Letters to the Editor
Ober C, Elias S, Kostyu DD, Hauck WW (1992) Decreased
fecundability in Hutterite couples sharing HLA-DR. Am J
Hum Genet 50:6-14
Oksenberg JR, Persitz E, Amar A, Schenker J, Segal S, Nelken
D, Brautbar C (1983) Mixed lymphocyte reactivity nonre-
sponsiveness in couples with multiple spontaneous abor-
tions. Fertil Steril 39:525-529
Schacter B, Weitkamp LR, Johnson WE (1984) Parental HLA
compatibility in parents of offspring with neural-tube de-
fects: evidence for a Tit-like locus in humans. Am J Hum
Genet 36:1082-1091
Address for reprints and correspondence: Dr. Carole Ober, Department of
Obstetrics and Gynecology, The University of Chicago, 5841 Maryland Avenue,
MC2050, Chicago, IL 60637. E-mail: carole@babies.bsd.uchicago.edu
© 1995 by The American Society of Human Genetics. All rights reserved.
0002-9297/95/5705-0032$02.00
Am. J. Hum. Genet. 57:1243, 1995
Reply to Ober
To the Editor:
Our citing of the reference by Kostyu et al. (1993) was
to give the readers an introduction to the work of Dr.
Ober and her colleagues, since it is important for the
general reader to identify the contributions of others
working in the field and to have one of their most recent
references. It was not our intent, nor was it appropriate
in this paper, to review this work in detail, since we
have done so in a variety of different contexts. Our
reviews and the evolution of the ideas presented in Jin
et al. (1995) are given in the reference section of that
paper, beginning with my 1983 review. In these publica-
tions, due credit is given to all in greater detail.
THOMAS J. GILL III
Department of Pathology
University of Pittsburgh School of Medicine
Pittsburgh
References
Gill TJ III (1983) Immunogenetics of spontaneous abortions
in humans. Transplantation 35:1-6
Jin K, Ho H-N, Speed TP, Gill TJ III (1995) Reproductive
failure and the major histocompatibility complex. Am J
Hum Genet 56:1456-1467
Kostyu DD, Dawson DV, Elias S, Ober C (1993) Deficit of
HLA homozygotes in a Caucasian isolate. Hum Immunol
37:135-142
1243
Address for reprints and correspondence: Dr. Thomas J. Gill III, Department
of Pathology, University of Pittsburgh School of Medicine, Scaife Hall, Room
716, Pittsburgh, PA 15261. E-mail: gill@med.pitt.edu
© 1995 by The American Society of Human Genetics. All rights reserved.
0002-9297/95/5705-0033$02.00
Am. J. Hum. Genet. 57:1243-1246, 1995
Our Tangled Heritage: Demographic History and
the Indian Caste System
To the Editor:
Mountain et al. (1995) have used mtDNA sequence vari-
ation to examine the genetic relationship among three
castes of India, the Havik, Mukhri, and Kadars, who
belong to the Brahmin (highest), Pancham (lowest), and
aboriginal castes (apparently ancient inhabitants of In-
dia), respectively. Phylogenetic analysis of the data re-
vealed an intermixing of lineages, which Mountain et
al. (1995, p. 984) attributed to either "extensive mixing"
of the three groups or the possibility that the "mtDNA
lineages . . . arose prior to the split" of the three castes.
They suggested that the cultural identification of the
populations included in the analyses were "inconsistent
with the genetic grouping." Mountain et al. found that,
in one case, five Mukhri sequences clustered with two
Havik sequences and that the Havik and Mukhri se-
quences were scattered "throughout the tree," indicating
some level of gene flow between the two populations.
Although the magnitude of gene flow (low, medium, or
high; sensu Slatkin 1985) among these populations is
not provided by Mountain et al., it must be high enough
to produce the homogeneity that obscured the branching
pattern of the lineages among the castes examined. The
results of the phylogenetic analysis appear to have sur-
prised Mountain et al., in the face of the sociocultural
background of the three castes.
Mountain et al. (1995, p. 988) do not provide an
approximate date as to when the split among these pop-
ulations might have occurred but suggest that the caste
society "crystallized fairly recently, -2,000 years ago."
This period coincides approximately with the time of
the codification of several of the dharma shastras (moral
codes), notably the laws of Manu (Basham 1989), which
have strongly influenced the social structure in Hindu
society. Mountain et al. seem to presume that such a
crystallized social structure with strict religious codes
may have not favored a significant amount of gene flow
among caste groups within the past 2,000 years. There-
fore, they inferred, on the basis of the phylogenetic anal-
ysis, that the lack of clustering of mitochondrial lineages
according to caste affiliation may be the result of mixing,
which predates the separation of populations. Because
1244
mtDNA is maternally inherited in humans, it is im-
portant to examine plausible cultural settings that might
have contributed to the exchange of maternal lineages
among the three castes, particularly since the migration
of Haviks into the northwestern region of Karnataka.
According to Slatkin (1987), gene flow is the genetic
change in populations that is due to movement of ga-
metes, individuals, or groups of individuals from one
place to another. Gene flow via recognized marriage is
a major component of the total gene flow observed in
modern human societies. However, both the union of
gametes through extramarital relationships and the
movement of individuals from one group into another
will also contribute to total gene flow. Such exchange
of genes among populations should yield the same ef-
fects on mitochondrial lineages as do marriages. The
Indian caste system is no exception to this rule. It is also
necessary to interpret the results in the context of the
cultural history of Karnataka in particular and southern
India in general. In the following, I have attempted to
show that the genetic and demographic patterns ob-
served by Mountain et al. may be due to (a) what I call,
"silent gene flow," which has occurred among the three
castes since the migration of Haviks into Karnataka,
and (b) the general influence of the agrarian system that
has prevailed in southern India during the past 1,000
years.
Sociocultural Patterns and Gene Flow
The Haviks migrated to the northwestern part of Kar-
nataka -1,300 years ago and settled in the Havik and
the Haiga provinces, which were part of the Kadamba
dynasty (Moraes 1931). The founders of the Kadamba
dynasty, who apparently allowed the Havik migration
into Karnataka, generally have been considered Brah-
mins, but it is not unlikely that some of them belonged
to the local aboriginal group, the "Nagas." After the
migration of Brahmins, however, even Dravidians, who
constitute the bulk of the ethnic groups in southern In-
dia, were received into the Brahminic fold (Moraes
1931). The Brahmins of medieval southern India moved
from place to place but were "not always descendants
of pure Brahmins" (Stein 1980). Conflicts between the
kings of the Kadamba dynasty and the kings who de-
scended from the local aboriginal castes are described
in the literature. For instance, around 1007-1008 A.D. a
major southern Indian ethnic group called the "Cholas"
invaded the Kadamba country and "slaughtered even
women, children, and Brahmans and taking their girls
to wife destroyed their castes" (Moraes 1931, p. 95).
The words "Cheras" (Kerala; Stein 1980) and "Cholas"
are the Dravidian equivalent of "Nagas" (Nanjundaiah
and Iyer 1928). The Cheras inhabited the western parts
of medieval southern India (Pillai 1969). Note that the
Kadar caste included in the study represents one of the
Letters to the Editor
aboriginal castes of Kerala. Interestingly, it has been
noted that the region of Karnataka studied by Mountain
et al. was ruled by an untouchable (Paraiah) king, was
later conquered by Brahmin kings, and seems to have
exchanged hands at least twice between the Kadambas
and the rulers of the untouchable class (Nanjundaiah
and Iyer 1928). Incidentally, many of the Havik Brah-
mins worship the same local female village deities (a
practice uncommon among Brahmins) that the agricul-
tural and other caste communities worship in this region
(Nanjudaiah and Iyer 1928), suggesting some degree of
relationship between the Haviks and the local inhabit-
ants. Furthermore, the "gotra" (exogamous clan; liter-
ally,"cow pen") system practiced particularly by Brah-
mins enforces exogamous marriage among various clans
of the Brahmin caste (Basham 1954). Marriages within
and among certain gotras are prohibited, but many
Brahmin clans have mixed gotras (Kosambi 1950).
Members of certain gotras have been known to admit
many local inhabitants freely into the Brahminic fold.
For instance, the Kashyapa gotra is "notorious for being
able from early days to absorb . . . aborigines who
wanted to become Brahmins" (Kosambi 1956, p. 110).
Interestingly, in Maharastra and Karnataka, the highest
number (82) of clans of Dravira Brahmins (of which
Haviks are a part) belong to the Kashyapa gotra (Sher-
ring 1872).
Mountain et al. suggest that the offspring of unions
between higher and lower castes move to the caste of
higher status; thus the progeny will always remain in
the higher caste, which may have also added to the pop-
ulation growth of Brahmins. The religious rules among
the Karnataka Brahmins allow this pattern of mobility
only in very rare and exceptional circumstances, such
as rape and abduction (Nanjundaiah and Iyer 1928).
Instead, the Manu's laws were upheld, in principle, by
all the dynasties that ruled over this region (Stein 1980).
Outside the gotra system, however, the religious codes,
including the laws of Manu, advocated two other sys-
tems of marriage for the Brahmin communities; they are
(1) hypergamy (anuloma, meaning "in the direction of
hair") and (2) hypogamy (pratiloma, meaning "against
the direction of hair"). In the former system, progeny
resulting from the union between a father from the
higher caste and a mother from the lower caste assumed
the mother's caste. For example, until recently, the Nam-
budiri Brahmins of Kerala married the Nayar women,
who belong to the fourth varna (Shudra caste group),
and they also maintained a matrilineal system. By con-
trast, in hypogamous marriage, children resulting from
the union of a Brahmin mother and a Shudra father
produced children whose status was lower than that
of either parent-a Chandala, who is an untouchable
(Basham 1954; Sagar 1975). A majority of the villages
donated to Brahmins during the medieval times, known
Letters to the Editor
as "Brahmadeya villages" (or land grants to Brahmins),
were multiethnic settlements consisting of cultivators
and members of other castes, including the untouchables
(the ideal Brahmadeya village had 18 castes). In these
communities, members of multiple castes lived together,
albeit in different quarters of the village complex (Stein
1980; Madhava 1991). Thus, in every way the Brahma-
deya villages were "woven into the texture of rural soci-
ety," in which Brahmins, in general, were not only ethni-
cally indistinguishable from their peasant contem-
poraries but were their neighbors (Stein 1980, p. 345)-
a pattern still found intact in many Karnataka villages.
In some medieval villages, however, a section was exclu-
sively reserved for individuals resulting from mixed
unions (Stein 1980). Nanjunadaiah and Iyer (1928)
stated that, although rules set out by various dharma
shastras for the Brahmins prohibited illegitimate unions,
"polygamy and prostitution continued to exist....
The wife guilty of adultery was generally repudiated,
and expulsion from caste usually followed" (Nanjun-
daiah and Iyer 1928, p. 356). These patterns suggest
that, although Brahmins and the untouchables are sepa-
rated by several caste levels in the hierarchical society,
as Mountain et al. have correctly noted, opportunities
existed, in the Brahmadeya villages and elsewhere in
medieval south India, for the collapse of these levels.
This may have facilitated the movement of individuals
from one caste to the other, through the narrow corri-
dors that connected the Indian caste society.
If 20 years is assumed to be generation length, as
suggested by Mountain et al., -50-70 generations have
elapsed since the immigration and subsequent expansion
of the Haviks in this region of Karnataka. As outlined
above, the prevailing social, political, and cultural con-
ditions during the past 1,000-1,250 years may have
provided enough opportunities for the three castes to
experience the magnitude of gene flow that the genetic
analysis suggests. Although the magnitude of gene flow
appears to be less than the suggested 3%, perhaps it
continued to occur in various forms and in variable
quantities over time, as suggested by Slatkin (1987).
Such occasional yet ongoing gene flow must be contrib-
uting toward the observed homogeneity among these
populations. Indeed, the results obtained by Mountain
et al. appear to be compatible with the observations of
Stein (1980, p. 5), who in his extensive work on southern
Indian agrarian societies, stated that "there is no validity
to the claim of a primordial ethnic separateness of Brah-
mans from most others of the southern peninsula."
Population Growth and the Agrarian System
Mountain et al. also imply that the Haviks may have
been engaging in agriculture for the past 2,000 years,
which may have contributed to their population growth.
On the contrary, although many Haviks were the own-
1245
ers of the Brahmadeya lands, the actual cultivation was
done by the lower castes (Kosambi 1956; Stein 1980;
Shivanna 1983; Madhava 1991), including the untouch-
ables. This practice changed gradually after the rebellion
of farmers, beginning in the 16th century, perhaps due
in part to the demand created by the European spice
traders (Madhava 1991). Therefore, Stein (1980, p. 68)
observed that, although Brahmins effectively dominated
the locals without cultivating skill or experience, "peas-
ant agriculture in south India was responsible for the
overwhelmingly large source of wealth to the society at
all levels." This agrarian society, supported by various
feudal systems that prevailed in medieval southern India,
may have favored a disproportionate distribution of re-
sources to the landowners, which in turn may have
added to their population growth. Clearly, population
growth of the Haviks may be interpreted as an overall
outcome of a more complex agrarian system that pre-
vailed in southern India, rather than as the result of
efforts of any particular caste under consideration.
Availability of excess resources is widely understood to
result in population growth in agrarian societies, as also
was noted by Kosambi (1956, p. 106), with special refer-
ence to Indian society: "as soon as people change from
food gathering to production, they breed rapidly, and
improved food supply leads to more children and more
maturity and longevity."
In conclusion, I believe that the genetic grouping
found by Mountain et al. appears to be more consistent
with the sociocultural history of the three castes than
Mountain et al. suggest. The nuclear DNA sequences
among Indian castes, which they wish to examine in the
future, should reveal patterns at least as homogenizing
as those reported in their paper. In general, agrarian
systems that prevailed in southern India may have influ-
enced the pattern of population growth of the members
of various caste groups.
Finally, it has been remarked that "India is a learning
laboratory for linguists, a museum for ethnographers
and anthropologists, a treasure trove for archeologists,
a nightmare for epidemiologists . . . India pulsates, vi-
brates, scintillates with such a plethora of human, ani-
mal, botanical, insect and divine life that no camera or
. . . pen, or cassette can fully capture" (Wolpert 1991,
p. 3). Is India a perpetual puzzle for evolutionary geneti-
cists?
DIDDAHALLY R. GOVINDARAJU
Department of Genetics
Yale University School of Medicine
New Haven
References
Basham AL (1954; reprint 1991) The wonder that was India.
Rupa, Calcutta
1246 Letters to the Editor

(1989) (Zysk KG [ed/ann]) The origin and develop- ancestral polymorphism (mtDNA lineages that arose
ment of classical Hinduism. Beacon, Boston prior to the separation of populations). Govindaraju ac-
Kosambi DD (1950) On the origin of Brahmin gotras. J Asiatic knowledges these two possibilities, then proceeds to ig-
Soc (Bombay) 26:21-80 nore the latter possibility, stating that our data indicate,
(1956) An introduction to the study of Indian history. "some level of gene flow between the two populations."
Popular Book Depot, Bombay
Madhava KGV (1991) Western Karnataka-its agrarian rela- We believe, however, that gene flow is only one of sev-
tions 1500-1800 A.D. Navrang, New Delhi eral possible interpretations of the observed data. While
Moraes GM (1931) The Kadamba Kula. BX Furtado & Sons, our data do not eliminate the possibility of gene flow,
Bombay particularly in the more distant past, they do suggest
Mountain JL, Hebert JM, Bhattacharyya S, Underhill PA, Ot- that high levels of recent gene flow are unlikely: we
tolenghi C, Gadgil M, Cavalli-Sforza LL (1995) Demo- observe little sharing of similar mtDNA types by Havik
graphic history of India and mtDNA-sequence diversity. Am and Mukri individuals (Mountain et al. 1995).
J Hum Genet 56:979-992 In our article we stated that the Havik have engaged
Nanjundaiah HV, Iyer LKA (1928) The Mysore tribes and in agricultural practices for hundreds or even thousands
castes. Mysore University, Mysore of years. We certainly did not imply that the Havik
Pillai KK (1969) A social history of the Tamils. Part 1. Univer- always worked the land themselves, as Govindaraju sug-
sity of Madras, Madras
Sagar SL (1975) Hindu culture and caste system in India. Up- gests. Such activity would make it difficult or impossible
pal Book Store, Delhi for the Havik to benefit maximally from an agrarian
Sherring MA (1872; reprinted 1974) Hindu tribes and castes, system. The Havik would be likely to gain more from
as represented in Banares. Vol 1. Cosmo, Delhi the practice of agriculture if they employed members of
Shivanna KS (1983) The agrarian system of Karnataka (1336- lower-ranking caste groups to carry out the cultivation.
1761). Prasaranga, Mysore University, Mysore This has been the practice, especially for crops such as
Slatkin M (1985) Rare alleles as indicators of gene flow. Evolu- rice (Campbell 1883). There is evidence, however, that
tion 39:53-65 the Havik themselves, both priests and laity, did carry
(1987) Gene flow and geographical structure of natural out the cultivation of a few special crops, including
populations. Science 236:787-792 spices and betel nuts. Buchanan (1870) noted such activ-
Stein B (1980) Peasant state and society in medieval south ity in 1801, as did Campbell (1883) later in the century.
India. Oxford University Press, Delhi We concluded (Mountain et al. 1995) that the
Wolpert AS (1991) India. University of California Press, Berke-
ley mtDNA sequences of two Indian caste groups suggest
that these groups have undergone dramatically different
Address for correspondence and reprints: Dr. Diddahally R. Govindaraju, demographic histories. While there may have been low
Department of Genetics, 333 Cedar Street, I-310 SHM, Yale University, New levels of gene flow between the two groups, in particular
Haven, CT 06510-8055. through extramarital relationships, such gene flow is
© 1995 by The American Society of Human Genetics. All rights reserved.
0002-9297/95/5705-0034$02.00 unlikely to have generated the observed pattern of pair-
wise nucleotide differences. It is more likely that the
differential allocation of resources during the agricul-
tural era enabled the Havik population to increase in
size while the Mukri population remained at a roughly
Am. J. Hum. Genet. 57:1246-1247, 1995 constant size. The observed patterns of mtDNA se-
quence diversity are consistent with such demographic
Reply to Govindaraju histories.
JOANNA L. MOUNTAIN,1 JOAN M. HEBERT,2
To the Editor: SILANJAN BHATTACHARYYA,3 PETER A. UNDERHILL,2
Govindaraju mentions a number of reasons why the CHRIS OTTOLENGHI,4 MADHAV GADGIL,5
magnitude of gene flow among Indian caste groups AND L. LUCA CAVALLI-SFORZA2
might be higher than we discussed in our recently pub- 'Department of Integrative Biology, University of
lished article (Mountain et al. 1995). As we stated California, Berkeley; 2Department of Genetics,
therein, some gene flow among caste groups may have Stanford University, Stanford; 3Calcutta; 4Paris; and
occurred. Without invoking several unrealistic assump- 5Centre for Ecological Sciences, Indian Institute of
tions, however, we cannot estimate the level of gene flow Science, Bangalore
on the basis of the available genetic data.
Govindaraju misinterprets our article at two points. References
We stated that the intermixing, in an inferred tree, of Buchanan F (1870) Journey from Madras through the coun-
mtDNA lineages from different caste groups can be at- tries of Mysore, Canara and Malabar. Higginbothams, Ma-
tributed either to gene flow among the groups or to dras