Ancestral Markers

1. SNPs (single nucleotide polymorphisms). SNPs are a change in a single nucleotide in a chromosome and occur infrequently; once they occur they are stable and typically define a whole chromosome and become its signature.
2. STRs (short tandem repeats, aka microsatellites) (see Figure 2). STRs change by the number of repeats and change at a much faster rate than SNPs.

By testing the combination of SNPs and STRs in our Y-DNA, we can gain information on our paternal ancestry, ranging from ancient history (thousands and tens of thousands of years ago) with the much slower mutating SNPs, to recent history (100-1000 years ago) with faster mutating STRs.  More simply, SNPs allow us to track ancient or deep ancestry, while STRs allow us to track recent ancestry in the range of immediate family history over several generations and the relatively modern use of surnames. (see Figure 3). 

There are 20 major Y-DNA haplogroups (designated by the letters A through T) stemming in a branching fashion from the Y-DNA prototype, aka “Y-DNA Adam” (haplogroup A), which may be seen as the root or trunk of the tree (see Figure 4).  Each branch and haplogroup after “Y-DNA Adam” is defined by a novel SNP or genetic change.  The Genebase Y-DNA backbone SNP Test Panel is used to determine Y-DNA haplogroups and additional panels are available to further resolve Y-DNA lineage into sub-haplogroups or subclades. 



Figure 4.  This phylogenetic tree is presented in a more typical inverted fashion, with the A-T haplogroups defined by SNP markers as they branch from the root.  In order to identify your personal haplogroup, simply follow the branches from the ‘enter’ point with the SNPs identified, here exemplified in green for Haplogroup E.        

The Haplogroup E story …so far

The Haplogroup E branch of Y chromosomes is identified by the presence of SNPs M40 and M96 (and others; SRY4064, SRY8299, and P29).  E1 is the predominant subclade, while E2 is much less frequent.  Within E1, E1b1 (defined by SNP P2) is the most abundant and widespread representative, and accounts for most of Haplogroup E worldwide.  E1b1 lineages vary in abundance over Africa and three main regions are evident from the distribution peaks of three subclades: E1b1a (SNP M2) in Sub-Saharan Africa, E1b1b1a (SNP M78) in East Africa and E1b1b1b (SNP M81) in Northwest Africa.   The difference in geographic location of Haplogroup E subclades also aligns with distinct language groups supporting the idea that there is prevailing father to son transmission of language in Africa.  This very general picture has recently yielded to finer views of African lineages and migrations through the definition and study of additional subclades and more remote branches of Haplogroup E.  Indeed, this is one most frequently revised Y-DNA haplogroups with several upgrades of its subclade nomenclature.  To help avoid confusion with this terminology, we always include the informative or defining SNP with each subclade as these remain constant over revision of subclades names and phylogenetic arrangements. 



Figure 6. The emergence of modern humans.  A schematic timeline is shown with the approximate appearance of Homo sapiens, with particular attention to the estimated origins of different ancestral Y-DNA haplogroups and subclades of Haplogroup E.  Below the timeline is shown key geological and anthropological events.   kya = thousand years ago, hg = haplogroup, LGM = last glacial maximum.


SNPy trails and the spread of Haplogroup E
The leading hypothesis concerning the birth of Haplogroup E is that it originated in Northeast Africa and is one of the first emigrations of modern humans out of Africa to other parts of the world.  However, its shared phylogeny with Haplogroup D (see Figure 4), which is not in Africa and found in the Middle East, may indicate that Haplogroup E first appeared in the Middle East and the migration back to Africa is responsible for its prevalence here.  The TMRCA for Haplogroup E is 37 ±10kya and its subclades diverged from ~28-2kya (see Figure 6 and 13).  The simplest (or most parsimonious) explanation is that it arose in Northeast Africa and subsequently spread from this location to all parts of Africa, where it is clearly the dominant Y haplogroup.  The spread of Haplogroup E was also part of an early colonization of the Middle East and later Europe (see Figures 7-9).  As a result, Egypt served many times as a crossroads for the ancestors in Haplogroup E. 


The movements of human populations bearing haplogroup E:


Figure 7.  A map depicting the movements of human populations bearing haplogroup E.  A miniature phylogenetic tree legend with color coding for SNPs and subclades is shown at the left.  The origin of this Y-chromosome is most likely in East Africa, near Ethiopia.  Migrations to the north carried Haplogroup E towards Egypt and the Levantine corridor to the MidEast (M35 peach path).  Another migration is proposed to carry Haplogroup E derivatives, such M81, to the West and establish populations in North Africa (dark green path). The MidEast population is thought to develop new subclades, such as M123 (bright green) and V13 (orange), that are part of the colonization of Europe via Anatolia and the Balkan Peninsula, as well as further into Asia and the Arabian Peninsula (dark blue paths for M34 and V22).  There is also evidence for migration back into Africa (M78, M123, M34, V22) and crossing of the Mediterranean Sea by subclades of Haplogroup E (dark greens, M81 and V65).  The populations with Haplogroup E subclades in West Central Africa, primarily Bantu groups with the M2 subclade, dispersed this subclade extensively in Sub-Saharan and Equatorial Africa (beige paths). The expansion also reached South Africa, with the Eastern route (shown with M2 branch M191 in teal) perhaps being favored over the Western (dashed path).  The M2 population is also shown leaving Africa from the West coast to indicate the slave ports that were used from ~1650-1850AD.  The routes and locations are based on evidence from several studies of Y-chromosome E haplogroups and haplotypes and represent one possible scenario for the ancestral origin and propagation of this haplogroup.  



Frequency and distribution of Haplogroup E in Africa:


Figure 8. A map illustrating the frequency and distribution of Haplogroup E in Africa.  The frequency of haplogroup E is shown as the blue portion of the pie charts distributed over different locations.  The highest concentration of this haplogroup in West Central Africa, where is accounts for nearly all Y-DNA observed.    



Frequency and distribution of Haplogroup E in Europe and portions of Asia and Africa:


Figure 9. A map illustrating the frequency and distribution of Haplogroup E in Europe and portions of Asia and Africa.  The portion of the pie charts colored in blue represent the fraction of Haplogroup E among Y-DNA in region.  While Africa displays the highest overall frequencies, the next highest frequencies are found around the Balkan Peninsula, including Greece and Crete.  The frequency of Haplogroup E drops precipitously to the North and East.     

The following diagram depicts the current, deeply branching phylogenetic tree for Y-DNA Haplogroup E:


Figure 10.  The current phylogenetic tree for Y-DNA haplogroup E and its subclades 


The procedure for identifying your Y-DNA Haplogroup E Subclade is as follows:

Your Y-DNA Subclade will be automatically determined for you after your Sublcade test is completed.  However, if you are interested in finding out how your subclade was determined, just follow these steps:

Step 1.  Examine your test results from the Genebase Y-chromosome Haplogroup E Subclade Testing Panel.  Keep track of all your positive or derived SNP states and consult the Haplogroup E Subclade phylogenetic tree diagram (see Figure 9) or Table 1. 

Step 2.  Start with the root or main branch of Haplogroup E, which is ascertained by the presence of SNP M40.  According to your test results, follow the branches with your SNPs from the Genebase Y-chromosome Haplogroup E Subclade Testing Panel.  The point at which you no longer have mutations to follow is the branch or subclade of Haplogroup E to which you belong!

Geographical Distribution of the Subclades of Y-DNA Haplogroup E

Figure 15. A map illustrating the frequency and distribution of the Subclades of Haplogroup E in African Americans in the United States.  The total frequency of Haplogroup E is shown as the blue portion of the smaller pie charts, while the larger pie chart shows the fraction of each subclade contributing to this frequency.  Three charts are shown from three different studies.  See Table 3 for a detailed account of these frequency and distribution of E subclades.

Detailed Accounts for the Subclades of Y-DNA Haplogroup E

E1a1. M44

E1b1. P2

E1b1a.  M2

The observed distribution also suggests that the Bantu (E1b1a/M2) migration did not take go north of Kenya and moved south along the Southeastern (Swahili) Coast of Africa.  A barrier of the Cushitic language and culture in Northeast Africa has been proposed to explain the limited introgression of the Bantu E1b1a/M2 subclade in these northern regions.  Nevertheless, the spread of the Bantu is fairly extensive and their linguistic family (Niger-Congo) is the most widely dispersed language family in Africa, supporting the Y-chromosome evidence for the spread of the Bantu people through wide portions of Africa and providing a strong example of correlation between language and phylogeny in Africa.  On the other hand, the widespread distribution of Bantu and the E1b1a/M2 subclade, is responsible for a reduced geographic structure or the correlation between Y-chromosome phylogeny and a specific geographic location, thus acting to somewhat homogenize the populations.  

The E1b1a/M2 subclade in Oman may be due to recent slave trade with Africa, but since M2 is highest in the West (e.g. Senegal) and drops off significantly to the North and East, it has been speculated that these slaves must have come from a fairly far distance in Central or West Africa. 

E1b1a/M2 is also the most common Y haplogroup in African Americans (50-75%), a result of slave trade from Sub-Saharan Africa.  In South America, the estimates are ~8% for the M2 subclade.  Subclades of E1b1a (defined by SNPs U181, M291, U174, U290, U175) have been examined only in African and European American populations, where they are present in the former and absent in the latter.  U174 or E1b1a7a is the most prevalent at about 24% of African Americans. 

E1b1a2. M116.2

E1b1a3. M149

E1b1a4. M154

E1b1a5. M155

E1b1a6. M10

E1b1a7. M191

E1b1a7a. U174

E1b1a8. U175

E1b1a8a. U209

E1b1a8a1. U290

E1b1a8a1a. U181

E1b1a8a2. P59

E1b1a9. P268

E1b1b1. M35

The E1b1b1*/M35* subclade can be found in both western and eastern regions of Africa, but clearly has much higher frequency in East Africa (25-50%).  This trend is opposite to E1b1a M2 frequency and distribution.  The limit of E1b1a/M2 in Northeast Africa was suggested to be result of close knit cultures of Cushitic language groups, which harbor a large fraction of the E1b1b1/M35 lineage, thus giving an explanation for low E1b1a/M2 and high E1b1b1/M35 frequencies in Northeast Africa.

The M35 predecessors, P2 and M215 are also thought to have an East Africa origin based on STR variation.  M35* and M78 have been found in Europe and the Middle East and may have participated in the demic diffusion of agriculture during the Neolithic Era.  M35* is found in East Africa (e.g. Ethiopia) and is absent in Oman and Egypt, so the M35 descendants in Oman are likely to have more recent origins as evidenced by the presence of the subsequent SNP variations and the E1b1b1/M35 descendant subclades (E1b1b1a, M78 or E1b1b1b, M81 or E1b1b1c, M123).  The STR variation in Egypt is greater than Oman, pointing to an older establishment of M35 in Egypt and supporting the notion that the Levantine corridor through Egypt was the route for the spread of M35 lineages in the Middle East.  The timing for this migration coincides with the Mesolithic Era.  It is found in present day countries of Lebanon (16%), Turkey (11%), Iraq (11%) and surrounding regions.  

An interesting note is that the extent of E1b1b1* (M35*) to the South is near the proposed migration of the M2 subclade through Kenya and that Tanzania has a mixed contribution of both the ‘West M2’ and ‘East M35*’ subclades.  This mixture has a unique chronology in that the introduction of M2 by the Bantu is a recent admixture episode in comparison to a Stone Age origin for the M35* subclade.

In Europe, the E1b1b1*/M35* subclade is more prevalent in the Ashkenazi Jewish population (20%) than the non-Jewish population (6%), possibly indicating a founding role for the E1b1b1*/M35* subclade for the Ashkenazi Jews in Europe. 

n.b. recent studies have identified a new SNP, M293 that account for many of the M35* paragroup.  This new subclade, designated E1b1b1f, appears to have a concentration around Tanzania (43%), the country that harbored the highest reported frequency of M35* (37%).  The E1b1b1f/M293 subclade has a TMRCA estimated at 10kya and is associated with a more recent migration (~2kya) and spread of pastoralism (livestock herding) southward to South Africa.  Along with the E1b1a/M2/Bantu, this provides another instance of demic diffusion of new technologies in Africa.

E1b1b1a. M78

The E1b1b1a (M78) subclade of Haplogroup E predominates in Europe wherever Haplogroup E is found.   Since this haplogroup is most frequent in East Africa, it is likely connected to Africa via the Middle East and the Levantine corridor through Egypt.  The exit from Africa is estimated within the Mesolithic era.  The route to Europe continued through Anatolia and used the Balkan Peninsula, e.g. Greece, in the expansion of this subclade to the West.  This movement appears to closely parallel (in place and time) those taken by Y-chromosome Haplogroup J.  Together, Haplogroup J and E are believed to have spread agricultural practices during the Neolithic Era to Europe from the Near and Middle East. 

Given the presence of E1b1b1a/M78 in North Africa, it is likely that the migration north also produced a western trek from Ethiopia or Sudan into this area.  There may have also been backflow of this haplogroup into Africa during the Neolithic, again bringing with it new agricultural techniques into Egypt.  

Note that M78 SNP is the second highest representative in the Balkans (~23%).  There is a moderate geographic structure in that the frequency of E1b1b1a/M78 is higher in the South (Greece, Macedonia, Albania, Serbia) than the North (Croatia, Bosnia).  Low to very low frequencies (<5%) are seen in Iran and Pakistan and these tend to the southern regions of these two countries.  A moderate frequency (6%) has been detected in the Atlantic island group of the Azores (Portugal).

The M78 subclade has been sub-divided into clusters a, b, g and d by STR haplotype (microsatellite) analyses and these were recently shown to correlate well with new SNPs that also further subdivided and refined M78 subclade. (See the E1b1b1a1 derivatives below).  The E1b1b1a* or M78* paragroup, which constitutes roughly 1% of the E1b1b1a M78 lineage, is largely restricted to North Africa and corresponds closely to the b microsatellite cluster that was found here.

E1b1b1a1a. M224

E1b1b1a1b. V32

For example, the most prevalent E subclade in Crete was defined as the E1b1b1a M78 a cluster.  It is quite likely that Greece was the source of this subclade on Crete and that this subclade is common overall in the Aegean region.  The estimates for the TMRCA of this subclade are 9-11kya outside of Europe (i.e. Near East) and 4-5kya in Europe.  The expansion time for the E1b1b1a2 (V13) subclade in Greece is estimated around 4-9kya, somewhat preceding the estimate for the origin of this subclade, which is due to the use of different mutation rate models.  The estimate for expansion on Crete is 3kya, which coincides with an influx of Mycenaean culture from the Greek mainland during the end of the Bronze Age.  The E1b1b1a2 (V13) most closely follows the route proposed for Y-chromosome haplogroup J-M12 that was part of the late Neolithic introduction of farming and agriculture to Europe and the advances of the ensuing Bronze Age.

E1b1b1a2a. V27

E1b1b1a3a. M148

E1b1b1a3b. V19

E1b1b1a4. V65

The E1b11b1b/M81 subclade has a TMRCA of 4-9kya and expansion around 2kya.  It is therefore relatively new or perhaps recently emerged from a bottleneck and is subject to genetic drift (high frequency of genetic signature, low complexity or variation) in its isolation.  This latter notion may fit with a model for the geographic isolation in Northwest Africa where the Sahara desert separates this population from the South and the Mediterranean Sea separates it from the North.  The origin of this subclades dates to a ‘wet Sahara’ period that followed the end of the Ice Ages, and the expansion of the population dates after this period in the desertification of the Sahara.  This could fit a scenario where the M81 subclade population was isolated after its founding and witnessed little gene flow because of the Sahara desert barrier.  

A minor amount is found in Iberia and Sicily, which almost surely arrived from Northwest Africa sources.  The presence of M81 (and M35 and M78) in the Iberian Peninsula, albeit at much lower frequencies, argues for a limited by tangible connection between North Africa and Iberia.  The variation of Y-chromosome haplotypes also supports this claim (as does the presence of European subclades in NW Africa).  It should be noted that not all E haplogroup members in Iberia are the E1b1b1b/M81 subclade and that there are a fraction of M78 subclade that likely traveled from mainland Europe.   The presence of M78 and M81 SNPs in the Portugal should be linked to their presence in the Azores in the Atlantic Ocean.

E1b1b1b1. M107

E1b1b1b2. M183

E1b1b1c1. M34

It was noted at moderate frequencies (5-20%) in Jewish populations (Ashkenazi, Ethiopian, Libyan and Yemeni) in Israel, providing additional evidence for a link between the Middle East and North Africa.   The E1b1b1c1/M34 subclade is also present in Anatolia, Iberia, Sardinia and Crete (frequencies hovering at 5%).
 

E1b1b1c1a. M84

E1b1b1c1b. M290

E1b1b1e. V6

E1b1c. M329

E1b2. P75

E2. M75

E2a. M41

E2b. M54

E2b1a. M200

Modal Haplotypes Associated with Y-DNA Haplogroup E

Your unique set of Y-DNA STR markers obtained through the Y-DNA STR test is referred to as your "Haplotype".  This is not to be confused with your "Haplogroup" which is determined by testing the SNP markers in your Y-DNA through Y-DNA SNP backbone and subclade testing.

When the Y-DNA STR markers are tested for large groups of people from around the world, the haplotypes which occur with the highest frequencies within certain populations are called "Modal Haplotypes". 

For example, the M78 subclade has been classified into four clusters (a, b, g, and d) based on the STR or microsatellite clustering pattern and three of these have strong ties to location (see Figure 12).   V65 and M78a are primarily found in Europe, V65 and M78b primarily in North Africa and V32 and M78g in East Africa.  The modal haplotypes listed from Tunisia, are not confined to Haplogroup E and therefore have influence from other Y-chromosome haplogroups.

Confirmation of haplogroup assignment is always made by SNP testing.  Conversely, haplogroup assignment does not indicate that you will have the modal haplotype, recalling the fact that STRs are rapidly changing markers.  Table 2 provides a list of modal haplotypes associated with Haplogroup E.

Table 2.  Modal Haplotypes associated with Haplogroup E
Arredi et al. 2004 Am. J. Hum. Genet.  Cinnioglu et al. 2004 Hum. Genet. Cruciani et al. 2007 Mol. Biol. Evol. Pereira et al. 2002  Ann. Hum. Genet.  Sanchez et al. 2005 Eur. J. Hum. Genet.  Zalloua et al. 2008 Am. J. Hum. Genet. www.yhrd.org/

Resources/Bibliography

Non-Public: Abstract-only available
1. Beleza S, Gusmão L, Amorim A, Carracedo A, Salas A. The genetic legacy of western Bantu migrations. Hum Genet. 2005 Aug;117(4):366-75. Epub 2005 Jun 1. PMID: 15928903

2. Cadenas AM, Zhivotovsky LA, Cavalli-Sforza LL, Underhill PA, Herrera RJ. Y-chromosome diversity characterizes the Gulf of Oman. Eur J Hum Genet. 2008 Mar;16(3):374-86. Epub 2007 Oct 10. PMID: 17928816

3. Capelli C, Brisighelli F, Scarnicci F, Arredi B, Caglia' A, Vetrugno G, Tofanelli S, Onofri V, Tagliabracci A, Paoli G, Pascali VL. Y chromosome genetic variation in the Italian peninsula is clinal and supports an admixture model for the Mesolithic-Neolithic encounter. Mol Phylogenet Evol. 2007 Jul;44(1):228-39. Epub 2006 Dec 13. PMID: 17275346

4. Cruciani F, Trombetta B, Novelletto A, Scozzari R. Recurrent mutation in SNPs within Y chromosome E3b (E-M215) haplogroup: a rebuttal. Am J Hum Biol. 2008 Sep-Oct;20(5):614-6. PMID: 18449920

5. Csányi B, Bogácsi-Szabó E, Tömöry G, Czibula A, Priskin K, Csõsz A, Mende B, Langó P, Csete K, Zsolnai A, Conant EK, Downes CS, Raskó I. Y-chromosome analysis of ancient Hungarian and two modern Hungarian-speaking populations from the Carpathian Basin. Ann Hum Genet. 2008 Jul;72(Pt 4):519-34. Epub 2008 Mar 27. PMID: 18373723

6. Fernandes AT, Rosa A, Gonçalves R, Jesus J, Brehm A. The Y-chromosome short tandem repeats variation within haplogroup E3b: evidence of recurrent mutation in SNP. Am J Hum Biol. 2008 Mar-Apr;20(2):185-90. PMID: 17990327

7. Gonçalves R, Freitas A, Branco M, Rosa A, Fernandes AT, Zhivotovsky LA, Underhill PA, Kivisild T, Brehm A. Y-chromosome lineages from Portugal, Madeira and Açores record elements of Sephardim and Berber ancestry. Ann Hum Genet. 2005 Jul;69(Pt 4):443-54. PMID: 15996172

8. Hammer MF, Chamberlain VF, Kearney VF, Stover D, Zhang G, Karafet T, Walsh B, Redd AJ. Population structure of Y chromosome SNP haplogroups in the United States and forensic implications for constructing Y chromosome STR databases. Forensic Sci Int. 2006 Dec 1;164(1):45-55. Epub 2005 Dec 5. PMID: 16337103

9. Hassan HY, Underhill PA, Cavalli-Sforza LL, Ibrahim ME. Y-chromosome variation among Sudanese: Restricted gene flow, concordance with language, geography, and history. Am J Phys Anthropol. 2008 Jul 10. [Epub ahead of print] PMID: 18618658

10. Henn BM, Gignoux C, Lin AA, Oefner PJ, Shen P, Scozzari R, Cruciani F, Tishkoff SA, Mountain JL, Underhill PA. Y-chromosomal evidence of a pastoralist migration through Tanzania to southern Africa. Proc Natl Acad Sci U S A. 2008 Aug 5;105(31):10693-8. Epub 2008 Aug 4. PMID: 18678889

11. Karafet TM, Mendez FL, Meilerman MB, Underhill PA, Zegura SL, Hammer MF. New binary polymorphisms reshape and increase resolution of the human Y chromosomal haplogroup tree. Genome Res. 2008 May;18(5):830-8. Epub 2008 Apr 2. PMID: 18385274

12. King RJ, Ozcan SS, Carter T, Kalfoğlu E, Atasoy S, Triantaphyllidis C, Kouvatsi A, Lin AA, Chow CE, Zhivotovsky LA, Michalodimitrakis M, Underhill PA. Differential Y-chromosome Anatolian influences on the Greek and Cretan Neolithic. Ann Hum Genet. 2008 Mar;72(Pt 2):205-14. PMID: 18269686

13. Nasidze I, Ling EY, Quinque D, Dupanloup I, Cordaux R, Rychkov S, Naumova O, Zhukova O, Sarraf-Zadegan N, Naderi GA, Asgary S, Sardas S, Farhud DD, Sarkisian T, Asadov C, Kerimov A, Stoneking M. Mitochondrial DNA and Y-chromosome variation in the caucasus. Ann Hum Genet. 2004 May;68(Pt 3):205-21. PMID: 15180701

14. Neto D, Montiel R, Bettencourt C, Santos C, Prata MJ, Lima M. The African contribution to the present-day population of the Azores Islands (Portugal): analysis of the Y chromosome haplogroup E. Am J Hum Biol. 2007 Nov-Dec;19(6):854-60. PMID: 17712788

15. Pereira L, Gusmão L, Alves C, Amorim A, Prata MJ. Bantu and European Y-lineages in Sub-Saharan Africa. Ann Hum Genet. 2002 Nov;66(Pt 5-6):369-78. PMID: 12485470

16. Robino C, Crobu F, Di Gaetano C, Bekada A, Benhamamouch S, Cerutti N, Piazza A, Inturri S, Torre C. Analysis of Y-chromosomal SNP haplogroups and STR haplotypes in an Algerian population sample. Int J Legal Med. 2008 May;122(3):251-5. Epub 2007 Oct 2. PMID: 17909833


Key Investigators:
Luigi Luca Cavalli-Sforza
 Stanford University, Stanford, California, USA
Cristian Capelli
 Universita’ Cattolica del Sacro Cuore, Rome, Italy
Fulvio Cruciani
 Università di Roma, ‘La Sapienza’, Rome, Italy
Michael F. Hammer
 University of Arizona, Tucson, Arizona, USA
Rene J. Herrera
 Florida International University, Miami, Florida, USA
Mark A. Jobling
 University of Leicester, Leicester, United Kingdom
Pavao Rudan
 Institute for Anthropological Research, Zagreb, Croatia
Rosaria Scozzari
 Università di Roma, ‘La Sapienza’, Rome, Italy 
Ornella Semino
 Università di Pavia, Pavia, Italy
Mark Stoneking
Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany
Chris Tyler-Smith
 The Wellcome Trust Sanger Institute, Hinxton, UK
Peter A. Underhill
 Stanford University, Stanford, California, USA