18, X22) had 5
pattern can be systematically linked with ways, canals, and other structures, many of to 10 ha, and small sites had 2 to 5 ha (14 ).
archaeological and oral historical evidence which are still in use today. Similar con- Thus, the actual residential area of a cluster
(11). Long-term in situ cultural develop- structed features (such as settlements, like X6 or X11 was at least 40 to 80 ha in
ment of Xinguano peoples over more than roads, weirs, and ponds) are known from an area of about 400 km2, with an estimated
1000 years (12) is clearly documented by culturally related peoples ( principally population of between 2500 and 5000 per-
continuity in (i) utilitarian ceramics used to Arawak speakers) across the southern Am- sons (or about 6 to 12.5 persons per km2 in
process and cook staple foods (13); (ii) azonian periphery (17–19) [supporting on- the study area).
settlement placement (at forest/wetland line material (SOM) text]. Areas within each galactic cluster can
transitions) and local land use, marked by The integrated settlement configuration be characterized as saturated anthropogenic
substantial forest and wetland alterations; was in place by c. 1250 to 1400 A.D., based landscapes, because virtually the entire
and (iii) settlement form, notably circular on radiocarbon dates from stratified depos- area in and between major settlements, al-
plazas with radial roads (14 ) (movie S1). its at X6, X11, and X13 ( Table 1) (14, 20). though not entirely cultural in origin, was
In the Kuikuro study area (Fig. 2) (15), Major curbed roads (10 to 50 m wide) carefully engineered and managed. Indeed,
19 major pre-Columbian settlements have articulate with plazas, ditches, and partition the road networks, oriented by the same
been identified, generally separated by 3 to space within villages and across the broad- system of cardinality that characterizes pla-
5 km and linked by a system of broad, er landscape, notably linking settlements za spatial organization, partitioned the
straight roads (16 ). Recognition and map- into “galactic” clusters across the region landscape into a gridlike or latticelike or-
ping of major earthworks at these sites (21). The Ipatse cluster includes four major ganization of nodes ( plazas) and connect-

Downloaded from https://www.science.org at FU Berlin/CBF on October 17, 2021

reveal their articulation in a remarkably residential settlements (X6, X17, X18, and ing thoroughfares, although patches and
X22), linked to a fifth unfortified “hub” site corridors of secondary and perhaps man-
(X13), with only limited residential occu- aged forests were likely common, as they
pation (Fig. 3A). Another cluster of sites, are today. Mapped archaeological features
centered on X11, shows a similar pattern of correspond to patches of acutely modified
a large (50 ha) fortified settlement connect- secondary growth, distinctive from sur-
ed to other smaller but still elaborate set- rounding forest and easy to recognize in

Fig. 2. Kuikuro study area showing

the distribution of major ditched
plaza centers (stars in circles), ma-
jor plaza centers (open circles),
and small plaza and non-plaza vil-
lages (black dots).

Fig. 1. Upper Xingu region image [Landsat 7

Enhanced Thematic Mapper, path 225, rows
68 to 69; 12 August 1999; image is a com-
posite false-color infrared with bands as-
signed as 5-4-3 (red-green-blue) to provide
the appearance of natural vegetation] with
the approximate boundaries of the PIX and
the Kuikuro study area (inset of Upper Xingu,
Brazil). The ecological transition between the
closed forests of southern Amazonia and the
more open savanna/gallery forest of the Bra-
zilian Planalto Central is shown (lower right).

www.sciencemag.org SCIENCE VOL 301 19 SEPTEMBER 2003 1711

 REPORTS

Fig. 3. Satellite image [Landsat 4 Thematic Mapper, path 225, row 69;
21 June 1992; bands were assigned as 5(red)-4(green)-3(blue)] with
global positioning system–mapped Ipatse cluster sites X6 and X13 (A,
insets) linked by the “north-south road” and transit-mapped X11 (B, road, as well as across high ground to X17 and X22 (fig. S1); X11 roads

Downloaded from https://www.science.org at FU Berlin/CBF on October 17, 2021

inset). Ditches are colored in red; road and plaza curbs are black. also connect it to the four satellites. MTFX, Mato Grosso (the state),
Fieldwork in 2003 demonstrates that roads extend fully from X13 to Formadores do Xingu (the archaeological region). The number refers
X18, and continue on to X19, X20, and beyond along the north-south to the site number.

Table 1. Radiocarbon dates from Nokugu ( X6) and other sites in the Kuikuro study area, southern PIX. satellite images. These patches or islands
Beta 176135 to Beta 176144 are reported here for the first time. Calibrated age ranges for samples dated are identified in the indigenous knowledge
in 2003 (numbered 176135 and up) were reported by Beta-Analytic laboratory; previous (1994) dates systems, including diverse species whose
were calibrated using CALIB 4.0 (29). ET, excavation trench of 1.0 by 10.0 m or more; EU, excavation unit
of 1.0 m2; S, southern side of plaza or site; N, northern side; Ditch 1, outermost; Ditch 2, middle; Ditch distributions are generally restricted to an-
3, innermost ditch in all sites. throsols (dark earth)—called egepe by the
Kuikuro—associated with ancient settle-
Conventional 2⌺-calibrated ments (22–24 ) (SOM text). Some areas
Lab no. Site/unit Provenance
radiocarbon age range related to major pre-Columbian settle-
Historical Xinguano (1700 A.D.–present) ments, like X6, X11, and X13, have not
Beta 176142 X6/ET2 20 ⫾ 50 modern* Ditch 3 (S), upper ditch infill returned to high forest after about 400 years
Beta 72260 X6/ET1 180 ⫾ 60 1520 –1940 A.D. Ditch 2 (S), upper ditch infill of abandonment, although other areas (such
Terminal “galactic” period (1400 –1700 A.D.) as roads, hamlets, gardens, fields, and park-
Beta 176137 X6/ET10 340 ⫾ 60 1460 –1640 A.D. Ditch 2 (N), upper ditch infill lands) show a highly patchy forest regrowth
Beta 81301 X6/ET1 360 ⫾ 70 1420 –1640 A.D. Ditch 2 (S), mid-ditch infill typical of postabandonment (after 1600 to
Beta 176135 X6/ET3 440 ⫾ 60 1420 –1480 A.D. Small plaza, subcurb intact 1750) succession.
Beta 72262 X11/EU1 440 ⫾ 70 1400 –1650 A.D. North road, intact/curb interface Recognition of the massive forest alter-
Beta 176140 X6/ET3 530 ⫾ 60 1400 –1430 A.D. Small plaza, subcurb intact ations associated with pre-Columbian occu-
Initial “galactic” period (1250 –1400 A.D.) pations requires an understanding of local
Beta 176139† X6/ET2 590 ⫾ 60 1300 –1420 A.D. Ditch 3 (N), basal fill biodiversity in the context of the complex
Beta 177724† X6/ET2 670 ⫾ 60 1260 –1410 A.D. Ditch 3 (N), basal fill cultural history of the area. The composi-
Beta 88362 X13/EU1 690 ⫾ 60 1260 –1300 A.D. Central plaza, subcurb intact tion of forest and wetland habitats reflects
Beta 78979 X6/ET1 700 ⫾ 70 1230 –1410 A.D. Ditch 2 (S), sub-berm intact
Beta 176136 X6/ET4 710 ⫾ 50 1270 –1300 A.D. Ditch 1 (S), basal fill
long-term cumulative changes, given that
the settlement areas were occupied more or
Late developmental (900 –1250 A.D.) less continuously over many generations,
Beta 72263 X11/EU1 900 ⫾ 60 1000 –1250 A.D. North road, subcurb, basal intact as well as the large-scale alteration and
Beta 88363 X13/EU1 910 ⫾ 80 1040 –1250 A.D. Central plaza, subcurb base intact
Beta 72261 X6/ET1 1000 ⫾ 70 950 –1210 A.D. Ditch 2 (S), sub-berm, base intact
management of local environments by
Beta 176141 X6/ET5 1 030 ⫾ 60 980 –1030 A.D. Central plaza, subcurb base intact dense late-prehistoric occupations (c. 1250
to 1650 A.D.). Present soil and biotic dis-
Initial Xinguano ( pre-900 A.D.)
tributions, often isomorphic with the distri-
Beta 176143† X6/ET2 1370 ⫾ 60 640 – 690 A.D. Mid-ditch 3 (N), mid-ditch
Beta 176138† X6/ET10 2110 ⫾ 40 190 – 60 B.C. Ditch (N), basal fill
bution of archaeological features, notably
plazas, residential areas, roads, and road-
*Two additional modern dates, Beta 98978 and Beta 176144, are considered invalid. The former was redated with a side hamlets, are in large part the result of
sample slightly higher in profile (Beta 81301). †Beta 176139 is inversed with 176143 and was redated by 177724. Beta
176138 also comes from stratified but mixed context of ditch infill, and both likely represent earlier materials that are pre-Columbian land-management strate-
mixed in ditch construction. gies. After c. 1600 to 1700, catastrophic

1712 19 SEPTEMBER 2003 VOL 301 SCIENCE www.sciencemag.org

 REPORTS

Fig. 4. Aerial photographs (U.S. Air Force/Força Aérea Brasileira 1967; same areas shows an ⬃30-year period. Graphic testimony of post-1492
1: 60,000) of Lake Ipatse (A) and Lake Kuhikugu (B) showing land-cover decline in village size is shown by comparing the size of X11 with the four
change during 6-year period (1961 to 1967) after abandonment (Ku- sequential Kuikuro villages (c. 1870s to 1961) in and north of the ancient
hikugu) and reoccupation (Ipatse). Comparison with Fig. 3 (1992) of site and by comparing X6 with the active village in 1967 and 1992.

depopulation (25) led to the abandonment cultivation and land management, indeed, 14. Materials and methods are available as supporting

Downloaded from https://www.science.org at FU Berlin/CBF on October 17, 2021

of these works and many settlements, re- material on Science Online.
provides a viable alternative. The present 15. The Kuikuro study area is about the same as the
sulting in extensive reforestation in many research emphasizes the critical importance Kuikuro (Carib Xinguano) traditional territory. It is
areas. The scale of the prehistoric settle- of collaborative research strategies, including about 1000 km2 and is located in an area of
ments, including exterior constructions, archaeological and ethnographic fieldwork, traditional Xinguano occupations that is 25,000 to
35,000 km2.
such as roads, hamlets, wetland structures, remote-sensed data analysis and geographic 16. Several additional large sites are known in the
and cultivation areas, suggests that agricul- information systems, and most important, in- study area, on the basis of indigenous knowledge
tural and parkland landscapes, rather than digenous participation, to understand the of dark-earth locations, and numerous smaller oc-
cupation sites are also known, including small
high forest, characterized the broad land- complex interplay of ecological, historical, road-side hamlets along the major roads.
scapes around ancient villages, as is true in and political conditions in Amazonia before 17. A. Metraux, BAE, Bulletin 143 (Smithsonian Insti-
contemporary villages. Metal technology, and after 1492. tution, Washington, DC, 1948), vol. 3, pp. 349 –
360.
however, has increased the speed at which 18. C. Erickson, Nature 408, 190 (2000).
forests can be converted into mosaic park- References and Notes 19. M. Heckenberger, in Comparative Arawak Histories:
lands of dispersed manioc gardens, sapé 1. W. Balee, Econ. Bot. 7, 1 (1989). Rethinking Culture Area and Language Group, J.
2. W. Denevan, Ann. Assoc. Am. Geog. 82, 369 Hill, F. Santos-Granero, Eds. (Univ. of Illinois Press,
grass fields, piqui groves, and secondary (1992). Urbana, 2001), pp. 99 –122.
forests (26 ) (Fig. 4). 3. D. Lathrap, The Upper Amazon (Praeger, London, 20. Here, “galactic” describes the regional site clusters
The Upper Xingu is a unique Amazo- 1970). organized around a center or hub ( X11 and X13),
4. C. Mann, Science 287, 786 (2000). with several major residential sites connected to it.
nian example of a tropical forest way of life 5. C. Mann, Atlantic Monthly 2001, 41 (March 2002). 21. S. Tambiah, Ritual, Performance, and Thought (Har-
that supported large, densely settled, and 6. This theory has been widely disseminated in popular vard Univ. Press, Cambridge, MA, 1985).
integrated regional populations over the media [e.g., “Fertile secret: How did ancient Amazo- 22. Dark earth forms in compost areas, although wide-
past 1000 years. Local ecology reflects the nians turn sand into rich soil? Garbage,” American spread burning produces minor but extensive soil
Broadcasting Corporation, 19 September 2002, avail- alterations.
dynamic interaction between the natural able online on http://abcnews.go.com/sections/ 23. W. I. Woods, J. McCann, Yearb. Conf. Lat. Am. Geogr.
environment, the influence of fairly large, scitech/DyeHard/dyehard020919.html; and “The se- 25, 7 (1999).
settled human populations, and the legacy cret of El Dorado,” British Broadcasting Corporation, 24. J. B. Petersen, E. G. Neves, M. J. Heckenberger, in The
19 December 2002, available online on www.bbc- Unknown Amazon, C. McEwan, E. Neves, C. Barreto,
of Euro-American colonialism over the past .co.uk/science/horizon/2002/eldorado.shtml. Eds. (British Museum Press, London, 2001), pp. 86 –
⬃500 years. Evidence of large, well-engi- 7. A. C. Roosevelt, Am. Anthropol. Assoc. Pap. 9 (1999), 105.
neered public works (such as plazas, roads, pp. 13–33. 25. M. Heckenberger, in Os Povos Indı́genas do Alto
8. M. J. Heckenberger, J. B. Petersen, E. G. Neves, Lat. Xingu: História e Cultura, B. Franchetto, M. Hecken-
moats, and bridges) in and between pre- Am. Antiq. 10, 353 (1999). berger, Eds., [Editora Universidade Federal do Rio de
Columbian settlements suggests a highly 9. R. Carneiro, Subsistence and Social Structure (Univ. Janeiro (UFRJ), Rio de Janeiro, 2001], pp. 77–110.
elaborate built environment, rivaling that of of Michigan Press, Ann Arbor, 1957). 26. W. Denevan, J. Steward Anthropol. Assoc. 20, 153
10. R. Carneiro, in Adaptive Responses of Native Amazo- (1992).
many contemporary complex societies of nians, R. Hames, W. Vickers. Eds. (Academic Press, 27. W. Denevan, Cultivated Landscapes of Native Ama-
the Americas and elsewhere (SOM text). New York, 1983), pp. 65–111. zonia and the Andes (Oxford Univ. Press, New York,
To suggest that Xinguano lands were inten- 11. M. Heckenberger, Antiquity 72, 633 (1998). 2001).
12. Initial Xinguano occupations date sometime be- 28. N. Smith, A. Serrão, P. Alvim, I. Falesi, Amazonia:
sively managed and developed, c. 1492, tween 200 B.C. and 800 A.D., but the exact date is Resiliency and Dynamism of a Land and Its People
however, does not imply that indigenous uncertain because the two earliest radiocarbon (United Nations Press, Tokyo, 1995).
land-use strategies, based on patchy devel- dates are from mixed deposits, and in one case 29. M. Stuiver, G. W. Pearson., Radiocarbon 35, 1
opment within long rotational cycles, are (Beta-Analytic Laboratory number 176143) the (1993).
dates are demonstrably out of sequence. 30. Ethnoarchaeological research in the Upper Xingu
comparable to modern nonindigenous 13. Manioc, fish, and piqui fruit constitute 90% or more by M.J.H., conducted in collaboration with the
clear-cutting strategies (27, 28). Xinguano of the diet (9). Museu Nacional (UFRJ), the Museu Goeldi, and the

www.sciencemag.org SCIENCE VOL 301 19 SEPTEMBER 2003 1713

 REPORTS
Kuikuro community, has been ongoing since 1991; Supporting Online Material Fig. S1
2001 to 2003 fieldwork was supported by NSF www.sciencemag.org/cgi/content/full/301/5640/1710/ References
grant Behavioral and Cognitive Sciences no. DC1 Movie S1
0004487 (2001 to 2003). We thank A. Melges, J. Materials and Methods
Petersen, and W. Hillman for their support. SOM Text 25 April 2003; accepted 25 July 2003

Resurrecting the Ancestral box, which mediates recognition of specific

response elements by estrogen and other

Steroid Receptor: Ancient Origin SRs (12), is identical only to that of the
human ERs (Fig. 1B). The ligand-binding
domain (LBD) of the Aplysia receptor is
of Estrogen Signaling less conserved but is also most similar to
that of the vertebrate ER. The Aplysia re-
Joseph W. Thornton,1* Eleanor Need,1 David Crews2 ceptor’s AF-2 activation domain—a small
region in the LBD that mediates ligand-
Receptors for sex and adrenal steroid hormones are absent from fully sequenced regulated interactions with coactivators
invertebrate genomes and have not been recovered from other invertebrates. (13)—is nearly identical to that of the hu-
Here we report the isolation of an estrogen receptor ortholog from the mollusk man ERs but not to those of the ERRs or
Aplysia californica and the reconstruction, synthesis, and experimental char- other SRs (Fig. 1B).
acterization of functional domains of the ancestral protein from which all extant The true test of orthology is phylogeny,
steroid receptors (SRs) evolved. Our findings indicate that SRs are extremely so we analyzed the relations among 74
ancient and widespread, having diversified from a primordial gene before the steroid and related receptors, including the
origin of bilaterally symmetric animals, and that this ancient receptor had Aplysia ER, using maximum parsimony
estrogen receptor–like functionality. This gene was lost in the lineage leading (MP) and Bayesian Markov Chain Monte
to arthropods and nematodes and became independent of hormone regulation Carlo (BMCMC) techniques (11). Both
in the Aplysia lineage. methods (Fig. 2A) strongly indicate that the
Aplysia sequence is an ortholog of the ver-

Downloaded from https://www.science.org at FU Berlin/CBF on October 17, 2021

Vertebrate genomes contain six evolution- that the SR family may have been lost in tebrate ERs. The node indicating orthology
arily related nuclear receptors for steroid the lineage leading to both phyla. A previ- with the vertebrate ERs is well supported,
hormones: two for estrogens (ER␣ and ous analysis of SR sequences indicated that with a BMCMC posterior probability of
ER␤) and one each for androgens (AR), the ancient progenitor of this protein class 100%, a bootstrap proportion of 90%, and a
progestins (PR), glucocorticoids (GR), and was most similar to extant ERs (10). decay index of 6. Although BMCMC prob-
mineralocorticoids (MR). These ligand- We used degenerate PCR and rapid am- abilities can sometimes overestimate statis-
activated transcription factors mediate the plification of cDNA ends to isolate an ER tical confidence (14 ), a 90% bootstrap nor-
actions of hormones that direct sexual dif- sequence (figs. S1 and S2) from a mollusk, mally indicates confidence well over 95%
ferentiation, reproduction, behavior, immu- the sea hare Aplysia californica. Using (15). Further, the maximum likelihood of
nity, and stress response (1). There are no primers derived from vertebrate ERs, we this phylogeny is ⬎100,000 times greater
orthologs of these genes in the insect Dro- amplified an ER-like cDNA sequence from than that of the best phylogeny in which the
sophila melanogaster, the nematode Cae- both adult neural tissue and ovotestes of A. Aplysia receptor is placed outside the clade
norhabditis elegans, or the urochordate californica (11). The protein sequence of of SRs. As this phylogeny shows, the gene
Ciona intestinalis (2, 3), and a polymerase the Aplysia receptor’s DNA-binding do- duplication that produced the first SR pre-
chain reaction (PCR) screen (4 ) failed to main (DBD) is highly similar to that of the ceded the ancient divergence of deuteros-
identify any of these genes outside the ver- vertebrate ERs but much less similar to tomes (the superphylum that includes chor-
tebrates. The most closely related nuclear those of other nuclear receptors, including dates and echinoderms) from protostomes
receptors are the estrogen-related receptors the ERRs (Fig. 1A). Within the DBD, the P [mollusks, arthropods, nematodes, anne-
(ERRs), an ortholog of which is present in
the fruit fly genome (2). Based on this gene
distribution, steroid receptors (SRs) are A B
thought to have evolved in the chordate DBD LBD P-box AF-2 CTE
lineage some 400 to 500 million years ago, AplysiaER 100 100 AplysiaER CEGCKA DLLTEMLDAHNS (+27)
due to a duplication of a more ancient ERR humanERα 88 35 humanERα ...... ...L......RL (+46)
humanERβ 85 32 humanERβ ...... ...L......RL (+30)
gene (4–6 ). Estrogens and other vertebrate- humanERR1 67 23 humanERR1 ..A... K.FL...E.MMD *
type steroids appear to be involved in the humanERR2 70 30 humanERR2 ..A... K.FL...E.KV *
reproductive endocrinology of certain mol- humanERR3 67 30 humanERR3 ..A... K.FL...E.KV *
lusks, however (7, 8). Further, arthropods D.melanERR 67 25 D.melanERR ..A... K.FL...EPLAR *
and nematodes are relatively closely related humanAR 58 21 humanAR .GS..V VDFP..MAEIIS (+18)
within the Ecdysozoan clade of molting humanPR 55 20 humanPR .GS..V VEFP..MSEVIA (+19)
organisms (9), suggesting the possibility humanGR 58 21 humanGR .GS..V IEFP..LAEIIT (+19)
humanMR 56 23 humanMR .GS..V VEFP..LVEIIS (+19)
Fig. 1. The Aplysia ER protein sequence is most similar to that of human ERs. (A) Percent similarity
1
Center for Ecology and Evolutionary Biology, Univer- of the Aplysia ER to steroid and related receptors of vertebrates and insects in the DNA- and
sity of Oregon, Eugene, OR 97403, USA. 2Section of ligand-binding domains. (B) Detail of sequences in the P box of the DBD, which mediates
Integrative Biology, University of Texas, Austin, TX recognition of the core response element on DNA; in the AF-2 activation function of the
78712, USA. ligand-binding domain, which is essential for ligand-activated transcription; and in the C-terminal
*To whom correspondence should be addressed. E- extension (CTE) of the protein, with the length of the CTE in amino acids indicated. Dots show
mail: [email protected] residues identical to those of Aplysia ER; an asterisk indicates the end of the coding sequence.

1714 19 SEPTEMBER 2003 VOL 301 SCIENCE www.sciencemag.org

 Amazonia 1492: Pristine Forest or Cultural Parkland?
Michael J. Heckenberger, Afukaka Kuikuro, Urissapá Tabata Kuikuro, J. Christian Russell, Morgan Schmidt, Carlos Fausto, and
Bruna Franchetto

Science, 301 (5640), • DOI: 10.1126/science.1086112

View the article online

https://www.science.org/doi/10.1126/science.1086112
Permissions
https://www.science.org/help/reprints-and-permissions

Downloaded from https://www.science.org at FU Berlin/CBF on October 17, 2021

Use of think article is subject to the Terms of service

Science (ISSN 1095-9203) is published by the American Association for the Advancement of Science. 1200 New York Avenue NW,
Washington, DC 20005. The title Science is a registered trademark of AAAS.
American Association for the Advancement of Science