Colonization Models and Initial Genetic Diversity in the Americ ALAN Gi, FIN! Abstract. The mode and tempo of colonization of the Americas estub- Hished the initial pattern of continental genetic diversity. Despite a long histo ry of study, the process of settlement remains controversial in terms oF dite, rite. and pattern, While there iy agreement that Asia way the source popula Gon, several different models have heen proposed for the colonization process. A classic model postulates a rapid spread of population (blitz- Krieg”) from a small band of hunters entering through the corridor between the Continental ice sheets cirea 11,000 years m2, Colonization occurred ay a Save of expansion across the kind masses of North and South America, An alternative mode! envisions the original colonists initially limiting settlement ti the coustline, using boats, and entering the Amenieas at an earlier date, cir ey 12.500 0p. Range expansion wlong this linear habitat from North to South, Ameniew could be rapid without requiring population s Unental turation of entire con ons. These models have markedly different implications far netic variation among Na ve A mericans, The blitzkrieg colonization process would have generated multiple founder effeets leading to extreme lass of ge- etic Variation, Computer simulation of thiy model shows ly complete fixation in 30 generations. Simulttion of the coastal model, on the other band, requires less extn tains substan= hal genetic variability after 100 generations. Although with the coastal mod mie demographic assumptions and img cl continental interiors are occupied less rapidly than with the blitzkrieg mod el, the coastal model allows earlier entry and rapid expansion to the southern limits of the hemisphere Despite a long history of study, the process of settlement of the Western Hemi- sphere remains controversial in terms of date, rate, and pattern, Archacologists: and linguists, as well as biological anthropologists, have a strong interest in the mode and tempo of colonization, since cultural, linguistic. and biological diversi- ty was established initially by the founding groups of colonists, Over the years, models based on all three kinds of data—archacological site distributions and dates, linguistic patterns, and biological variables (from morphology t@ DNA)— Depeaimcnt of Aniluwpelogy. University of Cahora, Riv ersite, CX 92821 Huis tGvitigy ebwnaes 3902. TACO L pp Lae) Copyright 2002 Wayne Stake Uorverity Preys, Best, MicbiganaS20 1. F404) KEY WORDS, NATIVE AMERICANS. GENETIC DIVERSITY, COASTAL COLONIZATION, BLITZ KRIEG COLONIZATION MODEL, COMBL TER SIMEL TION,2/FIx have profiterated (e.g.. Anderson and Gillam 2000: Fiedel 200): Fladmark 1979: Greenberg et al. 1986; Martin 1973; Schurr 2000; Steele et al. 1998), Clearly, a comprehensive mode! would at least account for all observed pat- terns of variation for all three domains; that is, patterns of languages and genes should be consistent with the archaeological evidence for rates and dates of set: Uement. Moreover, the model should be compatible with demographic con- straints on rates of growth and mobilities, The aim of this paper is to examine two such models using computer simulation methods and to evaluate them in terms of their implications for levels of genetic variation among Native American popu- lations, Colonization Models Rapid Expansion (“Blitzkrieg”) Model. Until relatively recently, there seemed Lo be a consensus among archacologists that the human settlement of the Americas was accomplished by hunters crossing the Beringean land bridge from Asia at a time of lowered sea level during the [ate Pleistocene (Fiedel 2000). In order to move from Beringea to the Americas, these first colonists had to pass through a narrow “ice-free corridor,” the only land route not blocked by massive continental glaciers. These hunters, possessing a technology based on fluted (Clo vis) spear points. exploited the naive Pleistocene megafauna and rapidly expand- ed thorough the interior of the North American continent down to South America (Fiede! 2000), This rapid expansion model was based on the observation that human pop: ulations can grow very rapidly. particularly when colonizing unoccupied habitat (Birdsell 1957). Martin (1973) extended this reasoni (“blitzkrieg”) advance of the original colonizing Americans as they entered a new and very favorable environment populated by large herds of animals never before hunted by humans. Human discases endemic to the Old World tropics would have been lell behind, further increasing the Favorability of the environment. Under these circumstances, Martin (1973) assumed that the rate of population growth described by Birdsell for Pitcsirn Island, 3.4% per annum, would have been pos- sible, implying a population doubling every 20 years. Martin turther assumed an average population density of one person per square mile. 2 total population of approximately 10’ in the roughly 10’ square mile area of the Americas (not in- cluding glaciated areas), Thus, only 340 years (or 17 generations) “would be the minimum time needed for a band of 100 individuals to saturate the hemisphere” (Martin 1973. 970). He noted that even with the much lower growth rate of 14 percent annually, saturation would be reached after only 800 years Martin's model assumes that the colonization process began with a small band (N= 100) at the outlet of the ice-free corridor in Alberta, Rapid growth of the human population led to local extinction of the large herbivores, fueling a postulating a lightning wave of advance al an average rate of 16 kilometers per year moving ever south- ward. The highest density of humans would be along the wave front. with lowerColonization Models and Genetic Diversity | 3 numbers remaining in the zone depleted of large herd animals. Thus the initial colonizing wave would reach the southern limit of South America in tess than 1000 years. Coastal Model. Although many alternatives to the Martin model exist, much recent interest has been shown in a coastal colonization route (Fladmack 1979: Gruhn 1988), Rather than consisting of @ ring of expansion through the interior of the continents, inifial settlement would haye been along the linear coastal habitat with later spread into the interior along river channels. Dixon (1999, 254-255) has summarized the logic and evidence for the coastal model. He states that the initial colonization occurred circa 13.500 B.r, or curlicr and that these colonists were accomplished with boats, The colonization date is 2500 years earlier than the opening of the ice-free corridor, allowing more time for the spread of the initial colonists and avoiding the necessity for the © plosive population yrowth rates of the blitzkrieg model. Early dates from South ‘America suggest that people must have entered the hemisphere before deglacia ton. Archaeological evidence, including Paleoindian generalized subsistence base. are consistent with a coastal environment. Finally, there is wood evidence for boats and skillful navigation for perhaps the last 40,000 years (e.g., the colo: nization of Australia required watercraft al least as early as this date), Use of boats would have made transport of people and material easier, al Jowing Jong distances to be crossed, Furthermore, once colonies Were estab- lished, continuing contact Would have been eased, allowing for networks of mate choice and gene How A coastal economy based on hunting of marine mammals. fishing. and shellfish gathering, with relatively easy boats. may have Jecess ta rich resources provided by lowed more sedent ry setilements. Such fixed settlements along with boat use might have removed a major demographic impediment to rapid population growth, the need for wide birth-spacing due to ehild-carrying burdens (Lee 1980), Dixon (1999. 40) sees colonization occurring initially within similar envi- ronments of “megapatches.” with the long north-to-south coastal margin com prising (he zone of earliest colonization (see alse Rogers et al. 1990 for a similar megapaich model), A consequence of this pattern of settlement would be the rap- id deployment of colonists to the geographic limit of the hemisphere, since initial range expansion occurring down the linear sea coast would avoid the need to “fill up’ the continental interior before expanding southward. Genetic Imp! ns. The colonization process not only established popula- lions over the entire North and South American continents: 1 also established the initial pattern of genetic Variation among these colonies. We cannot know exactly what that pattern was sinee present day Amerind genetic variation was affected by processes of fission and fusion, migration and genetic exchange among groups subsequent a cofonization. as welll as postconquest amafganiation and severe de-4/ tix population (Crawford 1998). We can presume, however, that extreme depletion of genetic variability would be unlikely, since many genetic variants are widely spread through extant populations in both continents (Crawford 1998: O'Rourke etal. 1992), The problem with the blitzkrieg colonization model (repeated rapid bud- ding from an initial small ancestral population) is just such reduction of genetic variation. As Cavalli-Sforza (1986) points out, the expectation for among-popula- tion variation, Fy, alter repeated budding events is Fy=t-| | -12N), ay where N, is the effective population size at generation f, and T1 is the product over all generations. Based on Mattin’s (1973) estimate of an original colonizing population (WV) of 100 individuals, implying an effective size (N,) approximately one-third the census size, and @ growth rate allowing populations to double every generation, Cavalli-Sforza (1986) found that “after 20 cycles of budding and growing, which may take 1000 years, Fs, hecomes 0.855, a very high heterogeneity indeed, close ‘o the absolute maximum of 1.” He goes on to point out that observed Fys in Amerinds are closer to between 0, and 0.2, It should be noted that Cavalli-Sforza calls this “heterogeneity” but does not remark that such among-population diver- sity can arise from within-population homogeneity. That is. if all loci are random ly fixed among a set of populations (i.c., zero internal variation), Fy) will be very large (sce results below) Simulation Models Blitzkrieg Model. The first model simulates colonization based on rapid pop- ulation growth and budding using parameters suggested by Cavalli-Storza (1986); that is, initial population size of 100 and NV, = 32. A second territory is col- onized from this original population by a small founder group of eight individu- als. With rapid population growth, this colony soon buds a new splinter group of cight and colonizes the next territory. Using Cavalli-Storza's parameters, the bud- ding cycle is 50 years from initial split through population growth of the new colony to fission size. Populations double every generation (c. 25 years). The col- onizing process thus begins with an original colony (N, = 32) from which a splin- ter group of effective size 8 colonizes a new territory, This colony doubles to N, 16 in the first generation after colonization, then to N, = 32 in the second genera tion, whereupon the process continues with a third and subsequent territories be- ing colonized. This model was simulated for a time span of 30 generations, The initial population, N, = 32, began with allele frequencies of 0.5 at each of 10 neutral loci. In order to mimic founder effect in the new colonies, each budding eventColonization Medely and Genetic Diversity 15 generated 10 new allele frequencies. each a random sample of 2V, genes from the parent gene pool. As the new colony doubled for two generations, random inter- gencrational genetic drift was simulated similarly by using « normal approxima tion to the binomial distribution. Five replicate runs were made Leapfrog Colonization of Linear Habitat (Coastal Model), The sccond model simulates colonization in a linear habitat with population growth and bud- ding in the two populations at the limit of expansion. “Leapfrogging” (Anderson and Gillam 2000) may occur as colonisis from the population located behind the terminal group occupy the next empty territory. As the available territories fill, population growth ceases, but migration between adjacent populations continues: (in a linear stepping-stone Fashion), The simulation began with 10 neutral alleles with initial frequencies of 0.5 in a single population (/ 25), This population represented the first colonists in the tar nortttwest coast of North America, Population growth in the population (and subsequent colonies) was i = NL FAG — NaN ade (2) where a is the growth rate (c. 0,007 per year in these experiments) and Njju. 1 the maximum population size (250 in these experiments). Once population size reached 250, colonization of the next territory to the south occurred. Colonizing groups constituted a set proportion (10%) of the donor population (usually 25 persons). Gene frequencies in the colonizing group were determined randomly to simulate founder effect using a procedure identical to that used tn the previous model. Once a colony population was established, each generation it experienced interenerational random genetic drift and stepping-stone migration with its near- est neighbors. To mimic leapfrogging, colonization could occur from the next to the terminal population as well as from the final population in the array. ‘The program was run for 100 generations. sufficient at the rate of and colonization to occupy 100 territories in a linear array down the coastline Because population growth behind the terminal colony fueled colonization (leaplrogging), the wave of colonization spread rapidly along the array at rough- ly one population per generation, Assuming an average territory length of 100 kilometers. this rate approximates 100 km per 25 years (one generation) or + km per year, a rate slower than the blitzkrieg model but sufficient to reach Tierra del Fuego in a few thousand years. Results. Blitzkrieg Model. Figure | shows the cumulative percentage of the 10 loci for the five replicate runs (tot of 50 loci) that had become fixed after 30 simulated generations. Clearly, the rapid expansion model leads to severe depletion of ze- netic variation, After only 10 generations, neatly half of the loci had become6/ FIX 100 2 Ss 60 40 FIXATION PERCENTAGE 20 0 5 10 18 20 25 30 GENERATION Figure 1. Cumutative percentages of the |() loci fixed after 30 generations in the five replicate runs of the rapid expansion (“blitzkrieg”) model fixed: by generation 20, 82% of the loci were fixed; and by the end of the runs (generation 30), 94% of genetic variation had been lost, For three of the runs, all variation was lost before the end of 30 generations: the other two runs show 80% and 90% fixation. This extreme loss of variability occurs in approximately 750 years (assuming a 25-year generation length), or 15 cycles of budding, Cavalli- Sforza (1986) predicted extreme heterogeneity as measured by Fy, for this mod- el. The present simulations suggest that heterogeneity between populations is ac- tually a consequence of homogencity within individual populations, since loci are randomly fixed through repeated founder effect, Coastal Model. Figure 2 presents the distribution for 10 loci in five replicates (50 loci total) of the coastal model simulation, These Fervalues were calculated at the end of 100 generations; since the rate of expansion was one colony per gen- eration, they are based on variation among the linear array of 100 populations, Not surprisingly, given the stochastic nature of the colonization process, the Fy, values are relatively high; the average over all 10 loci and five runs was 0.06. Values ranged from 0.02 to 0.16. In contrast to the blitzkrieg model, for the coastal mode] no loci were fixed in any of the runs. Average gene frequencies for the 10 loci at the end of the 100 generation runs was approximately 0.5, the starting allele frequencies. Extreme valuey for the gene frequency averages ranged from a low of 0.253 to a high of 0.838. As indicated by the Fer values, initial genetic variation was maintained in all colony populations.Colonization Models and Genetiv Diversity 17 NUMBER OF LOCI 12 10 8 6 4 : HHA itt é ff Tt DY eee S 0 005 O41 0.15 0.2 0.25 FST Figure 2. Distribution of Fy values at the end of 100 generations (100 populations) for LD loci in the five replicate runs of the coastal model. The average F,, over all 10 loci and five runs Discussion ‘The goal of this study was to compare the implications for genetic variation of two colonization models for the Americas. These models have been shown to contrast sharply in their genetic effects, but they also differ in their demographic requirements and assumptions. [n some respects. they represent extremes along a range of models Demographically. the blitzkrieg model requires an extreme growth rate for the human population. While it may be possible for human populations to grow this quickly, it may not be likely for mobile foragers to achieve this rate. Lee (1980) pointed out a major impediment to high fertility among the !Kung San, He showed how the child-carrying costs of women in daily foraging lengthened birth spacing and reduced overall fertility. The very high mobility postulated for the expanding Palcoindian hunters would seem to impose the same costs as for the !Kung, arguing against the basic demographic requirement of the blitzkrieg Surovell (2000) has proposed an alternative model of forager mobility and fertility. He contrasts foraging populations that move base camps frequently with those that maintain base camps for longer periods. The first strategy moves camps to the food patches. while the second requires people to cover larger daily foraging distances to collect food and return it to camp. Calculating energetic costs under several different assumptions, Surovell concludes that foraging patterns of the first type are compatible with high fertility, thus bolstering the rapid expansion model.8/ FIN Although colonists of a new continent are potentially in a unique (or at least a very rare) siluation, such that there may be no relevant ethnographic compar- isons to their demography or ecology. members of all human populations must find mates, Ethnographically, low-density. mobile foragers maintain wide mating newworks (Fix 1999), implying extensive gene flow among local populations. The blitzkrieg model fails to consider how such mate pools might be maintained (e.g.. MacDonald 1999). Lt should also be pointed out that these results are based on one set of pa- rameter values, those provided by Cavalli-Sforza (1986) based on Martin (1973). Responding to criticisms of the Martin model, Whittington and Dyke (1984) showed by simulation that more reasonable assumptions were compatible with some of Martin’s claims, particularly the possibility of the extinction of the megafauna by human hunters, Indeed, more recently, Alroy (2001) has strength- ened the argument for anthropogenic extinction through a series of simulations taking into account a variety of ecological features. His best-fit model still re- quires a relatively high human growth rate of 1.66% per annum and does not ad- dress the problem of maintaining mate pools nor loss of human genetic variabili- ty. Predictably, reducing the growth rate of the human population slowed the rate of expansion, negating a key attribute of the Martin model The demographic and population structure assumptions of the coastal mod- el are less extreme. The longer time span for colonization allowed by the earlier entry date and the linear trajectory of movement mean that population growth rates need not be as high as in the blitzkrieg model. A modest 0,007 annual rate of increase was sufficient in the present experiments. Efficient long-distance trans- port by boat would facilitate visiting and mating links between settlements and al- low leapfrogging to new territories beyond terminal colonies. These networks of mating among established settlements are crucial for stabilizing gene frequency variances. Genetic divergence among new colonies arising through founder effects is counteracted by continuing gene flow. As shown in the simulations, locus fixation is retarded and genetic variability along the length of the coastal settlements is maintained. ‘These two models surely do not exhaust all possible colonization scenarios. For instance, Beaton (1991) considered alternatives to the Martin model. One such model was the “transient explorer” strategy in which population budding oc- curred al very low group size with long-distance relocation to totally different ecological zones. This strategy would lead to rapid population spread prior to sat- uration of inhabited territories. As he points out, however, “such a strategy also implies very law social connectivity, very high inbreeding coefficients, low fe- cundity, and relatively high likelihood of the extinction of new buds due to sto- chastic events” (Beaton 1991, 215), and. it might be added, loss of genetic varia- tion for the same reasons as the blitzkrieg model Beaton (1991) contrasts his transient explorer strategy with what he called “estate settlers,” where large buds from established populations (“estates”) relo- cate only a short distance away and stay within the same ecological zone. ThisColonization Models and Genetic Diversity 19 model implies “high social connectivity. relatively numerous potential breeding partners, relatively high fecundity. and a lower random extinction probability” (Beaton 199], 215). A consequence of this colonization scenario would be a mutch slower rate of colonization. The coastal model incorporates aspects of this estate Settler strategy while at the same time allowing rapid colonization of the coastal “megapatch.” Conclusions The simulation results confirm Cavalli-Sforza’s (1986) prediction of the ex- treme genetic effects of the rapid expansion model. Not only is Fer representing differences among populations, extreme, but so also is the complete loss of ge- netic variation within populations. These results do not negate the possibility of an interior route of colonization but simply point out the unlikelihood of the Mar- tin model as the mechanism of such a colonization. In contrast, the simulation results for the coastal model demonstrate that reasonably rapid colonization can be commensurate with maintenance of genetic variation both among and within local populations Numerous models have been devised to account for different aspeets of the colonization problem. A comprehensive model would be consistent not only with the archacologically known dates and distributions of sites but also with the lin- quistic, dental, morphological, and genetic data. Moreover, it should fit reason- able expectations for the population structure and demography of human groups in these ecological circumstances, Clearly, neither of the simulation models pre sented here meets all these requirements, nor do these Wwo models encompass the range of possible routes and population structures for the colonists, Nonetheless, these experiments demonstrate that the coastal but not the blitzkrieg model meets the crucial criterion of maintaining genetic variation among Native American populations. Received 28 May 2001; revision received 6 Sepiember 2001 Literature Cited Abroy. J. 2001, A multispecies overkill simulation of the end-Pleisiocene megataunal mass extinction, Seience 282:1893- 1806 Anderson, D.G., and .C. 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