Complex E olu iona y His o y Wi h Ex ensi e Ances al
Gene Flow in an A ican P ima e Radia ion
Axel Jensen ,
1,
* F ances Swi ,
2
Do ien de V ies,
3
Robin M.D. Beck,
3
Lukas F.K. Kude na,
4
Sascha Knau ,
5
Id issa S. Chuma,
6
Julius D. Keyyu,
7
And ew C. Ki chene ,
8,9
Kyle Fa h,
4
Je ey Roge s ,
10
Tomas Ma ques-Bone ,
11,12,13,14,15
Ka e M. De wile ,
16
Ch is ian Roos,
17
and
Ka e ina Guschanski
1,2,
*
1
Depa men o Ecology and Gene ics, Animal Ecology, Uppsala Uni e si y, Uppsala SE-75236, Sweden
2
School o Biological Sciences, Ins i u e o Ecology and E olu ion, Uni e si y o Edinbu gh, Edinbu gh, UK
3
School o Science, Enginee ing & En i onmen , Uni e si y o Sal o d, Sal o d M5 4WT, UK
4
Illumina A i icial In elligence Labo a o y, Illumina Inc., Fos e Ci y, CA 94404, USA
5
Ins i u e o In e na ional Animal Heal h/One Heal h, F ied ich-Loe le -Ins i u , Fede al Resea ch Ins i u e o Animal Heal h,
G ei swald – Insel Riems 17493, Ge many
6
Tanzania Na ional Pa ks, A usha, Tanzania
7
Tanzania Wildli e Resea ch Ins i u e (TAWIRI), A usha, Tanzania
8
Depa men o Na u al Sciences, Na ional Museums Sco land, Edinbu gh EH1 1JF, UK
9
School o Geosciences, Uni e si y o Edinbu gh, Edinbu gh EH8 9XP, UK
10
Human Genome Sequencing Cen e and Depa men o Molecula and Human Gene ics, Baylo College o Medicine,
Hous on, TX 77030, USA
11
Ins i u e o E olu iona y Biology (UPF-CSIC), PRBB, Ba celona 08003, Spain
12
Ins i u Ca ala de Paleon ologia Miquel C usa on , Uni e si a Au onoma de Ba celona, Ba celona, Spain
13
Ca alan Ins i u ion o Resea ch and Ad anced S udies (ICREA), Ba celona, Spain
14
CNAG-CRG, Cen e o Genomic Regula ion (CRG), Ba celona Ins i u e o Science and Technology (BIST), Ba celona 08028,
Spain
15
Ins i ucio Ca alana de Rece ca i Es udis A anca s (ICREA) and Uni e si a Pompeu Fab a, Ba celona 08010, Spain
16
Depa men o Biological Sciences, Flo ida A lan ic Uni e si y, Boca Ra on, FL, USA
17
Gene Bank o P ima es and P ima e Gene ics Labo a o y, Ge man P ima e Cen e , Leibniz Ins i u e o P ima e Resea ch,
Go ingen 37077, Ge many
*Co esponding au ho s: E-mails: [email p o ec ed]; [email p o ec ed].
Associa e edi o : Ma y O’Connell
Abs ac
Unde s anding he d i e s o specia ion is undamen al in e olu iona y biology, and ecen s udies highligh hyb id-
iza ion as an impo an e olu iona y o ce. Using whole-genome sequencing da a om 22 species o guenons ( ibe
Ce copi hecini), one o he wo ld's la ges p ima e adia ions, we show ha ampan gene low cha ac e izes hei
e olu iona y his o y and iden i y ancien hyb idiza ion ac oss deeply di e gen lineages ha di e in ecology,
mo phology, and ka yo ypes. Some hyb idiza ion e en s esul ed in mi ochond ial in og ession be ween dis an
lineages, likely acili a ed by coin og ession o coadap ed nuclea a ian s. Al hough he genomic landscapes o
in og ession we e la gely lineage speci ic, we ound ha genes wi h immune unc ions we e o e ep esen ed in in-
og essing egions, in line wi h adap i e in og ession, whe eas genes in ol ed in pigmen a ion and mo phology
may con ibu e o ep oduc i e isola ion. In line wi h epo s om o he sys ems ha hyb idiza ion migh acili a e
di e si ica ion, we ind ha some o he mos species- ich guenon clades a e o admixed o igin. This s udy p o ides
impo an insigh s in o he p e alence, ole, and ou comes o ances al hyb idiza ion in a la ge mammalian
adia ion.
Key wo ds: phylogenomics, specia ion, ancien hyb idiza ion, e olu iona y genomics, mammalian adia ion, guenon.
A icle
Recei ed: July 05, 2023. Re ised: Oc obe 17, 2023. Accep ed: No embe 09, 2023
© The Au ho (s) 2023. Published by Ox o d Uni e si y P ess on behal o Socie y o Molecula Biology and E olu ion.
This is an Open Access a icle dis ibu ed unde he e ms o he C ea i e Commons A ibu ion-NonComme cial License (h ps://
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In oduc ion
Ancien hyb idiza ion has been epo ed in many o gan-
isms, including mammals (Taylo and La son 2019).
Howe e , owing o hei la ge genomes, s udies o en i e
mammalian adia ions, pa icula ly among species- ich
g oups, a e unde ep esen ed (bu see Gopalak ishnan
e al. 2018; Cha ez e al. 2022), and mos cases ocus on
pai s o species (Taylo and La son 2019). Ye , la ge adia-
ions wi h lineages o di e en ages o e a unique oppo -
uni y o unde s and how inc easing lineage di e gence
along a specia ion con inuum may impac he abili y o
hyb idize and he ou come o hyb idiza ion e en s. As e-
p oduc i e isola ion accumula es wi h gene ic dis ance
(Coyne and O 2004), he impac and consequences
o in og ession may a y, as well as he mechanisms
ha allow o genomic incompa ibili ies o be o e come.
Se e al s udies ha e epo ed ha in og ession be ween
di e gen lineages may spa k apid specia ion and adap i e
adia ions by in oducing no el gene ic a ia ion (Meie
e al. 2017; Ma ques e al. 2019; S a dal e al. 2020).
Comp ehensi e genomic da ase s om species- ich adia-
ions o e unique possibili ies o s udy he in e play be-
ween hyb idiza ion, adap a ion, and specia ion.
He e, we ocus on guenons ( ibe Ce copi hecini), a
species- ich g oup o A ican p ima es ha adia ed o e
he las ca. 10 o 15 million yea s (MY) (Guschanski e al.
2013; Kude na e al. 2023). Wi h 89 axa and o e 30 dis-
inc species (IUCN 2022), guenons ep esen one o he
wo ld's la ges p ima e adia ions, spanning a b oad ange
o di e gence imes. Guenons a e enowned o hei eco-
logical, mo phological, and ka yo ypic di e si y and ha e
a ac ed he a en ion o e olu iona y biologis s and ecol-
ogis s o decades (Du illaux e al. 1988; Glenn and Co ds
2002; G ubb e al. 2003; Ens am and Isbell 2007; Moulin
e al. 2008). Ye , despi e possessing mul iple cha ac e is ics
ha ac as ep oduc i e ba ie s in o he s udy sys ems,
guenons eadily hyb idize, e en ac oss deep e olu iona y
dis ances (De wile e al. 2005; de Jong and Bu ynski
2010; De wile 2019). Fo example, De wile (2019) epo s
iable and a leas pa ially e ile hyb ids be ween
Ce copi hecus mi is and Ce copi hecus ascanius, 2 species
ha di e ged ca. 5 million yea s ago (MYA) (Kude na
e al. 2023) and di e in ch omosome numbe s. Genomic
s udies ha e also iden i ied ancien gene low in se e al
guenon lineages (S a dal e al. 2017; an de Valk e al.
2020; Ayoola e al. 2021), bu he ex en and ole o ances-
al hyb idiza ion h oughou he clade is unknown.
As such, guenons p o ide a highly in o ma i e sys em o
s udy he e olu ion o ep oduc i e isola ion and speci-
a ion in he con ex o a la ge adia ion. Speci ically, we
aim o (i) s udy genomic pa e ns o in og ession and me-
chanisms ha allow ba ie s o gene low o be o e come
a di e en e olu iona y dis ances, (ii) in es iga e he e-
pea abili y o in og ession landscapes along he speci-
a ion con inuum and (iii) explo e he unc ional ole o
in og essed egions and iden i y loci con ibu ing o e-
p oduc i e isola ion.
Resul s
Da ase , Sequencing and Geno yping
We compiled a da ase o whole-genome sequences om 37
samples belonging o 24 p ima e species (supplemen a y
able S1, Supplemen a y Ma e ial online; an de Valk e al.
2020; Ayoola e al. 2021; Kude na e al. 2023). These included
22 guenon species om all 6 gene a, Allenopi hecus,
Alloch ocebus, Chlo ocebus, E y h ocebus, Miopi hecus, and
Ce copi hecus (Fig. 1A), which collec i ely show a high deg ee
o sympa y h oughou sub-Saha an A ica (Fig. 1B). The
mos species- ich genus, Ce copi hecus, is commonly di ided
in o 6 e olu iona y dis inc species g oups: cephus, mi is,
mona, neglec us, diana, and hamlyni (G ubb e al. 2003;
Lo Bianco e al. 2017), all ep esen ed in ou da ase . We
also included 2 ou g oup species: Macaca mula a ( hesus
macaque) and Ce cocebus o qua us ( ed-capped manga-
bey). A e age ead mapping dep h a ied be ween 15.7
and 57.7 (median = 29.8). We called geno ypes agains
he hesus macaque e e ence genome (Mmul_10,
GenBank: GCA_014858485.1) and a e s ingen il e ing
(Ma e ials and Me hods), we ob ained 1.18 billion geno-
yped si es ac oss he au osomes, 52 million si es on he
X-ch omosome, and 63,565 si es on he Y-ch omosome.
O hese, 140 and 4.2 million si es we e biallelic single nu-
cleo ide polymo phisms (SNPs) on he au osomes and he
X-ch omosome, espec i ely. Addi ionally, we assembled
and anno a ed he mi ochond ial genomes (m DNA) o
all samples.
Species T ee In e ences
We cons uc ed a mul ispecies coalescence ee in
ASTRAL (Zhang e al. 2018), using 3,346 independen
au osomal gene ees, each ep esen ing a 25 kb genomic
egion sampled e e y 500 kb along he genome (Fig. 1C;
supplemen a y ig. S1, Supplemen a y Ma e ial online;
Ma e ials and Me hods). All gene a, species g oups and
species we e monophyle ic wi h maximal local pos e io
p obabili y (lpp) suppo (lpp = 1, supplemen a y ig. S1,
Supplemen a y Ma e ial online). The ee opology was
la gely consis en wi h he ecen p ima e phylogeny based
on ul aconse ed elemen s (UCE; Kude na e al. 2023), ex-
cep o he placemen o he genus E y h ocebus and he
diana species g oup. Bo h hese disc epancies in ol e apid
di e si ica ions wi h sho in e nal b anches and s ong in-
comple e lineage so ing (ILS), as illus a ed by a high deg ee
o gene ee disco dance a ound hese nodes (no malized
qua e sco e = 38% and 44%, espec i ely), which may be
di icul o esol e using UCE loci due o hei slow e olu-
ion (Beje ano e al. 2004).
We es ima ed di e gence imes on he ASTRAL opology
by combining 4 independen MCMCT ee uns (Yang 2007),
which con e ged a highly simila node age es ima es and
join ly esul ed in e ec i e sample sizes (ESS) ≥ 285 o all
nodes (supplemen a y ig. S2, Supplemen a y Ma e ial on-
line). These analyses sugges ha he guenons spli om
he Papionini ibe ca. 14.6 MYA (Fig. 1C; supplemen a y
able S2, Supplemen a y Ma e ial online), ollowed by he
Jensen e al. · h ps://doi.o g/10.1093/molbe /msad247 MBE
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4
681012
14MYA
44
45
38
C. hamlyni
C. diana
C. oloway
C. neglec us
C. pogonias
C. lowei
C. mona
C. albogula is
C. mi is
C. nic i ans
C. pe ua is a
C. cephus
C. ascanius
M. ogouensis
Allen. nig o i idis
E. pa as
Chl. d yas
Chl. pyge y h us
Chl. sabaeus
A. sola us
A. lhoes i
A. p eussi
Ce coc. o qua us
M.mula a
Ce coc. o qua us
M. mula a
M. ogouensis
Allen. nig o i idis
C. hamlyni
Chl. sabaeus
Chl. d yas
Chl. pyge y h us
A. sola us
C. ascanius
C. cephus
C. pe ua is a
A. p eussi
A. lhoes i
C. nic i ans
C. mi is
C. albogula is
E. pa as
C. mona
C. lowei
C. pogonias
C. neglec us
C. oloway
C. diana
A B
C
246 8 10 12 14 MYA
64
76
88
Fig. 1. Taxonomy, species ichness and mi onuclea disco dances among guenons. (A) Taxonomic o e iew o he 22 species included in his
s udy, shown acco ding o genus and species g oups. The colo o he e ical ba s co esponds o b anch colo s in (C). (B) Species ichness/
deg ee o sympa y o species included in his s udy, based on species dis ibu ions om IUCN (2022). (C) As al species ee ob ained
om 3,346 au osomal gene ees (le ) and maximum likelihood ee cons uc ed wi h RaxML om comple e mi ochond ial genomes ( igh ),
wi h connec o s highligh ing phylogene ic disco dances. Node anno a ions show b anch qua e suppo (le ) o boo s ap suppo ( igh ),
whe e his was <95%. B anches a e colo ed based on genus/species g oups as in (A). T ee opologies we e es ima ed om all a ailable samples
(supplemen a y igs. S1 and S7, Supplemen a y Ma e ial online) and we e subsequen ly p uned o a single sample pe species p io o di e gence
da e es ima es wi h MCMCT ee, applying ossil calib a ions o he nodes anno a ed wi h as e isks. Nodes we e o a ed o aid isualiza ion o
mi onuclea disco dances. Pho o c edi o (A): hamlyni: NRowe/all hewo ldsp ima es.o g; diana, Chlo ocebus: K. Guschanski; neglec us:
M. D’haen; mona: S. Knau ; mi is: M. Mpongo & K. De wile ; cephus: S. C aw o d & K. De wile ; Alloch ocebus: T. Ukizin amba a;
E y h ocebus: T. Valkenbu g; Miopi hecus: P. Paixão; Allenopi hecus: D. Su he land.
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i s spli wi hin he guenons ca. 13.4 MYA, di iding hem
in o 2 majo clades. One o hese clades con ains he gene a
Miopi hecus (M) and Ce copi hecus (C), which di e ged
om each o he ca. 12.4 MYA. The mainly a bo eal species
g oups belonging o he genus Ce copi hecus adia ed ca. 8
o 11 MYA, e e ed o as he “A bo eal clade” he ea e .
The o he majo clade con ains he genus Allenopi hecus
(Allen), as sis e o he e es ial gene a Chlo ocebus (Chl),
E y h ocebus (E), and Alloch ocebus (A), he ea e e med
he “Te es ial clade.” The Te es ial clade spli om
Allenopi hecus ca. 12.5 MYA and unde wen apid adia ion
ca. 8 MYA.
We epea ed he same p ocess wi h 118 X-ch omosomal
loci, esul ing in an iden ical opology wi h highly
simila di e gence imes (supplemen a y igs. S3 o S5,
Supplemen a y Ma e ial online). The placemen o
E y h ocebus as a sis e o Chlo ocebus ecei ed low sup-
po (lpp = 0.53), likely due o apid adia ions and a high
deg ee o ILS.
Samples om male indi iduals we e a ailable o 17 spe-
cies and hey we e used o cons uc a Y-ch omosome
phylogeny wi h RaxML (S ama akis 2014). Compa ed
wi h he au osomal phylogeny, his ee disag eed only
in he placemen o E y h ocebus, in line wi h he incom-
ple e suppo ob ained o his node in o he da ase s
(supplemen a y ig. S6, Supplemen a y Ma e ial online).
Conside ing he high opological conco dance among nu-
clea ma ke s o di e en inhe i ance modes, we he ea e
e e o he au osomal phylogeny as he “species ee”
(Fig. 1C), al hough some unce ain y emains ega ding
he exac placemen o E y h ocebus.
Mi onuclea Disco dances Sugges Ancien
Hyb idiza ion
We assembled he mi ochond ial genomes o all samples,
cons uc ed a maximum likelihood ee in RaxML, and es-
ima ed di e gence imes wi h MCMCT ee (Fig. 1C;
supplemen a y igs. S7 and S8, Supplemen a y Ma e ial on-
line; Ma e ials and Me hods). The mi ochond ial phyl-
ogeny was consis en wi h p e ious epo s (Guschanski
e al. 2013) and showed se e al ha d incong uences
wi h he species ee (Fig. 1C; supplemen a y ig. S7,
Supplemen a y Ma e ial online). Mos s ikingly, he e -
es ial genus E y h ocebus is nes ed wi hin he A bo eal
clade, sis e o he cephus and mi is species g oups, and
2 e es ial Alloch ocebus species—Alloch ocebus lhoes i
and Alloch ocebus p eussi—clus e oge he wi h he a -
bo eal cephus species g oup, whe eas hei congene
Alloch ocebus sola us is sis e o he e es ial genus
Chlo ocebus.
Topological di e ences be ween nuclea and mi ochon-
d ial phylogenies can be caused by ILS o hyb idiza ion. We
explo ed he p obabili y o ILS causing he obse ed mi o-
nuclea disco dances using simula ions and ound ha
opological con lic s whe e a lineage changes posi ion
om being nes ed in one clade o being nes ed wi hin an-
o he we e highly unlikely o occu unde ILS alone
(supplemen a y ig. S9, Supplemen a y Ma e ial online).
Fo example, while E y h ocebus pa as shi ed posi ion
ac oss a single node in 19% o 10,000 simula ions, only a
single simula ion esul ed in a shi ac oss 2 nodes, which
would s ill be insu icien o explain i s placemen in
he eal da a (supplemen a y ig. S9B, Supplemen a y
Ma e ial online). Thus, ILS emains a plausible explana ion
o lineages shi ing posi ions ac oss single nodes, e.g.
Miopi hecus and Ce copi hecus diana, whe eas he deepe
mi onuclea disco dances a e mo e likely explained by hy-
b idiza ion and mi ochond ial in og ession.
Ancien Gene Flow is P e alen Among Guenons
To u he in es iga e ancien hyb idiza ion, we used
Dsui e (Malinsky e al. 2021) o calcula e D-s a is ics and
4- a ios (Du and e al. 2011) on au osomal da a o all
possible ios o guenon species, using he hesus macaque
as ou g oup. Ou o 1,540 es ed ios, 865 p oduced sig-
ni ican D-s a is ics, indica i e o gene low. Howe e ,
hese a e no independen as sha ed ances y may c ea e
signals o gene low in close ela i es o descendan s o
he in ol ed lineages. To disen angle his complex pa e n,
we used di e en combina ions o D-s a is ics simila o
he D
FOIL
-me hod (Pease and Hahn 2015). Addi ionally,
we applied an app oach adap ed om he pa i ioned
D-s a is ic (Ea on and Ree 2013), whe e we excluded
sha ed a ian s o de ec “ca yo e e ec s,” a phenom-
enon ha p oduces posi i e D- alues in close ela i es
o he ac ual sou ce, as a consequence o hei sha ed an-
ces y. B ie ly, i di ec ional gene low occu s om species
A o species B, his will also gene a e a signal o excess allele
sha ing be ween any species mo e closely ela ed o A han
o B, whe eas his is no he case i gene low is es ic ed o
he opposi e di ec ion (mo e de ails in Ma e ials and
Me hods; Fig. 2). Iden i ying hese e ec s allowed us o
disen angle he p ima y sou ce and ecipien lineages
(i.e. in e di ec ionali y) o mos gene low e en s.
We de ec ed he s onges signal o excess allele sha ing,
indica i e o ances al hyb idiza ion, be ween he cephus
and mona species g oups (D = 0.15 o 0.29, Fig. 2, e en s
A1 and A2 in Fig. 3). The 4- a ios, which p o ide an
es ima e o he p opo ion o in og ession ac oss he gen-
ome, sugges ed ha a leas 10% o 20% o he genome
was in og essed (simula ions ha e shown ha 4- a ios
may subs an ially unde es ima e he ac ual p opo ion
o gene low [S a dal e al. 2020]). This gene low e en
also p oduced signi ican alues o D be ween he cephus
g oup and Ce copi hecus neglec us, he la e being sis e
o he mona g oup (Fig. 2). Howe e , his was likely d i en
by sha ed ances y be ween C. neglec us and he mona
g oup, as hese D- alues app oached ze o when only
p i a e alleles we e conside ed (Fig. 2). This sugges s di ec-
ional gene low om he mona g oup, wi h ca yo e -
e ec s om C. neglec us, in o he cephus g oup.
Simila ly, we ound excess allele sha ing be ween he
mona and mi is g oups, also p ima ily d i en by ca yo e -
e ec s due o he sha ed ances y be ween he cephus and
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mi is g oups (Fig. 2). Hence, we conclude ha he e has
been bidi ec ional gene low be ween he ances o s o
he cephus and mona g oups. The D- alues a ied subs an-
ially among cephus and mona g oup species (Fig. 2), sug-
ges ing mo e han a single ances al pulse o gene low. The
simples scena io ha could explain he obse ed D- alues
in ol es 2 bidi ec ional pulses o gene low: one be ween
Ce copi hecus pe au is a and he mona g oup ances o ,
and a second be ween Ce copi hecus pogonias and he
ances o o Ce copi hecus cephus/ascanius (A1 and A2 in
Fig. 3). No ably, he spli be ween C. cephus and C. ascanius
p e-da es ha be ween C. pogonias and Ce copi hecus
mona/lowei in ou di e gence ime es ima es, con adic ing
he p oposed second gene low pulse in o he C. cephus/
ascanius ances o . Howe e , di e gence ime es ima es
om genomic egions wi h low in og ession be ween he
cephus and mona g oups p oduced a subs an ially
younge spli ime be ween C. cephus and C. ascanius, pos -
da ing he di e gence be ween C. pogonias and C. mona/
lowei by ca. 1 MY (supplemen a y ig. S10, Supplemen a y
Ma e ial online). These es ima es a e b oadly consis en
wi h he di e gence imes p oposed by Kude na e al.
(2023) and sugges ha in og ession om he mona g oup
likely in la ed ou di e gence ime es ima es among cephus
g oup species.
The second s onges gene low signal was de ec ed be-
ween he A bo eal and Te es ial clades (D ∼0.12, 4- a io
∼0.03 o 0.04; e en B1 and B2 in Fig. 3). We applied he
same pola iza ion app oach and ound ha mos D- alues
can be a ibu ed o a bidi ec ional gene low e en be-
ween he ances o s o he 2 clades, ca. 11 o 12 MYA (e en
B1; supplemen a y ig. S11, Supplemen a y Ma e ial online).
Howe e , he e es ial genus Alloch ocebus sha es mo e al-
leles wi h he A bo eal clade han i s sis e genus
Chlo ocebus (supplemen a y ig. S12A, Supplemen a y
Ma e ial online), sugges ing ha gene low con inued
o eoccu ed along he ances al Alloch ocebus b anch
(e en B2; Fig. 3). This is also suppo ed by he p esence
o a cephus g oup-like m DNA in A. lhoes i/p eussi
(Fig. 1C; discussed below) and a end owa ds excess al-
lele sha ing be ween speci ically he cephus g oup and
Alloch ocebus (supplemen a y ig. S12B, Supplemen a y
Ma e ial online). The eason ha his end is la gely non-
signi ican is likely due o he ex ensi e gene low wi hin
he A bo eal clade (Fig. 3).
Fu he mo e, we ound e idence o gene low be ween
he ances o o he mi is g oup and Ce copi hecus hamlyni
(Fig. 3; e en C; D ∼ 0.11, 4- a io = 0.04), he cephus and
mi is g oups (e en D, 2 pulses o gene low; D ∼ 0.07,
4- a io = 0.02 o 0.04; Fig. 3; supplemen a y ig. S13,
Supplemen a y Ma e ial online), C. pogonias and he eas e n
C. mona popula ion (e en E; D = 0.04, 4- a io = 0.01; also
epo ed by Ayoola e al. [2021], Chlo ocebus d yas and
Chlo ocebus pyge y h us (e en F; D = 0.03, 4- a io = 0.01;
as epo ed by an de Valk e al. [2020]) and A. sola us
and A. lhoes i (e en G; D = 0.02, 4- a io = 0.01). Using
he pola iza ion app oach, we could in e ha e en D
was bidi ec ional. The mos pa simonious explana ion o
he inc easing D-s a is ics wi h mo e dis an P1-lineages ob-
se ed in e en C and E is di ec ionali y om he mi is g oup
in o C. hamlyni and om he eas e n C. mona popula ions
in o C. pogonias, espec i ely (Fig. 3). We canno es o he
M. mula a
mi is g oup
cephus g oup
mona g oup
C. neglec us
P1: mi is g oup
P2: cephus g oup
P3: mona g oup
P1: C. neglecus
P2: mona g oup
P3: mi is g oup
C. neglec us
P2: mona g oup
P3: cephus g oup
-0.1
0.0
0.1
0.2
0.3
0.4
Ds a is ic
P1: mi is g oup
P2: cephus g oup
P3: C. neglec us
P2: C. pogonias
P2: C. pe au is a
P2: C. pe au is a
P2: C. pogonias
P2: C. mona/
lowei
P2: C. mona
/lowei P2: C. cephus/
ascanius P2: C. cephus/
ascanius
A B
Excess
allele
sha ing
P2-P3
No
excess
allele
sha ing
Nega i e D due o he "mi o e ec " o
pa i ioned D-s a is ics (no gene- low P3-P1)
Fig. 2. D-s a is ics and pa i ioned D-s a is ics. (A) Schema ic o e iew o gene low e en A (Fig. 3), wi h b anch colo s co esponding o he pa i ions
used o es ima e p i a e allele sha ing. Solid black a ows show he in e ed gene low, and dashed g ay lines show allele sha ing in e ed as “ca yo e ”
e ec s. (B) Fou es s o excess allele sha ing be ween he mona g oup, cephus g oup, mi is g oup, and C. neglec us, simila o he D
FI
, D
OL
, D
IL
, and D
FO
o he D
FOIL
es (Pease and Hahn 2015), espec i ely. G ay poin s and dis ibu ions show he D-s a is ics o all combina ions o axa om he e-
spec i e g oups as depic ed in he panel heade , wi h M. mula a as ou g oup, using all SNPs. Colo ed poin s and iolin dis ibu ions show he
D-s a is ics o he same ios (connec ed by g ay lines) a e emo ing si es wi h sha ed alleles be ween he cephus and mi is g oups (o ange, wo
le mos panels) o Ce copi hecus neglecus and he mona g oup (blue, wo igh mos panels). No e ha some D alues u n nega i e a e emo ing
sha ed ances al a ia ion, which is an expec ed consequence o his me hod and should no be in e p e ed as excess allele sha ing be ween P1 and P3
(Pease and Hahn 2015). E o ba s show he lowes and highes D-s a is ic ±3 s anda d e o s. Posi i e D-s a is ics ha app oaches ze o o become
nega i e a e sha ed alleles a e emo ed a e in e p e ed as ca yo e e ec s, indica ing di ec ionali y.
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opposi e di ec ion in hese 2 e en s since ou da ase lacks
sis e lineages o C. hamlyni and C. pogonias.
In o al we pinpoin 7 majo ances al gene low e en s (A
o G, Fig. 3), some o which occu ed in se e al pulses (A1 and
A2, B1 and B2, D1 and D2, ea ed as sepa a e pulses o he
same e en as hey a e s ongly in e dependen ). The di e -
ence in age be ween he nodes sepa a ing P2 om i s closes
sis e and ha sepa a ing P3 om P2, p o ides a minimum
ime o di e gence a he ime o gene low. These imes an-
ged om 0.7 o o e 5 MY (Fig. 3C), sugges ing ha ep o-
duc i e isola ion may emain incomple e o long pe iods.
We also in e ed hyb idiza ion e en s wi h an independen ,
model-based app oach based on phylogene ic ne wo ks
using PhyloNe wo ks (Solís-Lemus and Ané 2016; Solís-
Lemus e al. 2017). Since PhyloNe wo ks does no allow mul-
iple e icula ions along he same b anch, we analyzed
subse s o he ee o es each independen e en and ound
s ong suppo o all o hem (supplemen a y igs. S14 o S21,
Supplemen a y Ma e ial online). Howe e , we ully acknow-
ledge ha he p esen ed scena ios a e likely an o e simpli i-
ca ion, and addi ional gene low e en s may ha e occu ed.
Among he iden i ied gene low e en s, e en s D and E
mos likely in ol ed lineages wi h di e en ch omosome
numbe s based on he known ka yo ypes o he ex an spe-
cies (Fig. 3; Sineo e al. 1986; Lo Bianco e al. 2017). To in es-
iga e i his was he case in olde e en s, we econs uc ed
he ances al ka yo ypes using Ch omE ol (Hohna e al.
2016; F eyman and Höhna 2018). The 4 independen uns e-
u ned unique ances al s a es o in e nal nodes and con-
e ged poo ly (low suppo [lpp ≤ 25]; supplemen a y igs.
S22 and S23, Supplemen a y Ma e ial online). Howe e , all
econs uc ions sugges ha he mo e ancien e en s A
B
A
Fig. 3. Excess allele sha ing and gene low e en s among guenons. (A) D-s a is ic (ci cles) and 4- a ios (diamonds) as es ima ed by Dsui e
illus a ing excess o allele sha ing caused by he 7 iden i ied gene low e en s. The combina ions o es ed axa a e shown on he le (wi h
M. mula a as ou g oup). Posi i e D-s a is ic alues indica e gene low be ween P3 and P2 axa and a e connec ed by lines o he 4- a ios
ha e lec he p opo ion o gene low. The alues we e ob ained o all possible membe s o he espec i e species g oups, o which mo e
han a single ep esen a i e was a ailable in ou da ase . In e en s C and E, we obse ed dec easing D-s a is ics wi h mo e closely ela ed P1
axa (anno a ed as dashed shapes), indica ing di ec ionali y om P2 in o P3. (B) Schema ic o e iew o he iden i ied gene low e en s.
A ows a e shown whe e di ec ionali y could be in e ed. Mi ochond ial in og essions, accompanying nuclea gene low be ween in e nal
b anches, a e shown as dashed ci cles wi h an a ow. Dashed ci cles on ips highligh species ha ca y an in og essed mi ochond ion, wi h
ci cle colo co esponding o he mos likely in og ession e en . The dono in B2 was no ully esol ed, as illus a ed by he ques ion ma k,
and he dashed line o he C. cephus/ascanius di e gence illus a es he likely o e es ima e o his node's age (see main ex ). Whe e a ailable,
anno a ions o he igh o species labels show he ch omosome numbe o ex an species. (C) Schema ic o e iew o he minimum ime since
di e gence a he ime o in og ession, based on he di e gence ime es ima es. The di e gence ime es ima e be ween he eas e n and wes e n
popula ions o C. mona was e ie ed om Ayoola e al. (2021).
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(p ima ily A2), B, and C occu ed ac oss di e en ka yo ypes.
Thus, 5 ou o 7 majo gene low e en s a e mos likely exam-
ples o c oss-ka yo ypic gene low. The emaining 2 e en s
occu ed wi hin he ka yo ypically s able Alloch ocebus and
Chlo ocebus gene a (F and G), al hough he ka yo ype o
Chl. d yas is no known and ka yo ypic di e ences may in-
ol e mo e han di e ences in ch omosome numbe s.
A Combina ion o In og ession and ILS Bes Explains
Mi onuclea Disco dances
The de ec ed gene low e en s di ec ly explain 2 o he 5 ha d
mi onuclea disco dances (Figs. 1C and 3; e en s F and E),
whe eas he emaining cases a e mo e complex. Ou esul s
sugges ha hese disco dances a e bes explained by a com-
bina ion o in og ession and ILS: In og essed mi ochond ia
seg ega e in he ances al popula ion and become ixed only
in a subse o descendan lineages. Fo example, he hamlyni
g oup is a membe o he A bo eal clade in he species ee,
bu sis e o he Te es ial clade in he mi ochond ial phyl-
ogeny. Con adic ing he di ec in og ession o mi ochon-
d ia in o hamlyni om he Te es ial clade, we ound no
signal o nuclea gene low in o hamlyni a e i di e ged
om he es o he A bo eal clade (supplemen a y ig. S24,
Supplemen a y Ma e ial online). A scena io in which a
Te es ial-like m DNA in og essed in o he A bo eal clade
ances o du ing e en B1 and was subsequen ly e ained
only in he hamlyni g oup is hus mos compa ible wi h
ou esul s (Fig. 3B). Simila ly, despi e indis inguishable le els
o nuclea gene low be ween all membe s o he genus
Alloch ocebus and he A bo eal clade (supplemen a y ig.
S25, Supplemen a y Ma e ial online), only he A. lhoes i/p e-
ussi lineage ca ies he in og essed cephus g oup-like
m DNA. This haplo ype was mos likely ans e ed in o
he Alloch ocebus ances o in e en B2 bu di e en ially e-
ained du ing subsequen di e gence. The A bo eal-like
m DNA o he genus E y h ocebus is also likely he esul o
ances al in og ession and subsequen di e en ial so ing,
as his lineage shows lowe le els o nuclea gene low wi h
he A bo eal clade han o he membe s o he Te es ial
clade (supplemen a y ig. S11, Supplemen a y Ma e ial on-
line). A complica ing ac o is ha his scena io equi es
he e en ion o mi ochond ial polymo phism o e 2 speci-
a ion e en s (nodes), acco ding o ou species ee.
Howe e , as men ioned abo e, unce ain y emains ega d-
ing he phylogene ic posi ion o E y h ocebus, as al e na i e
opologies place i as sis e o a clade con aining he
Chlo ocebus and Alloch ocebus gene a (Kude na e al.
2023). Gi en his la e placemen , he m DNA polymo ph-
ism only needs o be e ained o e a single specia ion e en .
Mi ochond ial In og ession Ac oss Deeply Di e gen
Lineages was Facili a ed by he Co-so ing o Alleles in
Nuclea Genes Wi h Mi onuclea In e ac ing
Func ions
We iden i ied se e al mi ochond ial in og essions ac oss
deeply di e gen lineages. Nuclea and mi ochond ial
genes in e ac du ing he essen ial p oduc ion o ATP ia
oxida i e phospho yla ion (OXPHOS), and se e al epo s
a ibu ed hyb id in iabili y o mal unc ioning mi onuc-
lea complexes (Bu on 2022). The e o e, we in es iga ed
whe he mi ochond ial in og essions we e acili a ed by
coin og ession o mi onuclea in e ac ing genes. We
es ed his in one o he mos ex eme cases, he in og es-
sion o a cephus g oup-like mi ochond ion in o he ances-
al Alloch ocebus lineage, which in ol es lineages
sepa a ed by a leas 5 MY o independen e olu ion
(Fig. 3C). While A. lhoes i and A. p eussi a e ixed o an in-
og essed mi ochond ial genome, hei sis e , A. sola us,
e ains he ances al m DNA. To es i alleles in genes
wi h known mi onuclea in e ac ing unc ion (N-m genes,
supplemen a y able S3, Supplemen a y Ma e ial online)
we e di e en ially so ed alongside he in og essed
m DNA, we in es iga ed i hese genes we e mo e cephus-
like in A. lhoes i/p eussi compa ed wi h genes wi hou such
in e ac ions. Howe e , N-m and con ol genes showed
simila le els o cephus g oup ances y in A. lhoes i/p eussi,
and he e was no di e ence in absolu e di e gence o
A. sola us, sugges ing a lack o b oad-scale coin og ession
o N-m genes (supplemen a y ig. S26, Supplemen a y
Ma e ial online). Nex , we assessed SNP pa e ns on a
gene-by-gene basis o iden i y signa u es o ine-scale coin-
og ession o N-m genes (Fig. 4A). Using he same gene
se s (N-m and con ol), we coun ed cephus g oup-like al-
leles e ained only in ei he A. lhoes i/p eussi o A. sola us.
We used Chlo ocebus o pola ize he ances al Te es ial
clade allele and coun ed 2 SNP pa e ns: ca ego y
1—g ouping A. lhoes i/p eussi wi h he cephus g oup and
A. sola us wi h Chlo ocebus (in ag eemen wi h he
m DNA opology) and ca ego y 2—g ouping A. sola us
wi h he cephus g oup and A. lhoes i/p eussi wi h
Chlo ocebus (opposing m DNA opology, Fig. 4A). I only
ILS is in ol ed, we expec equal equencies o bo h
ca ego ies. Howe e , i a non-neu al p ocess a o s he
e en ion o coadap ed mi onuclea a ian s, we expec
an excess o ca ego y 1 SNPs. In line wi h coin og ession
o N-m alleles, he e was a clea excess o ca ego y 1
SNPs in N-m compa ed wi h con ol genes (Fig. 4B;
supplemen a y able S4, Supplemen a y Ma e ial online).
In N-m genes, we ound 196 ca ego y 1 SNPs and 96
ca ego y 2 SNPs, whe eas simila numbe s o bo h SNP
ca ego ies we e ound among con ol genes (a maximum
o 133 and 131, espec i ely). Mo e han hal o he
ca ego y 1 N-m SNPs we e loca ed in he genes
NDUFA10 and LRPPRC (70 and 31, espec i ely) and
included se e al nonsynonymous a ian s (3 and 1,
espec i ely, supplemen a y able S3, Supplemen a y
Ma e ial online). No nonsynonymous cephus-like a ian s
we e ound in A. sola us in hese genes, and ac oss all con-
side ed N-m genes, we de ec ed a g ea e numbe o
cephus-like nonsynonymous a ian s in lhoes i/p eussi
han in sola us (11 s. 1). Mu a ions in NDUFA10 and
LRPPRC ha e been linked o dys unc ion o mi ochond ial
complexes I (Hoe s e al. 2011) and IV (Oláho á e al. 2015),
bo h o which a e in ol ed in OXPHOS. Ou esul s hus
sugges ha e aining cephus-like a ian s in hese genes
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may ha e been essen ial o o e come mi onuclea incom-
pa ibili ies and o acili a e mi ochond ial in og ession.
Admixed Genomes a e a Mosaic o Di e en
Ances ies Wi h Ele a ed He e ozygosi y in
In og essed Regions
Nex , we in es iga ed he spa ial pa e ns o gene low o
unde s and he genomic a chi ec u e o in og ession.
Fo simplici y, we only es ed he io se up ((P1, P2) P3)
wi h he highes D- alues o e en s occu ing in se e al
pulses (A1, B1, D1, Fig. 3). We cons uc ed neighbo -
joining ees in non-o e lapping 25 kb windows along
he genome and assigned hem o 3 main opologies:
T ee 1 co esponds o he species ee, T ee 2 shows he
in og essed opology, and T ee 3 is consis en wi h ILS.
The species ee— he mos equen opology in all in-
s ances—was in e spe sed wi h sho egions o in o-
g essed and ILS-de i ed ances y in all e en s (Fig. 5A;
supplemen a y igs. S27 o S32, Supplemen a y Ma e ial
online). Consecu i e windows o in og essed ances y
we e a e, in line wi h ancien iming o gene low
(supplemen a y ig. S33, Supplemen a y Ma e ial online).
No ably, T ee 2 may also a ise h ough ILS and he p opo -
ion o in og essed ances y mus be assessed ela i e o
T ee 3, which is expec ed o esul only om ILS. T ee 2
A
BC
Fig. 4. P e alence o p i a ely e ained in og essed cephus g oup alleles in A. lhoes i/p eussi and A. sola us in nuclea genes in ol ed in mi o-
chond ial unc ions (N-m ) compa ed wi h he genomic backg ound. (A) Schema ic o e iew o he 2 conside ed SNP ca ego ies. The dashed
line in he species ee illus a es he mi ochond ial in og ession om he cephus g oup o he ances al Alloch ocebus b anch, subsequen ly
e ained only in he A. lhoes i/p eussi lineage. The ci cles illus a e he 2 ca ego ies o SNPs di e en ially ixed be ween he cephus g oup (ligh
ci cles) and Chlo ocebus (black ci cles): Ca ego y 1 g oups A. lhoes i/p eussi wi h cephus and can a ise h ough ILS and mi onuclea coseg ega-
ion, whe eas ca ego y 2 g oups A. sola us wi h cephus and is expec ed only om ILS. (B) Numbe o SNPs pe 1,000 base pai s o ca ego ies 1 and
ca ego y 2 ac oss 199 N-m genes ( ed diamonds) and 100 samples o 199 o he nuclea genes (g ay do s). (C) P opo ion o ca ego y 1 SNPs
con ibu ed by 33 N-m genes wi h a leas one such si e, highligh ing he iden i y o he 2 mos impo an genes.
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was always mo e equen han T ee 3 and, in line wi h ou
D-s a is ics analyses, we ound he highes ela i e p opo -
ions o T ee 2 in e en s A o D.
To assess how gene ic di e si y ela es o local ances y,
we calcula ed he e ozygosi y in he same 25 kb au osomal
windows as abo e. He e ozygosi y co ela es posi i ely wi h
local ecombina ion a e, mainly due o educed linked
selec ion (Nachman 2001; Cu e and Payseu 2013). The
same mechanism is p edic ed o c ea e a posi i e co el-
a ion be ween in og ession and ecombina ion a e:
In og essed haplo ype blocks, which a e p edominan ly
dele e ious, a e e icien ly pu ged in egions o low
Topology
Mean He e ozygosi y
nig o i idis lhoes i
p eussi
sola us
pa as d yas
pyge y h us
sabaeus
ascanius
cephusmi is
nic i ans
albogula is
pe au is a mona
lowei
pogonias neglec us diana
oloway
hamlyni ogouensis o qua us
mula a
B
C
D
C. neglec us
mona g oup
mona g oup
mona g oup mona g oup (1)
mona g oup (2)
C. pe au is a
C. neglec us
C. neglec us
C. neglec us
C. pe au is a
C. pe au is a
C. pe au is a
M. mula a
M. mula a
M. mula a
M. mula a
123
A
C
ch 1
ch 2
ch 3
ch 4
ch 5
ch 6
ch 7
ch 8
ch 9
ch 10
ch 11
ch 12
ch 13
ch 14
ch 15
ch 16
ch 17
ch 18
ch 19
ch 20
ch X
0 50,000,000 100,000,000 150,000,000 200,000,000
Genomic posi ion (Basepai )
2.88 %
4.76 %
9.57 %
33.13 %
49.65 %
Au osomes
2.82 %
3.16 %
9.77 %
18.72 %
65.54 %
X-ch omosome
Allenopi ecus
Alloch ocebus
E y h ocebus
Chlo ocebus
mi is
cephus
mona
neglec us
diana
hamlyni
Miopi hecus
Papionini
0.002
0.004
0.006
31 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3
123 1 23 1 23 1 23 1 23 1 23 1 23 1 23 1 23 1 23 1 23 1 23
Fig. 5. Dis ibu ion, p e alence and he e ozygosi y o in og essed genomic segmen s. (A) Fi e possible ee opologies ob ained om 25 kb
genomic windows o he in og ession e en A1 (Fig. 3), in ol ing C. neglec us, mona, and cephus g oups (he e ep esen ed by C. pe au is a),
oo ed wi h M. mula a as ou g oup. T ee 1 g oups he lineages acco ding o he species ee. T ee 2 g oups he mona g oup species and C.
pe au is a monophyle ically o he exclusion o C. neglec us and can be caused by ances al in og ession o ILS. T ee 3 places he C. pe au is a
wi h C. neglec us and is expec ed o be caused only by ILS. The emaining 2 ees (ligh blue and g ay) ep esen mo e complex opologies, which
could be caused by, e.g. mo e ecen in og ession o ILS. (B) The genomic loca ion o he di e en ee opologies along he M. mula a ch o-
mosomes, and (C) hei ela i e abundance on he au osomes and he X-ch omosome. Black blocks in (B) co espond o egions o he genome
wi h insu icien in o ma ion o in e ences, equen ly loca ed a ound cen ome es and elome es. (D) He e ozygosi y in windows co espond-
ing o T ee 1, T ee 2, and T ee 3 opologies (shown as colo ed ci cles along he x axis) calcula ed o all samples and species. Connec o s show
signi ican wi hin-sample di e ences in he e ozygosi y be ween ee opologies, as assessed by ANOVAs ollowed by pos hoc Tukey's es s co -
ec ed o mul iple es ing.
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epea ed 100 imes wi h eplacemen , e ie ing 100
con ol gene se s o 199 genes each. We calcula ed F
D
and
D
XY
o each gene se wi h popgenWindows.py and
ABBABABAwindows.py (h ps://gi hub.com/simonhma in/
genomics_gene al). Fd was calcula ed o bo h A. lhoes i/p e-
ussi and A. sola us as P2, using all membe s o he cephus
g oup as P3, Allenopi hecus nig o i idis as P1 and M. mula a
as ou g oup. D
XY
was calcula ed ac oss 3 pai s: A. lhoes i/p e-
ussi e sus cephus g oup, A. lhoes i/p eussi e sus A. sola us,
and A sola us e sus cephus g oup. I N-m genes coe ol ed
wi h he in og essed m DNA genome, we expec o ind a
s onge signal o cephus g oup in og ession in hese genes
compa ed wi h con ol genes in A. lhoes i/p eussi, bu no
such pa e n in A. sola us. This would also lead o lowe
D
XY
be ween A. lhoes i/p eussi and he cephus g oup bu
inc eased D
XY
be ween A. lhoes i/p eussi and hei sis e
A. sola us in he N-m genes.
We also coun ed p i a e cephus g oup SNPs in A. lhoes i/
p eussi in ela ion o A. sola us. This was done o assess
ine-scale a ia ion ha may ha e acili a ed he mi ochon-
d ial in og ession. A cus om py hon sc ip was used o
iden i y and coun SNPs in 2 ca ego ies: Ca ego y 1:
A. lhoes i/p eussi ixed o he same allele as he cephus
g oup, whe eas A. sola us and Chlo ocebus spp. a e ixed
o he al e na i e allele (a nuclea pa e n ha is conco d-
an wi h m DNA genome ances y), Ca ego y 2: A. sola us
ixed o he cephus g oup allele, A. lhoes i/p eussi and
Chlo ocebus spp. ixed o he al e na i e allele (disco dan
wi h m DNA genome ances y). The numbe o SNPs in
each ca ego y was hen compa ed be ween N-m and con-
ol genes, and he p edic ed impac o hese mu a ions was
es ima ed using he Ensembl Va ian E ec P edic o
(McLa en e al. 2016).
Supplemen a y Ma e ial
Supplemen a y ma e ial is a ailable a Molecula Biology
and E olu ion online.
Acknowledgmen s
We hank Ch is ophe Escudé, Lau ianne Cacheux, and
Be and Bed’Homme a he Muséum Na ional
d’His oi e Na u elle, Pa is, o p o iding guenon cell cul-
u e samples, and Jean-Pie e Gau ie o issue samples
ha o m he bulk o da a used in his p ojec , as well
as Ma eike Janiak, Tom an de Valk, Simon Ma in,
and Kon ad Lohse o bioin o ma ic suppo and help ul
discussions. The compu a ions we e enabled by e-
sou ces in p ojec s SNIC 2022/6-325 and SNIC 2022/
5-561, p o ided by he Swedish Na ional In as uc u e
o Compu ing (SNIC) a Uppsala Uni e si y
(UPPMAX), pa ially unded by he Swedish Resea ch
Council h ough g an ag eemen no. 2018-05973. The
p ojec was suppo ed by he Swedish Resea ch
Council VR (2020-03398) o K.G., Zoologiska S i else
g an s o A.J., and a UKRI NERC S anda d g an (NE/
T000341/1) o D.d.V and R.M.D.B.
Au ho Con ibu ions
Concep ualiza ion: A.J., K.G., Me hodology and analyzes:
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W i ing—o iginal d a : A.J., K.G.; W i ing— e iew and
edi ing: all au ho s.
Con lic o in e es s a emen . Employees o Illumina, Inc.
a e indica ed in he lis o au ho a ilia ions. All o he
au ho s decla e no con lic o in e es .
Da a A ailabili y
The sequencing da a used in his p ojec a e a ailable on
he Eu opean nucleo ide a chi e (h ps://www.ebi.ac.uk/
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