Phylogeographic patterns of mtDNA reflecting the colonization of the Canary Islands

Ann. Hum. Genet. (1999), 63, 413–428

Printed in Great Britain

413

Phylogeographic patterns of mtDNA reflecting the colonization of the

Canary Islands

J. C. RANDO", V. M. CABRERA", J. M. LARRUGA", M. HERNA! NDEZ", A. M. GONZA! LEZ",

F. PINTO" H.-J. BANDELT#

"Departamento de GeneU tica, Universidad de La Laguna, E-38271 La Laguna, Tenerife#Mathematisches Seminar, UniversitaX t Hamburg, D-20146 Hamburg, Germany‘

(Received 25.5.99. Accepted 30.9.99)

Although the Canary Islands were settled by humans, possibly of Berber origin, as late as

2500 years ago, the precise course and numbers of early migrations to the archipelago remain

controversial. We have therefore analysed mtDNA variation (HVS-I as well as selected RFLP sites)

in 300 individuals from the seven Canary Islands. The distribution and variation across the islands

in a specific mtDNA clade of Northwest African ancestry suggest that there was one dominant initial

settlement process that affected all the islands, from east to west. This indicates that a certain

genetic affinity of present-day Canary Islanders to Northwest African Berbers mainly stems from

the autochthonous population rather than slaves captured on the neighbouring African coast. The

slave trade after the European conquest left measurable, though minor, traces in the mtDNA pool

of the Canary Islands, which in its majority testifies to the European immigration.

The Canarian archipelago is formed by seven

main islands, the nearest of which, Fuerte-

ventura, is about 100 km off the north-western

coast of Africa (Fig. 1). Archaeological data

(Tejera, 1992; Navarro et al. 1990) indicate that

these islands have been inhabited for about 2500

years. Settlements with different physical and

cultural traits were often separated either by

space or time on most islands (Bravo et al. 1983).

Although the precise origin of these aboriginal

settlers is still unknown, anthropometric mea-

surements from aboriginal mummies (Schwi-

detzky, 1963, 1975), archaeological data such as

alphabetic inscriptions on stones and pottery,

linguistic analogies in names of places (Tejera,

1992; Leo! n & Perera, 1996), and gene pool

Correspondence: Dr Vicente M. Cabrera, Departa-mento de Gene! tica, Universidad de La Laguna, E-38271La Laguna, Tenerife, Spain. Tel: 34 922 318350; Fax: 34 922 318311

E-mail: vcabreraull.es

sharing of rare alleles and haplotypes (Pinto et al.

1994; Cabrera et al. 1996) all point to a close

relationship with the Berber cultural complex

from Northwest Africa. After a period of only

occasional contact, it was as late as the fifteenth

century that the Europeans, mainly Spaniards,

invaded and with difficulty conquered the Ca-

nary Islands, beginning with Lanzarote in 1402

and finishing with Tenerife in 1496. Normans

conquered the islands of Lanzarote, Fuerte-

ventura, and El Hierro first, in a very fast

process and practically without fighting because

of the low number of aboriginal people there. In

La Gomera the occupation was initially seem-

ingly peaceful, but eventually led to the ex-

ecution of a large number of male aboriginals.

The conquest of Gran Canaria, La Palma and

Tenerife was even more dramatic, because of its

duration and the high number of battles, in the

course of which many aboriginal inhabitants

were killed, whilst others were enslaved in large

numbers (Sua! rez et al. 1988). After the conquest

414 J. C. R

Fig. 1. Geographic location of the Canary Islands.

Europeans, in the beginning mainly Spaniards

and Portuguese, settled in increasing numbers in

all seven islands. The demographic expansion in

the Canary Islands has been impressive. The

total aboriginal population in the fifteenth

century has been estimated at around 60000,

with less than one hundred inhabitants for the

small island of El Hierro (Macı!as-Herna! ndez,

1988). At present the Canarian census is approx.

1600000, and El Hierro, with 8000 inhabitants,

continues to be the least populated island. The

first slaves who were brought to the islands

(Lanzarote, Fuerteventura, and El Hierro in the

first instance) were captured on the neighbouring

north-westernAfrican coast (‘white ’ slave trade).

Later the Portuguese transported sub-Saharan

African slaves to Gran Canaria and Tenerife,

from where they were further sold to the other

islands (‘black’ slave trade). Noteworthy migra-

tions also took place in the opposite direction,

from the Canary Islands (to America), during the

periods of economic crisis in the 18th century.

The enigma of the aboriginal Canary Islanders

and the complexity of the migrational process

have been the main stimuli for carrying out

classical genetic studies on the present-day

Canarian population (Martell et al. 1986; Morilla

et al. 1988; Afonso et al. 1989; Pe! rez et al. 1991;

Larruga et al. 1992; Pinto et al. 1994; Moral et al.

1997; Esteban et al. 1998). Typically, these

papers address the admixture problem with refer-

ence to the European, North African, and sub-

Saharan African genetic contribution. By and

large, most previous analyses agree upon ad-

mixture proportions of 60–75% European, 20–

30% North African, and 5–10% sub-Saharan

African, although notable heterogeneity was

detected between islands, and even within the

main islands (Tenerife and Gran Canaria). A

pilot study of mtDNA (HVS-I) sequences

sampled in Tenerife (Pinto et al. 1996a), however,

proposed quite different percentages, which

raises the questions of (1) whether mitochondrial

DNA represents a meaningful marker for re-

constructing features of a complex settlement

history and (2) whether standard techniques

applicable for nuclear data can be adopted for

mtDNA studies without caveats.

The aim of this paper is to conduct a more

thorough analysis of mtDNA samples from all

seven islands (Lanzarote, Fuerteventura, Gran

Canaria, Tenerife, La Gomera, La Palma, and El

Hierro), which addresses the preceding two

questions as well as the following points: (i)

determining the numbers and courses of the

prehistoric migrations to the Canary Islands; (ii)

finding the geographic origin of these first

settlers ; (iii) differentiating between the genetic

input from these settlers and the much later

arrival of ‘white ’ slaves (who also may have been

of Berber origin) ; and finally (iv) estimating the

impact of the European colonisation on the

autochthonous mtDNA gene pool of the seven

islands.

Sampling

A total of 300 blood samples from unrelated

Canary Islanders have been analysed (Table 1),

Phylogeography of Canarian mtDNA 415

including the 54 sequences from Pinto et al.

(1996a), re-analysed in Rando et al. (1998). Only

those individuals whose maternal ancestry in the

Canary Islands goes back for two or three

generations have been selected; the birthplace of

the earliest known maternal ancestor was chosen

as the sample location. Voluntary donors were

asked for consent and anonymously filled in an

inquiry form about the birthplaces of all their

known ancestors.

Sequencing

Total DNA was isolated and PCR amplified as

described in Pinto et al. (1996a). The sequences

of 403 bp of the first hypervariable segment

(HVS-I) from position 15997 to 16399, according

to Anderson et al. (1981), were determined and

aligned. To gain more information for haplo-

group classification, several amplified segments

were digested with restriction endonucleases

(testing the sites 1715 DdeI, 3592 HpaI, 7025

AluI, 8249 AvaII, 8994 HaeIII, 10394 DdeI and

10397 AluI ) following Chen et al. (1995) and

Torroni et al. (1996). In two instances DNA was

amplified for hypervariable segment II (HVS-II)

with the primers of Vigilant et al. (1989) and

sequenced as in Pinto et al. (1996a). By direct

sequencing rather than using a mismatched

primer (Torroni et al. 1996), we determined the

nucleotide at position 12308 (in order to decide

upon haplogroup U status). One sequence from

El Hierro was checked for heteroplasmy at

position 16129, following the method of Bendall

et al. (1996).

Phylogeographic analyses

We build upon the phylogenetic analyses

performed in Richards et al. (1996, 1998), Torroni

et al. (1996) and Macaulay et al. (1999) for

European mtDNA data and in Chen et al. (1995)

and Watson et al. (1997) for African mtDNA

data, which allow the assignment of most

European and African mitochondrial sequences

to basal clusters}haplogroups, characterised by

‘signature’ HVS-I and}or RFLP motifs (re-

ferring to the 14-enzyme system). The sequences

are first assigned to the three RFLP super-

haplogroups L1, L2 (Chen et al. 1995) and L3

(Watson et al. 1997), which together cover all

RFLP haplotypes obtained so far. The sub-

Saharan African sequences of the Afro-Eurasian

super-haplogroup L3 (defined by ®3592 HpaI)

are further grouped into the clusters L3a*

(®10394 DdeI, but apparently lacking any

markers for the familiar Eurasian haplogroups),

L3b (10084 TaqI), L3d (®8616 MboI), L3e

(2349 MboI), and L3* (comprising the un-

assigned sequences within L3), as described in

Rando et al. (1998). In order to clarify the cluster

status of the sequences under study we apply

partial RFLP typing, especially in those cases

where the HVS-I status alone did not allow

unambiguous cluster assignment. HVS-I se-

quence types are reported here by listing the

transitions relative to the Cambridge Reference

Sequence (CRS; Anderson et al. 1981) but

omitting the ‘16’ prefix: for instance, the type

172–219 refers to sequences which differ from

CRS exactly at nps 16172 and 16219 by tran-

sitional changes; other kinds of mutations are

indicated by suffixes (see Table 1).

To trace the origins of migrations, we focus

on those clusters of the mtDNA phylogeny

(Macaulay et al. 1999) which are diagnostic for

certain geographic regions within appropriate

time horizons (Richards et al. 1998). When faced

with rather recent migration events, particular

emphasis is put on the analysis of shared

(diagnostic) sequence types between regions

(Horai et al. 1996). To accomplish this, the Can-

arian sequences have been compared to 217 pub-

lished sequences from the Iberian peninsula (IP)

and to 255 published sequences fromNorth Africa

(NA); see Table 1. The IP sequences are mainly

from the northern part of the peninsula, whereas

the NA pool is geographically somewhat more

balanced (as sampled from Algeria, Morocco,

West-Sahara, Mauritania, and even including

Tuareg sequences). The scarcity of sequences in

the IP pool which are southern Iberian is, in a

way, an advantage for admixture analyses

because the southern region is expected to have

been affected by immigration from Africa, either

416 J. C. R

Table 1. Mitochondrial DNA variation in the Canary Islands: classification, distribution, and

matches with mtDNA sequences from the Iberian Peninsula and North Africa. Sequence types for

HVS®I are described by listing the variant positions minus 16000 relative to CRS; the variants

indicate transitions unless a suffix (A, G, C, T or d ) specifies a transversion or a deletion; superscript

(h) indicates heteroplasmy; additional information outside HVS®I refers to specific restriction sites or

nucleotide positions. A prefix triangle _ indicates a probable Canarian founder type; an attached

exclamation mark signifies high probability, whereas a question mark expresses rather low probability;

sequence types with prefix y are likely descendants of founder types. Cluster notation follows

Richards et al. (1998) and Rando et al. (1998), with corresponding motif in brackets. Sample locations

are: L,¯ Lanzarote; F,¯ Fuerteventura; C,¯ Gran Canaria; T,¯ Tenerife; G,¯ La Gomera;

P,¯ La Palma; H,¯ El Hierro. The two mtDNA pools IP and NA screened for matches (h) with

Canarian sequence types comprise 217 sequences (IP: Galicians$, Portuguese%, various Spanish

populations% excluding Basques) and 255 sequences (NA: Berbers from Algeria% and Morocco&, other

Moroccans&, Mauritanians&, West®Saharans&, Tuareg'), respectively; matches are scored within nps

16069–16370, the A to C transversion at np 16183 being disregarded

Sequence Type Population MatchHVS-I (16...) Additional sites L F C T G P H Total IP NA

L1b (126 187 189 223 264 270 278 311)126 187 189 223 264 270 278 311 . . 1 . . . 1 2 h126 187 189 223 264 270 278 293 311 362 1 . . . . . . 1104 187 189 223 270 278 289 293 311 . . 1 . . . . 1093 126 187 189 223 264 270 278 293 311 . . . . 1 . . 1126 183T 187 189 223 264 270 278 311 . . . . . . 1 1

L2 (223 278 390)223 278 294 309 390 . . 1 1 . . . 2 h189 192 269 278 294 309 390 . . 1 . . . . 1093 189 192 223 260 278 294 309 390 . . . 1 . . . 1

L3* (223)041 223 239 ®8249 AvaII, 8994 HaeIII,

10394 DdeI, ®10397 AluI1 . . . . . 1 2

209 223 311 10394 DdeI, ®10397 AluI . . . 1 . . . 1 h h169 193 195 223 243 261 ®8249 AvaII, 8994 HaeIII,

10394 DdeI, ®10397 AluI. . . 1 . . . 1 h

L3a* (223, ®10394 DdeI, ®10397 AluI)092 223 278 294 1715 DdeI, ®3592 HpaI,

®10394 DdeI, ®10397 AluI. . . . . . 1 1

L3b (124 223 278 362)223 278 311 362 . . 1 . . . . 1124 183C 187A 189 223 278 362 . . . 1 . . . 1

L3d (124 223)124 223 256 311 . . . . 3 . . 3

M1 (129 189 223 249 311, 10394 DdeI,10397 AluI)129 185 189 223 249 311 10397 AluI . 1 . . . . . 1 hA (223 290 319)111 209 223 290 319 362 . . . . . . 1 1

C (223 298 327)223 298 325 327 . . . 1 . . . 1H/U* (CRS)_?CRS 4 5 8 14 1 9 3 44 h h311 . . 1 1 1 1 . 4 h h111 . . . . 3 . . 3189 1 . . 1 . . . 2 h129 2 . . . . . . 2 h220 . 1 . 1 . . . 2263 . 2 . . . . . 2


Table 1 (cont.)


176 . . 1 1 . . . 2 h354 . . 2 . . . . 2278 . . . 1 1 . . 2 h051 162 . . . 1 1 . . 2172 . . . 1 . . 1 2 h085 1 . . . . . . 1129 316 1 . . . . . . 1167 . 1 . . . . . 1188 . 1 . . . . . 1129 189 . 1 . . . . . 1 3093 209 . 1 . . . . . 1280C 293 . 1 . . . . . 1086 134 . . 1 . . . . 1218 328A 362 . . 1 . . . . 1 h119 . . 1 . . . . 1256 . . 1 . . . . 1354 355 . . 1 . . . . 1126 . . . 1 . . . 1248 . . . 1 . . . 1248 294 . . . 1 . . . 1291 . . . . 1 . . 1093 183C 189 293 . . . . . 1 . 1162 . . . . . 1 . 1 h290 . . . . . 1 . 1320 . . . . . 1 . 1209 261 304 . . . . . 1 . 1362 . . . . . 1 . 1336 . . . . . . 1 1(pre-)V (298)298 . . 2 2 . . . 4 h h291 298 . 1 . . . . . 1189 259G 298 . . . 1 . . . 1

H (CRS, ®7025 AluI)_!260 ®7025 AluI 1 2 . 1 . . 3 7 hy042 260 ®7025 AluI 1 . . . . . . 1 hy189 260 ®7025 AluI . . . 1 . . . 1y179 260 ®7025 AluI . . . . . 1 . 1189 257 356 ®7025 AluI . . . 3 . . . 3183C 189 257 356 ®7025 AluI . . . 2 . . . 2189 356 ®7025 AluI . . 1 1 . . . 2183C 189 356 ®7025 AluI . . 1 . . . . 1107 187 268 ®7025 AluI, 12308A 1 . . . . . . 1172 174 304 ®7025 AluI, 12308A 1 . . . . . . 1 h111 129 179 256 342 ®7025 AluI, 12308A . . 1 . . . . 1

U* (CRS, 12308G)_129 169 172 189 12308G 1 . . . 1 1 . 3y086 129 169 172 189 12308G . 1 . . . . 2 3y086 129 169 172 189 294 12308G . 1 . . . . . 1y107 129 169 172 189 12308G . . . . . 1 . 1

U2 (129C 189, 12308G)051 129C 183C 189 362 . . . 1 . . . 1051 092 129C 183C 189 . . . . . 1 . 1

U4 (356, 12308G)356 7025 AluI . . . 1 . . . 1 h

U5 (270, 12308G)192 270 . 4 . . . 1 1 6114A 192 256 270 294 . . . 2 . 1 . 3189 192 270 1 1 . . . . . 2 h h189 270 . . . 2 . . . 2 h270 1 . . . . . . 1

418 J. C. R

Table 1 (cont.)


093 224 270 12308G 1 . . . . . . 1256 270 311 1 . . . . . . 1256 270 . . . 1 . . . 1 h163 189 270 . . . 1 . . . 1172 183C 189 270 274 311 325 357 . . . . 1 . . 1074 189 192 270 . . . . . 1 . 1

U6a (172 219 278, 12308G)092 172 219 278 1 . . . . . . 1172 219 278 . . 1 . . . . 1 h172 183C 189 219 278 12308G . . . . . . 1 1 h h

U6b (172 219 311, 12308G)_!163 172 219 311 12308G 2 2 2 3 7 8 . 24_!092 163 172 219 311 12308G . 1 2 1 5 . . 9y163 164T 172 219 311 1 . 1 . . . . 2 hy048 163 172 219 311 12308G . 1 . . . . 1 2y129 163 172 219 311 12308G 1 . . . . . . 1

y092 129h 163 172 219 311 12308G . . . . . . 1 1

K (224 311)093 224 311 . . 3 . . . 2 5 h h093 189 224 311 . . . 2 . . . 2048 162C 192A 224 311 . . . 2 . . . 2188 224 311 1 . . . . . . 1189 224 311 . . . . . . 1 1224 311 . . 1 . . . . 1 h h

J* (069 126)_?069 126 . . 1 1 1 1 2 6 h h069 126 311 1 . . . . 3 . 4069 126 145 . . 2 . . . . 2069 126 319 1 . . . . . . 1069 126 150 1 . . . . . . 1069 126 311 352 . . . . 1 . . 1

J1 (069 126 261)069 126 145 231 261 1 . . . . 1 1 3 h069 126 261 . . . 1 . . . 1 h069 126 163 261 . . . 1 . . . 1

J2 (069 126 193)069 126 193 278 . . . 1 . . . 1 h

T* (126 294)126 294 296 304 . . . 3 . 3 . 6 h_126 292 294 1 1 . 1 . . . 3_126 220 292 294 2 1 1 . . . . 4y037 126 292 294 . 2 . . . . . 2y126 234 292 294 . . . 2 . . . 2y126 220 265 270 292 294 . 1 . . . . . 1126 294 296 . . . . . 1 1 2 h126 292 294 296 . . 1 . . . . 1 h126 147 294 296 297 304 . . 1 . . . . 1294 304 . . . . 1 . . 1126 240T 241 294 304 . . . . . 1 . 1126 145 294 296 304 . . . . . 1 . 1126 223 294 296 304 . . . . . 1 . 1126 296 304 . . . . . 1 . 1126 153 274 293 294 296 . . . . . . 1 1

T1 (126 163 186 189 294)126 163 186 189 284 294 . . . . 3 . 1 4126 163 186 189 294 . 2 . . . . . 2 h h126 163 186 189 249 294 311 . . . 2 . . . 2126 163 184d 186 189 294 . . . 1 . . . 1126 163 186 189 261 294 . . . . . 1 . 1


Table 1 (cont.)


I (129 223)129 172 223 291 311 391 . . . 1 . . . 1129 172 223 311 391 . . . . . . 1 1129 223 259 261 391 . . . . . . 1 1

W (223 292, 8249 AvaII, ®8994HaeIII)223 292 295 8249 AvaII, ®8994 HaeIII . . . . . 2 . 2 h223 292 8249 AvaII, ®8994 HaeIII . 1 . . . . . 1 h

X (189 223 278, ®1715 DdeI, 00153G)189 223 255 278 ®1715 DdeI . . 2 2 . 1 . 5 h189 223 278 1715 DdeI, 00153G" . . . . 1 1 . 2 h183C 189 223 255 278 1715 DdeI, 00153G# . . . . . 1 . 1 h

Total 33 36 45 73 33 50 30 300

" The full HVS®II type relative to CRS is 00073–00146–00153–00256–00263; the transition at np 00256 causes again of 255 RsaI; this site in conjunction with 1715 DdeI has previously been observed in an X sequence type fromthe Near East (Macaulay et al. 1999).

# The full HVS®II type relative to CRS is 00073–00153–00195–00225–00227–00263; the HVS®I&II type is thusidentical (ignoring length polymorphisms in the C®runs) to an X sequence type from Finland (Brown et al. 1998).

$ Salas et al. (1998).% Co# rte-Real et al. (1996).& Rando et al. (1998).' Watson et al. (1997).

through the Islamic conquest or slave trade. We

then take those mtDNA types found in the

Canary Islands as diagnostic for Iberian or North

African ancestry, respectively, which either have

exclusive matches with one region but not the

other or belong to region-specific clusters. The

relative maternal contribution of these two

regions to the Canarian mtDNA pool (as repre-

sented by the sample) is linearly extrapolated

from the diagnostic proportion. The amount of

sub-Saharan African ancestry may be estimated

directly from our classification of sequence types

(with only minor correction accounting for earlier

gene flow to North Africa and Iberia) inasmuch

as almost all sub-Saharan African sequences can

easily be distinguished from autochthonous

European or North African sequences.

The age of clusters is calculated as the mean

distance (i.e. average number of scored mu-

tational steps) ρ from inferred ancestral sequence

types (Morral et al. 1994) and converted into time

by assuming that one transition within np

16090–16365 corresponds to 20180 years (For-

ster et al. 1996). For this calibration, transitions

outside this scoring frame, transversions, inser-

tions and deletions are thus disregarded. The

standard deviation σ of the estimator ρ is

approximated (with a Poisson process) from

below by (ρ}n)"/# where n denotes sample size.

This approximation is satisfactory when most

pairs of sequences in the sample coalesce close to

the most recent common ancestor of the sample.

Such a situation may be expected with an initial

colonisation event or a rapid spread of an

intruding population over a large area.

For sample comparisons, nucleotide diversity

is calculated as the mean pairwise distance per

position within a sample, using the MEGA

program (Kumar et al. 1993), and heterozygosity

(1®Σixi#) is computed by considering all distinct

mtDNA types formally as alleles of a gene.

Classification of the Canarian mtDNA sequences

Table 1 lists the 138 different haplotypes

obtained from the 300 sampled sequences ac-

cording to haplogroup and refined cluster status,

which can be predicted by HVS-I motif alone or

in conjunction with specific RFLP sites (see

Material and Methods). Fifteen sequences fall

into the sub-Saharan African-specific clusters

420 J. C. R

L1b, L2, L3b, and L3d; another five sequences

are subsumed under L3a* or L3* inasmuch as

they lack any further apparent markers for

allocation to known Eurasian or African mtDNA

clades; we regard them as of sub-Saharan African

origin by default (despite the fact that one of

them, the rather enigmatic type 169–193–195–

223–243–261, matches a Galician sequence; Salas

et al. 1998). Three sequences belong to the Asian

super-haplogroup M. One of them bears a

familiar HVS-I motif (129–189–223–249–311)

that can be spotted around the Mediterranean

area at low frequency and in the Nile Valley at

7% (Krings et al. 1999). The other two sequences

are members of haplogroups A and C but bear

the American-specific mutations at nps 16111,

16362 (for A) and 16325 (for C), respectively

(Forster et al. 1996). The C sequence constitutes

the founder type of C in America, but the A

sequence bears an additional transition at np

16209, which matches a sequence from a Colom-

bian individual (Horai et al. 1993). The ap-

pearance of Native American mtDNA sequences

in the Canary Islands can be explained as a result

of (i) the slave trade which also brought some

Amerindians to the islands in the 16th century

(Lobo Cabrera, 1979) or (ii) the return of

Canarian emigrants to the Caribic (and South

America) in the 18th and 19th centuries (Castel-

lano & Macı!as, 1997). All the remaining

sequences (92%) are virtually subsumed by the

familiar nine European}West Asian haplogroups

(Torroni et al. 1996).

One of the mtDNA haplogroups omnipresent

in Europe, U, has an early offshoot with an

aberrant geographic distribution: U6, charac-

terized by transitions at nps 16172 and 16219

relative to CRS (the root HVS-I type of U as well

as H), is found at considerable diversity and

frequency in Northwest Africa, less frequently in

the Sahel zone, and only sporadically in neigh-

bouring areas. U6 itself can be subdivided into

two subgroups, which we name here U6a and

U6b; the former is defined by a transition at np

16278, whereas the latter is described by a basal

(transitional) change at np 16311 (see Fig. 2 of

Rando et al. 1998). Within U6b a subsequent

transition at np 16163 (‘Canarian motif ’) gave

rise to the cluster U6b1, which is restricted to the

Canary Islands – except for two singular occur-

rences (of types sharing an additional trans-

version with two Canarian sequences) in Galicia

and Portugal.

Founder mtDNA types

The geographic distribution of the U6b types

suggests that those Canarian (U6b1) sequences

bearing the transition at np 16163 and not found

in the continental samples were carried to the

Canary Islands by the first Neolithic settlers. It

is rather unrealistic to assume that no other

mtDNA sequences would have entered the

islands with the first migration(s). In order to

detect major founder mtDNA types we stipulate

that such a type would have been distributed

across several islands. In contrast, later arrivals

of mtDNA types (through slave trade) are

expected to have affected the seven islands

differentially. Specifically, we employ the fol-

lowing initial criterion as an ad hoc approach: a

type qualifies as a potential founder if it is

present in either & 4 islands, or in three islands

such that some one-step descendant which is

absent in Europe is sampled in yet another

island; if in the latter case this descendant itself

appears in three islands, we regard it as a

potential founder too. This relaxed majority

rule accounts for potential drift effects and

postulates that a fairly widespread one-step

descendant of a major founder type rather

constitutes a minor founder type than an

autochthonous variant. Anticipating North Afri-

can origin of the first wave(s) of settlers, a second

(optional) criterion would come into play, which

requires the type either to belong to an autoch-

thonous North African cluster or to be no further

than one mutational step away from a sampled

North African sequence. Finally, we need to rule

out that a frequent mtDNA type which was

brought to the Canary Islands several times in

the course of the European immigration would

be inferred as a founder type. Therefore, the final

criterion to be passed is that the type in question

either be rare in Europe or, when abundant in


the European mtDNA pool, exceed the expected

relative frequency within the total Canarian

mtDNA sample with an anticipated Iberian

fraction of about 60%.

Nine sequence types from Table 1 meet the

first criterion (cluster assignment given in

brackets): (i) 163–172–219–311 (U6b), (ii) 092–

163–172–219–311 (U6b), (iii) 260 (H), (iv) 129–

169–172–189 (U*), (v) 126–292–294 (T*), (vi)

126–220–292–294 (T*), (vii) CRS (H}U*), (viii)

069–126 (J*), and (ix) 311 (H}U*). Types (i) and

(ii) belong to the autochthonous North African

cluster U6; types (iii), (vii), (viii), and (ix) are

present in North Africa, and the three remaining

types are closely related to North African types:

an immediate ancestor of type (iv) and one-step

descendants of types (v) and (vi) (assuming a

back mutation at np 16294) are found in North

Africa. Thus, all nine types meet our (optional)

second criterion. As to the final criterion, the first

six types are absent or rare in Europe, but the

last three are abundant. In order to reconstruct

relative frequencies of the three types (CRS, 069–

126, and 311) in a hypothetical Iberian source

population (as a proxy for the true European

contribution), we pool the four Spanish popu-

lations (North Spain, Andalusia, Catalonia, and

miscellaneous Spain) from Co# rte-Real et al.

(1996) for one fraction and pool the Portuguese

of the latter data set with the Galicians from

Salas et al. (1998) for a second fraction; we let the

former fraction contribute 2}3 to the relative

frequencies and the latter one 1}3. If 180

sequences in our total Canarian sample came

from this composed pool, then one would expect

32–33 CRS sequences, 2–3 of type 069–126, and

6 of type 311. Comparing these numbers with the

observed numbers in the sample (44, 6 and 4,

respectively), we conclude that type 311 does not

meet our third criterion, but CRS and 069–126

do. The fact that the CRS constitutes by far the

most frequent type in the mtDNA sample of the

Moroccan Berbers additionally fosters the idea

that the CRS could have been carried to the

islands by the first migration(s). Summarising,

we would thus predict 6–8 major founder

sequences which were passed on to the contem-

porary Canarian mtDNA pool. There are ad-

ditional types in the Canarian sample which

likely are of Northwest African origin; for

example, the three U6a sequences. These, and

seven further sequences among those which

match North African but not Iberian sequences

(see Table 1), could have arrived in the Canarian

Islands at later times, in particular with the

‘white ’ slave trade from the north-western

African coast.

The types (i)–(vi) listed above, for which we

tentatively predict founder status, are indicated

in Table 1 by the prefix _. The sequences that

apparently descended from them (by one or two

mutations) are marked with y; the sequence

126–292–294–296 though is unmarked as it

matches an Iberian sequence and moreover could

have descended by a parallel mutation from a

sequence of type 126–294–296. The types (vii)

and (viii) (marked with _?) may also have

contributed founder sequences according to our

analysis, but it is impossible to decide precisely

how many of these sequences and the numerous

one-step derivatives actually descended from a

true founder sequence. Leaving these sequences

aside for an age estimation, we count altogether

69 sequences (marked with _!, _, or y), which

we refer to as the pioneer pool. When we allocate

each of these sequences to its nearest founder

type, we score a total of nine transitional steps

plus half a step for the heteroplasmic event

within nps 16090–16365. Thus, the average

distance ρ to the six founders equals 9.5}69. This

corresponds to an age of 2800³900 years (see

Materials and Methods), which is perfectly

compatible with the archaeological date for the

first human settlement in the Canary Islands.

The distribution and diversity of U6 or the

pioneer pool are quite uneven across the seven

islands. La Gomera has by far the highest

percentage (36%) of U6, which however is

represented by only two types; next comes La

Palma with a single type (16%); see Table 2. The

apparently reduced mtDNA diversity in these

two islands is also reflected in the overall mtDNA

heterozygosity as well as the heterozygosity

within the pioneer pool. The highest pioneer pool

422 J. C. R

Table 2. Diversity within the populations of the Canary Islands. Populations are coded as in Table 1

Population HeterozygosityNucleotidediversity Frequency of U6

Pioneer poolheterozygosity

L 0.9477 0.01296 0.152 0.86F 0.9306 0.01184 0.111 0.89C 0.9338 0.01273 0.133 0.72T 0.9407 0.01177 0.055 0.79G 0.8815 0.01412 0.364 0.56P 0.9152 0.01279 0.160 0.45H 0.9389 0.01597 0.100 0.69

heterozygosities (with intermediate U6 frequen-

cies) are observed in Lanzarote and Fuerte-

ventura, the two islands closest to the African

coast. This pattern likely reflects an initial

settlement process via island hopping (as de-

scribed by stepping stone models), starting in the

easternmost islands and ending in the west-

ernmost islands (with the peculiarity of El

Hierro; see below).

Impact of the European colonization on the

Canarian mtDNA pool

The pioneer pool within the total sample

probably does not quite exhaust the actual pool

of those sequences that descended from North-

west African sequences. In order to assess the

relative contributions of the maternal input from

Northwest Africa and Europe, we aggregate the

available HVS-I sequences from the Iberian

peninsula (IP) and from Northwest Africa (NA)

into two pools, as described in the footnote to

Table 1. Then 10 sequence types from the

Canarian sample are shared with both IP and

NA, whereas 21 types match IP sequences and 10

match NA sequences exclusively. Taking sam-

pling frequencies into account, the proportion of

exclusive sequence matches with the IP pool

versus the NA pool is 39:21. This proportion,

however, could possibly deemphasise the African

contribution since U6b does not yield any NA

matches at all. For another estimation, we would

aim for directly reconstructing the Northwest

African part of our sample. This should embrace

the pioneer pool as well as those 15 sequences of

the CRS and 069–126 types which we have

tentatively predicted in the above founder

analysis. If ancestors of these sequences indeed

arrived in the islands as early as 2500 years ago,

then we would expect about two 1-step deri-

vatives. Further, the three U6a sequences should

be included, as well as the remaining nine

sequences with exclusive NA matches, plus one 1-

step derivative (an L1b sequence from El Hierro).

Then in total we count 99 sequences, constituting

33% of the sample, with a tentative ancestry in

Northwest Africa. We therefore believe that

25–40% is a realistic range for the Northwest

African contribution to the Canarian mtDNA

sample. The sub-Saharan African mtDNA input

via slave trade makes up no more than about 5%

of the total sample, taking into consideration

that in present Northwest African populations at

least 4% of the mitochondria are of sub-Saharan

African origin (Rando et al. 1998). A minute

portion of the sample, about 1%, is of Amer-

indian descent. Thus, the vast majority of the

mtDNA sequences have recent European an-

cestry, which testifies to the profound impact of

the European immigration to the Canary Islands

in the course of the last centuries.

As can be seen from Table 1, the IP and NA

matches are apparently not evenly distributed

across the seven island samples. In order to

assess the influence of the European immigration

to the islands differentially, we will focus on

mtDNA types that are taken to be diagnostic for

either the Iberian peninsula or (Northwest)

Africa. We regard the mtDNA types from

clusters L1, L2, L3a*, L3b, L3d, and L3* as

diagnostic for sub-Saharan African origin and

the pioneer pool together with U6a as diagnostic

for Northwest Africa. Diagnostic for the Iberian

peninsula are haplogroups I, W, X, and U2,


Fig. 2. Relative occurrences of mtDNA types which are diagnostic for the Iberian or African fraction of theCanarian mtDNA pool; the diagnostic types encompass 40% (Gran Canaria and Tenerife) to 58% (LaGomera) of the sampled sequences; population codes are as in Table 1; the left points (*) of the segmentsrepresent North African input, and the right points (E) represent both North and sub-Saharan Africaninput; the stippled line partitions the islands into two groups with different colonization history.

which are virtually absent in Berber populations.

From the remaining types in the total sample,

the exclusive NA matches and IP matches are

further added to the diagnostic pools for North-

west Africa and the Iberian peninsula, respect-

ively. Thus, altogether 141 sequences (47%) can

be seen as diagnostic this way. The percentages

for the three diagnostic portions of the seven

island samples can be displayed in 3-dimensional

space, which in Fig. 2 is projected to two

dimensions, highlighting the contrast between

Iberian and African input. There appears to be a

sharp contrast between the samples from Lan-

zarote, Fuerteventura, La Gomera, El Hierro on

the one side, and Gran Canaria, Tenerife and La

Palma on the other: the former have quite a

pronounced African affinity (and a relatively low

Iberian affinity), whereas for the latter samples it

is the other way round. This marked division is

even seen in the relative proportions of the CRS

in the samples: in the latter it occurs at more

than 17% but in the former at less than 14%

frequency. This division then seems to reflect the

different colonisation history: the conquest of

Gran Canaria, Tenerife and La Palma was more

disastrous to the aboriginal population than for

the other four islands that were conquered first.

Although El Hierro is the westernmost island,

it seems to have close genetic bonds with

Fuerteventura and Gran Canaria, in view of

several sequence matches. To quantify the

sharing of infrequent types, we calculated the

probabilities of sequencematches between islands

restricted to those types that are shared by at

most three islands. The obtained values were

rounded down to multiples of 2.5 and visualised

in a multigraph (Fig. 3). The pronounced genetic

connection of El Hierro with the other islands,

especially Fuerteventura, can be explained in

part by population movements from Lanzarote

and Fuerteventura to El Hierro after the Norman

conquest.

424 J. C. R

Fig. 3. Diagram displaying the probabilities (roundeddown to multiples of 2.5^) of sequence matches betweenislands within the pool of those 206 sequences which arematched between at most 3 islands (thus excluding thefour most frequent types and types 069–126 and 311):each single link in the multigraph thus represents asummand of 2.5^ probability; island codes are as inTable 1.

Phylogeography of mtDNA focusses on the

spectrum and area-specificity of major haplo-

groups, geographic distribution of matched or

closely related sequences, and diversity in re-

gional clades of rather recent origin, in order to

unravel different settlement processes and mi-

grational routes. For example, the different

population histories of the two neighbouring

equatorial islands of Bioko (with its mainly

autochthonous population) and Sa4 o Tome!(settled by slave trade) are clearly manifest in

the phylogeographic patterns of sampled

mtDNAs; see table 2 of Mateu et al. (1997). The

population history of the Canary Islands is much

more intricate, in that both types of those

settlement processes probably occurred on each

island, in addition to subsequent influx of

European settlers on a large scale. Mitochondrial

DNA, rather than the Y-chromosome, appears

to be an ideal genetic indicator for distinguishing

between different settlement processes in this

particular case because (1) at present finer

phylogeographic information is available for

mtDNA compared to Y, and (2) the paternal

traces of the autochthonous Canarian population

in the current gene pool may be too insignificant

since the mortality of aboriginal males was

probably much higher than that of females

during the European conquest.

Our study of 300 HVS-I mtDNA sequences

sampled across the Canary Islands revealed a

subdominant type, 163–172–219–311, at fre-

quency 8% that has never been found outside

the Canary Islands. The whole mtDNA clade

U6b1 rooted at this type seems to be autoch-

thonous to the archipelago, notwithstanding the

singular occurrences of U6b1 in Portugal and

Galicia (which were in contact with the Canaries

during the colonial period). The distribution and

diversity of U6b1 across the seven islands (Table

1) suggest that the two types 163–172–219–311

and 092–163–172–219–311 may have been foun-

ders which arrived at the two easternmost

islands, from where they spread westward to the

other islands during the initial settlement process

(archaeologically dated as about 2500 years ago).

A few other types, such as the H type 260, may

have accompanied the U6b1 types, but it is

impossible to give a clear-cut decision on which

types were among the first founders. For in-

stance, it is difficult to decide whether a one-step

descendant of a major founder type constitutes

an autochthonous variant or a minor founder

type. Our founder analysis suggests that more

than 20% of the total sample could have its

origin in the pioneer settlement of the islands.

We can, however, neither claim that the pioneer

population was necessarily an ethnically homo-

geneous group nor exclude the possibility that

there were additional (small-scale) migrations

from the north-western African coast to specific

islands, or later occasional contacts. It seems

though that later migrations did not leave a

major footprint in the current Canarian mtDNA

pool, in view of merely 1% U6 sequences in the

total sample which do not have the Canarian

motif (U6b1). The genetic analysis cannot prove

either that the first settlers ethnically were

Berbers, since the salient area-specific marker U6

by far predates any meaningful ethnic asso-

ciations. In fact, the clade U6 (with root motif

172–219, dubbed ‘Berber motif ’), being omni-

present in the Berber populations, may have

been present in North Africa for more than

40000 years and its subclade U6b (with motif

172–219–311) for more than 20000 years (mainly


restricted to the westernmost part of North

Africa).

The Canary Islands have been a frequent

target of admixture studies. Different markers,

methods, and settings have been used in this

context. If the objective of admixture studies is

to shed light on the historical processes that

shaped a ‘mixed’ population, then care should

be taken that the source populations, being

themselves mixed relative to deeper time levels,

be well defined and reconstructed in their genetic

composition at the appropriate time horizon. For

instance, in our analysis we have tacitly assumed

that populations in Northwest Africa 2500 years

ago resembled present-day Berber populations in

Morocco with respect to their mtDNAs, which

may be approximately true given historical

accounts. If, however, the anticipated date for

the relevant migration events was 10000 years

ago, then one would have to face the problem

that more than half of the Northwest African

mtDNA pool had its ancestors elsewhere at that

time, mainly in Europe and the Near East

(Rando et al. 1998; Macaulay et al. 1999).

Moreover, admixture percentages alone do not

provide a clue to the historical processes that led

to the formation of a population in some areas.

Uniparental markers, though more vulnerable to

effects of genetic drift than nuclear markers,

offer the additional advantage of reflecting

demographic aspects in a measurable time scale.

One would not employ the full potential of

mtDNA or Y markers when one resorted to

comparing genetic distances between mtDNA

samples. The phylogenetic position of a mtDNA

sequence in a rooted tree, though scaleable to

time under the assumption of a constant mol-

ecular clock, cannot be scaled to any meaningful

quantity that would reflect regional affinity.

Therefore the average distance of a mtDNA

sequence to a mtDNA sample representing a

hypothetical source population does not indicate

whether the sequence has its ancestry in that

population or not. For instance, a typical

European (HVS-I) X type 189–223–278 would

be closer by distance to sub-Saharan African L2

types than to a European mtDNA sample.

Consequently, the admixture percentages calcu-

lated for the initial mtDNA sample from Tenerife

(Pinto et al. 1996a) are not exempt of such

criticism. MtDNA types should rather be allo-

cated to areas of origin (under a given time

horizon) by phylogeographic analysis. The no-

torious difficulty then is that some types may

appear to be enigmatic in view of the current

mtDNA database or other types (such as CRS)

may nearly be ubiquitous and could not be

assigned unambiguously, so that one would have

to focus on those types which indeed may be

regarded as diagnostic for certain geographic

areas. Contrasting European with sub-Saharan

African populations, one could take mtDNA

haplogroup H as diagnostic for Europe and

L1}L2 as diagnostic for sub-Saharan African, as

proposed by Parra et al. (1998). Although the

diagnostic types would probably cover about one

half of a mixed mtDNA sample, the resulting

admixture percentages are prone to considerable

error because, in particular, the frequency of

haplogroups L1}L2 in sub-Saharan African

samples varies considerably (Watson et al. 1997,

fig. 4). For a similar reason, the diagnostic IP

percentages in Fig. 2 would not yield reliable

admixture values. The simple majority rule

based on the HpaI site at np 3592 (separating

L1}L2 from L3) and positions 16223 and 16311,

as employed by Krings et al. (1999) in order to

distinguish Eurasian from sub-Saharan African

mtDNAs in a zone of admixture (Nile Valley),

inevitably results in misclassification within L3:

the majority of genuinely African L3 types would

be scored as Eurasian because they lack the

16311 transition, whereas a very small number

of European L3 types (most of haplogroup I)

would be scored as sub-Saharan African. These

pitfalls can largely be avoided by applying

partial RFLP analysis combined with HVS-I

motif searches in the mtDNA database, so that

possibly more than 95% of the mixed sample

could be categorised correctly. In our mtDNA

sample from the Canary Islands 6–7% of the

sequences are ultimately of sub-Saharan African

ancestry. This, however, does not necessarily

imply that ‘black’ slaves carried the corre-

426 J. C. R

sponding ancestral mtDNAs to the archipelago.

In fact, the present-day Northwest African

populations have a small contribution (& 4%) of

sub-Saharan African mtDNAs. Further, since

two sequences in our sample are of Amerindian

descent, it is realistic to expect further sequences

of American origin in the sample, perhaps one of

which in turn could have an earlier sub-Saharan

African ancestry. Therefore it seems that no

more than 4–5% of the mtDNAs in the total

sample (as well as in the subsample from

Tenerife) directly descended from the victims of

the ‘black’ slave trade to the Canary Islands. It

is interesting to note that the sub-Saharan

African-specific nuclear marker G6PD fast allele

A, which is virtually absent in Moroccan Berbers,

would predict 3–5% direct sub-Saharan African

input to the Canarian sample (using the data of

Pinto et al. 1996b ; Roychoudhury & Nei, 1988).

On the other hand, sub-Saharan African popu-

lations, especially in the Sahel zone bordering the

Sahara, have a little North African admixture.

For example, the Fulbe bear 13% mtDNAs of

northern origin (5 H, 1 U5a, 1 U6a, 1 U6b

sequences in a sample of 60; Watson et al. 1997),

which is not so surprising in view of the Fulbe

diaspora (Newman, 1995). But even in a sample

of 240 mtDNAs from Senegal (Graven et al. 1995;

Rando et al. 1998) there are 7 (3%) sequences of

Northwest African ancestry (namely, 2 H, 2

U5a, 1 U6a, 2 U6b sequences). Although some of

this northern input could have originated

through rather recent diffusion of Berbers to

their southern neighbours, the subclade U6a

(with root motif 172–219–278) possibly spread

into the Sahel zone much earlier, when the (last)

desertification of the Sahara began. The most

frequent U6 type, 172–189–219–278, is not only

found in the Fulbe and Senegalese populations,

but also in the Songhai, and in the East African

Kikuyu (Watson et al. 1997); thus, some U6a

sequences have become genuine sub-Saharan

African sequences. This explains the seeming

paradox which puzzled Krings et al. (1999) in

categorising the single U6a sequence from the

Nile Valley (in Egypt). U6 sequences along with

a few sub-Saharan African sequences have also

invaded the Iberian mtDNA pool: 3% of the

pooled Portuguese}Galician sample belongs to

U6 and an equal amount to other sub-Saharan

African clusters.

Maternal contribution, as deduced by mtDNA

data, appears to be in good agreement with the

nuclear data concerning the quantitative esti-

mates of the genetic contribution of Europeans,

North Africans and sub-Saharan Africans to the

Canarian gene pool. It seems though that the

North African mtDNA input to the Canary

Islands is slightly larger than has been predicted

by nuclear studies. One should bear in mind,

however, that sampling strategies might strongly

influence the results. For example, the gene pool

of La Gomera clearly deviates from that of

Tenerife in several quantitative aspects. We

therefore cannot concur with the view expressed

by Moral et al. (1997) that the population of

Tenerife ‘can be considered to be representative

of the general Canarian population’. Even within

a single island there may be striking contrasts as

to the mtDNA composition: for example, all U6

sequences from La Palma stem from the southern

part of the island. It would thus be interesting to

study the micro-geographical genetic patterns in

the Canary Islands in more detail using mtDNA

and Y chromosome markers.

In summary, our analysis of 300 mtDNA

sequences from the Canary Islands suggests that:

(i) one major initial migration (of a not necess-

arily homogeneous founder population) pro-

ceeded from east to west, that (ii) had its origin

in Northwest Africa (although the exact point of

departure cannot be determined from the genetic

data), whereas (iii) later arrivals from Northwest

Africa, in the course of the slave trade, had a

comparatively minor impact on the Canarian

mtDNA pool, but (iv) the European colonisation

led to differential reduction and partial trans-

location of the aboriginal population and eventu-

ally to a massive influx of Europeans, especially

to the larger islands.

We thank the Centros de Salud of the Canary Islandsfor blood samples. This research was supported by grantPB93-0558 from DGES to V. M. Cabrera and a PhDgrant from the Gobierno de Canarias to J. C. Rando.


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Phylogeographic patterns of mtDNA reflecting the colonization of the Canary Islands

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