Zoologica Sc ip a. 2024;53:487–508.
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487
wileyonlinelib a y.com/jou nal/zsc
Recei ed: 18 Decembe 2023
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Re ised: 19 Ma ch 2024
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Accep ed: 23 May 2024
DOI: 10.1111/zsc.12672
ORIGINAL ARTICLE
A new an sh ike (A es: Thamnophilidae) endemic o he
Caa inga and he ole o clima e oscilla ions and d ainage
shi in shaping c yp ic di e si y o Neo opical seasonal
d y o es s
PabloCe quei a1,2,3
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Gab iela R.Gonçal es1,2
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Tânia F.Qua esma3,4
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Ma celoSil a4
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Mau oPicho im5
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Alexand eAleixo3,4
This is an open access a icle unde he e ms o he C ea i e Commons A ibu ion License, which pe mi s use, dis ibu ion and ep oduc ion in any medium, p o ided
he o iginal wo k is p ope ly ci ed.
© 2024 The Au ho (s). Zoologica Sc ip a published by John Wiley & Sons L d on behal o Royal Swedish Academy o Sciences.
Co e pla e: Illus a ion o Sakespho oides niedeguidonae ( emale MPEG 84680, male MPEG 84480). Illus a ion by Edua do B e as.
1P og ama de Pós- g aduação Em
Zoologia, Museu Pa aense Emílio
Goeldi/Uni e sidade Fede al do Pa á,
Belém, Pa á, B azil
2Labo a ó io de Biogeog a ia da
Conse ação e Mac oecologia-
BIOMACRO, Ins i u o de Ciências
Biológicas, Uni e sidade Fede al do
Pa á, Belém, Pa á, B azil
3Ins i u o Tecnológico Vale, Belém,
Pa á, B azil
4P og ama de Pós- g aduação Em
Biodi e sidade e E olução, Museu
Pa aense Emílio Goeldi, Belém, Pa á,
B azil
5Depa amen o de Bo ânica e Zoologia,
Uni e sidade Fede al Do Rio G ande
Do No e, Na al, B azil
Co espondence
A. Aleixo, Ins i u o Tecnológico
Vale – ITV, Rua Boa en u a da Sil a,
955- 66055- 090, Belém, PA, B azil.
Email: alexand e.aleixo@i .o g
Funding in o ma ion
Coo denação de Ape eiçoamen o
de Pessoal de Ní el Supe io , G an /
Awa d Numbe : 1537057 and 1537056;
Financiado a de Es udos e P oje os,
G an /Awa d Numbe : 0118003100
Abs ac
The Caa inga is he la ges pa ch o Seasonal D y T opical Fo es in he Neo opics,
loca ed in no heas e n B azil and cha ac e ized mainly by deciduous ege a ion
and ex eme ain all seasonali y. I has his o ically been ea ed as a biologically
impo e ished domain, bu ecen s udies unco e ed new di e si ica ion pa e ns
and se e al new axa o ogs, mammals, insec s, and ishes. He e we employed a
dense sampling egime o e alua e whe he he São F ancisco Ri e (SFR) would
ha e p omo ed gene ic di e si ica ion and ixed pheno ypic di e ences and how
Qua e na y clima ic oscilla ions shaped dis ibu ion and popula ion sizes in a
Caa inga endemic species, he Sil e y- cheeked An sh ike (Sakespho oides c is-
a us). We adop ed an in eg a i e app oach using mul ilocus gene ic, plumage,
ocal da a, and ecological niche modelling (ENM) o cha ac e ize e olu iona y
uni s and niche sui abili y in pas scena ios. We eco e ed s ong gene ic s uc-
u e ac oss he SFR ha was cong uen wi h plumage and ocal a ia ion, e eal-
ing a ye undesc ibed species named he ein as Sakespho oides niedeguidonae, sp.
no . (u n:lsid:zoobank.o g:ac :2B9FC637- 008A- 4E9A- B92B- 69ED7FE23823s).
The spli ing ime es ima ed be ween he newly desc ibed species and S. c is a us
is consis en wi h he es ablishmen o he mode n cou se o SFR, wi h a mo e
ecen cou se shi appa en ly p omo ing he seconda y con ac be ween he wo
species in he Raso da Ca a ina egion. A e hei spli , bo h species expe ienced
inc eases in popula ion sizes and ange sizes a simila imes du ing he Las
Glacial Maximum. We expec o he Caa inga a ian endemic lineages o show
simila pa e ns o gene ic di e en ia ion ac oss he SFR ha we e enhanced by
Qua e na y clima ic oscilla ions.
488
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CERQUEIRA e al.
1
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INTRODUCTION
Seasonally D y T opical Fo es s (he ea e SDTFs) a e
ee- domina ed ecosys ems wi h a mo e o less con inuous
canopy in which g asses a e a mino elemen and ho ny
species a e p ominen . The ege a ion is mos ly decidu-
ous du ing he d y season, wi h deciduousness inc easing
as ain all declines in olume, al hough in he d ies o -
es s he e is a ma ked inc ease in e e g een and succu-
len species (Mooney e al.,1995; Penning on e al.,2000).
The SDTFs has cu en ly a discon inuous dis ibu ion
wi h e y he e ogeneous pa ches, including o ma ions as
di e se as all o es on mois e si es o cac us sc ub on
he d ies . In Sou h Ame ica his he e ogenei y p omp ed
he ecogni ion o dis inc co e a eas h oughou SDTFs
such as he ‘Caa inga nucleus' in no heas e n B azil, he
‘Misiones nucleus' in he Pa aná- Pa aguay basin, and he
‘Subandean Piedmon nucleus' in sou hwes e n Boli ia
and no hwes e n A gen ina (Penning on e al., 2000,
2006; P ado,2000; P ado & Gibbs,1993; Ra e e al.,1978;
Sil a & Ba es,2002).
The Caa inga is he la ges a ea o SDTFs and en-
compasses he e ogeneous a id and semi- a id o ma ions
su ounded by mo e mesic o ma ions, ex ending o
~800 km2 and ep esen ing 11% o he B azilian e i o y
(IBGE,1985). The geomo phology o his egion plays an
impo an ole in i s biogeog aphic his o y, wi h al i udes
anging om sea le el in he no h, an a e age 400–700 m
h ough Bahia and Minas Ge ais s a es in he cen al
pa , o o e 1000 m on he slopes o he Espinhaço ange
(Taylo & Zappi,2004). In addi ion o geological p ocesses
in he Paleogene−Neogene, Qua e na y clima ic oscilla-
ions also con ibu ed o he high le els o obse ed ende-
mism (We neck,2011).
The biogeog aphic his o y and di e si ica ion pa e ns
o SDTFs ha e ecei ed ela i ely less a en ion han hose
o Neo opical ain o es s (Amazonia and A lan ic Fo es ).
This is in pa because Caa inga was his o ically ea ed
as a species impo e ished domain wi h low endemism, a
concep alsi ied by ecen s udies (Mooney e al.,1995;
Penning on e al., 2000; We neck, 2011). Many s udies
ha e analysed Caa inga axa unde phylogene ic, phylo-
geog aphic and gene ic popula ion dynamics app oaches,
including insec s (Cou inho- Ab eu e al., 2008; F anco
& Man in, 2013), liza ds (Oli ei a e al., 2015; Passoni
e al.,2008; Siedchlag e al.,2010; We neck e al.,2015),
ogs (Thomé e al.,2016), mammals (Fa ia e al.,2013;
Nascimen o e al.,2011, 2013), ishes (Cos a e al.,2018),
and ees (Cae ano e al., 2008). Despi e he ecen in-
c ease in he numbe o s udies ocusing on Caa inga di-
e si ica ion pa e ns, addi ional s udies a e necessa y o
add ess he exis ence o cong uen spa io- empo al his o-
ies ac oss axa. In his sense, bi ds a e one o he leas
sampled axa by phylogene ic s udies di ec ed a Caa inga
endemic lineages, in s ong con as o o he domains
such as Amazonian and he A lan ic Fo es (do Ama al
e al.,2013; Sil a e al.,2019).
He ein, we p esen he i s mul i- cha ac e sys em-
a ic s udy in eg a ing gene ic, mo phological, ocal, and
ecological da a on a Caa inga endemic bi d species, he
Sil e y- cheeked An sh ike Sakespho oides c is a us (de
Wied- Neuwied, 1831). Un il ecen ly, his species was
placed in he genus Sakespho us, bu no el gene ic and
mo phological da a eco e ed i as non- monophyle ic,
p omp ing he ans e o S. c is a us o he sepa a e genus
Sakespho oides (B a o e al.,2021; G an sau,2010). The
endemic Sakespho oides c is a us is widely dis ibu ed in
he Caa inga domain, being cu en ly ega ded as mono-
ypic. Based on ou ield obse a ions and he examina-
ion o emale specimens, which led o he i s insigh s
on plumage and song a ia ion in Sakespho oides, cou-
pled wi h published e idence on ocal a ia ion de ec ed
ac oss he São F ancisco Ri e (Capelli e al.,2020), he ein
we e alua ed whe he gene ic di e en ia ion and ixed
pheno ypic di e ences would also be ound on opposi e
banks o he São F ancisco Ri e (he ea e SFR). We also
es ed wi h he molecula da a whe he any di e en ia-
ion ac oss he SRF would co ela e empo ally wi h he
es ablishmen o i s mode n cou se. Finally, we ca ied
ou ecological niche modelling and his o ical demog aphy
analyses o e alua e any cong uences in dis ibu ion and
popula ion sizes o S. c is a us ac oss he Caa inga do-
main media ed by Qua e na y clima ic oscilla ions.
2
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METHODS
2.1
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Sampling
We s udied and analysed plumage and mo phome ic
a ia ion in a o al o 1079 Sakespho oides c is a us speci-
mens (818 males, 261 emales) including s udy skins
(n = 92) and digi al pho og aphs a ailable in online da a-
bases (n = 987; TableS1). To in es iga e song a ia ion, we
analysed a o al o 115 di e en sound eco dings (n = 95
loudsongs, n = 29 calls; mo e han one ocaliza ion ype
KEYWORDS
bioacous ics, biogeog aphy, in eg a i e axonomy, niche modelling, São F ancisco Ri e
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489
CERQUEIRA e al.
could be p esen in he same eco ding) a ailable in on-
line da abases (TableS2).
We sequenced 58 issue samples om h oughou S.
c is a us ange (TableS3), 39 o hem belonging o he le
bank and 19 o he igh bank o he SFR. As ou g oups, we
used sequences o 29 Thamnophilidae species closes e-
la ed o he S. c is a us om GenBank based on opologies
o phylogenies in e ed by B um ield and Edwa ds(2007)
and B a o e al.(2021; see TableS4 o species names and
GenBank accession numbe s).
We ga he ed all a ailable occu ence eco ds o S. c is a-
us (n = 568) o En i onmen al Niche Modelling (ENM)
om he Species Link da abase (h p:// splink. c ia. o g.
b ), Sound a chi e Xeno- can o (h p:// www. xeno- can o.
o g), Wikia es (h p:// www. wikia es. com. b ), Ve ne
(h p:// www. e n e . o g/ index. h ml), Ebi d (h p:// www.
ebi d. o g/ ), and museum specimens deposi ed a Museu
Pa aense Emílio Goeldi (MPEG), Museu de Zoologia
da Uni e sidade de São Paulo (MZUSP), Uni e sidade
Fede al de Pe nambuco (UFPE), Uni e sidade Fede al
do Rio G ande do No e (UFRN), Uni e sidade Es adual
de Fei a de San ana (UEFS), and pe sonal obse a ions
ga he ed du ing ieldwo k. We inspec ed all occu ences
o e o s in locali y names and geog aphic coo dina es
by compa ison wi h he B azilian o ni hological gaze ee
(Payn e J & T aylo J .,1991).
2.2
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Plumage and
mo phome ic analyses
To documen geog aphic a ia ion in plumage pa e ns,
we analysed s udy skins and digi al pho og aphs. We used
cha ac e s wi h disc e e a ia ion such as colou s o he
c own, back, h oa , b eas , ail, and p esence o ba ing
and s eaks. All colou s anda diza ions we e based on
Smi he(1975). We s udied he ype se ies o S. c is a us
h ough high quali y digi al pho os, which include an
adul male (AMNH 6819), an adul emale (AMNH 6820)
and a ju enile emale (AMNH 6821) held a he Ame ican
Museum o Na u al His o y, New Yo k, USA.
We used a digi al callipe (nea es 0.1 mm) o measu e
he ollowing cha ac e s in s udy skins o 24 emales and
54 males (TableS1): (1) leng h o la ened wing (LW), (2)
a sus leng h (Ta L), (3) ail leng h (TaiL), (4) bill leng h
om he skull inse ion (BL1), (5) bill leng h om an e io
edge o nos ils (BL2), (6) bill wid h a an e io edge o
nos ils (BW), and (7) bill dep h a an e io edge o nos-
ils (BD). We es ed o signi ican di e ences in hese
measu emen s using ANOVA wi h a Tukey es o a pos-
e io i compa ison using a da ase composed o males and
emales. Gi en hei o e all plumage conse a ism, males
we e assigned o di e en g oups ollowing he geog aphic
loca ion o emales. We es ed all measu emen s o ho-
mogenei y o a iance and no mali y be o e ANOVA, and
pe o med s a is ical analyses using he package ‘s a s' in
R so wa e e sion 4.3.1 (R Co e Team,2023).
To suppo ou in e p e a ions o he deg ee o ge-
ne ic and pheno ypic di e en ia ion in Sakespho oides,
we in e ed i s dispe sal abili y in compa ison o o he
Thamnophilidae species occu ing in d y open and humid
o es ege a ion ypes. To do so, we used mo phome ic
da a om he AVONET da ase (Tobias e al.,2022) o ex-
ac measu emen s and indices ela ed o wing size and
shape a ia ion (see TableS5 o he species and num-
be o indi iduals analysed), which a e ega ded as good
p oxies o ligh e iciency and dispe sal abili y in bi ds
(Cla amun ,2021; Cla amun & W igh ,2017). We con-
side ed he ollowing wing a ibu es: (1) wing Leng h
(leng h om he ca pal join o he ip o longes p ima y
in millime es); (2) Kipp's Dis ance (leng h om he ip
o he i s seconda y ea he o he ip o he longes p i-
ma y in millime es); (3) seconda y1 (leng h om he
ca pal join o he ip o he i s seconda y in millime-
es); and (4) Hand- Wing Index (100*DK/Lw, whe e DK is
Kipp's dis ance and Lw is wing leng h). We used he Hand-
Wing Index (HWI) and aw measu emen s e lec ing
wing shape and size o pe o m a P incipal Componen
Analysis (PCA) o de e mine whe he hese a iables can
explain dispe sal abili y a ia ion be ween Sakespho oides
and o he an bi d species wi h in e ed low dispe sal abil-
i y. We u he es ed o signi ican di e ences in mean
HWI be ween Sakespho oides and o he an bi d species as
a di ec compa ison o dispe sal capaci y, also conside ing
di e en axonomic and ecological g oupings (i.e. gene a
and en i onmen ype, see TableS5). We checked o no -
mali y and homogenei y o a iance p io o a K uskal–
Wallis es and a pai wise Wilcox es (Mann–Whi ney) i
di e ences in HWI exis ed. We pe o med all s a is ical
analyses using he package ‘s a s' in R so wa e e sion
4.3.1 (R Co e Team,2023).
2.3
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Vocal analyses
We used ocaliza ions o explo e pu a i e di e en ia ion
ac oss he SFR. Ini ially, we sea ched o quali a i e cha -
ac e s by isualizing spec og ams o loudsongs, which
a e cha ac e ized as sho se ies o ca. 10 no es, wi h he
ini ial no es being sha p and s iden , ollowed by a se-
ies o aspy no es (Zimme e al., 2003). We could no
assign homologies among calls due o he small numbe
o eco dings ac oss di e en loca ions in ou sample and
he high deg ee o a ia ion o his ocal ype in di e -
en s ess con ex s (i.e. playback, ma e con ac , p esence
o p eda o s).
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490
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CERQUEIRA e al.
All sound eco dings we e s anda dized be o e isu-
aliza ion. We con e ed all iles o ‘.WAV’ o ma , wi h
a sampling a e o 44,100 Hz and bi dep h o 16 bi s in
he mono pa e n. Spec og ams we e gene a ed and an-
alysed on so wa e Ra en P o 1.5 (Co nell Labo a o y o
O ni hology) wi h a Hamming window ype, window size
o 512 samples, a ime g id 90% o e lap, and DFT size o
2048 samples. We analysed he syn ax and no e s uc u e
quali a i ely h ough a blind inspec ion and g ouping
p in ed sonog ams, ollowed by an assessmen o whe he
he g oupings ma ched he pa e ns unde s udy, ollow-
ing he p ocedu e in Ca nei o e al.(2012).
We also measu ed some pa ame e s based on spec o-
g ams and oscillog ams: numbe o sha p no es (NN1),
du a ion o all sha p no es including he in e als be-
ween no es in seconds (s; DS1), pace o sha p no es sec-
ion (di iding NN1 by DS1; Pace1), highes and lowes
equency o all sha p no es in he z (Hz; HighF1 and
LowF1), del a equency o all sha p no es in he z (di e -
ence be ween HighF1 and LowF1; DF1), peak equency
o all sha p no es in he z ( he equency a which maxi-
mum powe occu s wi hin he selec ion; PeakF1), numbe
o aspy no es (NN2), du a ion o all aspy no es includ-
ing he in e als be ween no es in seconds (DS2), pace o
aspy no es sec ion (di iding NN2 by DS2; Pace2), peak
equency o all aspy no es in he z (PeakF2), numbe o
no es along he en i e song (NN), du a ion o o al song
including he in e als be ween no es in seconds (DTS),
pace o o al song (di iding NN by DTS; Pace), and peak
equency along he en i e song in he z (PeakF). We in-
es iga ed signi ican di e ences in hese measu emen s
using an ANOVA wi h a Tukey es o a pos e io i com-
pa ison. We es ed all measu emen s o homogenei y o
a iance and no mali y be o e pe o ming ANOVA, we
pe o med s a is ical analysis using he package ‘s a s' in
R so wa e e sion 4.3.1 (R Co e Team,2023).
2.4
|
DNA ex ac ion,
ampli ica ion, and sequencing
We ex ac ed DNA samples om muscle issues o se-
quence wo mi ochond ial (NADH dehyd ogenase subu-
ni 2– ND2 and Cy och ome b – Cy b) and one nuclea
ma ke s (Glyce aldehyde 3- Phospha e Dehyd ogenase –
G3PDH). To al DNA was ex ac ed using s anda d p oce-
du es wi h he phenol- chlo o o m echnique (Samb ook
e al., 1989). We pe o med ampli ica ions using a
Polyme ase Chain Reac ion (PCR) unde he ollowing
ampli ica ion p o ile: 12.5 μL o Mas e Mix 1x, 8.5 μL
o H2O, 1.0 μL (200 ng/μL) o each p ime ( o wa d and
e e se) o all genes (see TableS6) and 2.0 μL (20 ng) o
genomic DNA. P ocedu es o genes Cy b and G3PDH
included an ini ial cycle o 5 min a 94°C, ollowed by 35 cy-
cles o 1 min a 94°C, 1 min a 57°C o Cy b and 55°C o
G3PDH (annealing empe a u e), and 1 min a 72°C, wi h
a inal ex ension o 5 min a 72°C. Fo he ND2 agmen ,
he PCR eac ion consis ed o an ini ial cycle o 5 min a
94°C, ollowed by 35 cycles o 30 s a 94°C, 1 min a 55°C
(annealing empe a u e), and 30 s a 72°C, wi h a inal ex-
ension o 5 min a 72°C. An aliquo o each ampli ica ion
was loaded in 1% aga ose gel o check o he ampli ica-
ion p oduc s. Then, he ampli ied p oduc s we e pu i ied
using PEG- 8000 (Polie ilenoglicol- 8000) o emo e PCR
esidues. We sequenced he amplicons wi h a Big Dye
Te mina o Cycle Sequencing S anda d Ve sion 3.1 ki s
in an au oma ed sequence model ABI 3130 (Applied
Biosys ems). Sequences gene a ed in his s udy we e de-
posi ed in GenBank (www. ncbi. nlm. nih. go ; Accession
Numbe s PP842021–PP842121).
2.5
|
Phylogene ic analyses and
gene ic dis ances
We edi ed and inspec ed sequences o any inse ions,
dele ions and s op codons, using he so wa e BioEdi
7.1.3 (Hall, 1999). The alignmen was pe o med using
Clus alW algo i hm implemen ed in he same so wa e
BioEdi 7.1.3. He e ozygous si es o nuclea ma ke s we e
ansla ed ollowing he IUPAC code.
We es ima ed he e olu iona y model ha bes ex-
plained he ob ained sequences in jModelTes 2.1.4
(Da iba e al.,2012), and subsequen ly used in a Bayesian
In e ence (BI) o es ima e phylogene ic ela ionships
among he specimens sequenced wi h M Bayes 3.1.2
(Ronquis & Huelsenbeck, 2003). Analyses o he con-
ca ena ed da ase we e pa i ioned by gene. Fou pa -
allel simul aneous uns o 3 × 106 gene a ions each
we e ca ied ou , sampling one ee e e y 1000 gene a-
ions. We used he So wa e TRACER 1.5 (Rambau &
D ummond,2009) o e i y consis ency o esul s and o
check whe he E ec i e Sample Size (ESS) alues we e
g ea e han 200 (D ummond e al.,2007). T ees ob ained
be o e he Ma ko chain eached s able and con e gen
likelihood alues we e disca ded as bu n- in. To es ima e
gene ic dis ances be ween and wi hin lineages eco -
e ed in phylogenies we ob ained unco ec ed pai wise
p- dis ances based on he m DNA da ase using he so -
wa e MEGA 5.2 (Tamu a e al.,2011). We also compa ed
he gene ic di e gence be ween Sakespho oides lineages
wi h hose obse ed be ween closely ela ed/sis e species
pai s o o he Neo opical Suboscine passe ines (mainly
Thamnophilidae; see TableS7). This se o species include
bo h hose whose anges a e limi ed by majo Amazonian
i e s as well as some species li ing in sympa y o wi h
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491
CERQUEIRA e al.
allopa ic o pa apa ic anges no sepa a ed by a majo
i e (TableS7). We used sequences o he ND2 ma ke
ob ained om his s udy and GenBank, and analysed
hem wi h he so wa e MEGA 5.2 (Tamu a e al.,2011)
based on unco ec ed pai wise p- dis ances.
2.6
|
Coalescence- based species
delimi a ion (BPP)
To es o in e speci ic limi s and gene ic di e en ia-
ion wi hin S. c is a us we used he so wa e Bayesian
Phylogene ics and Phylogeog aphy (BPP; e sion 2.2).
BPP uses a Bayesian app oach o gene a e p obabili ies o
specia ion be ween closely ela ed axa, using mul ilocus
sequence da a and a phylogene ic hypo hesis as a guide
ee (Rannala & Yang,2003, 2013; Yang & Rannala,2010).
We pe o med BPP analysis using bo h algo i hms 0
and 1 wi h di e en ine- uning pa ame e s (ε o 0, and α
and m o 1) ollowing he so wa e's ecommenda ions o
e i y consis ency o esul s. To assess a ia ion o popula-
ion size pa ame e s, we simula ed h ee scena ios o p io
combina ions ep esen ing di e en ances al popula ion
sizes and di e en ages o sepa a ion be ween lineages: (1)
la ge e ec i e popula ion size (Ne) and deep di e gence
wi h gamma dis ibu ion p io s o θ (popula ion size) and
τ (di e gence ime) – G(1, 10) and G(1, 10); (2) small Ne
and shallow di e gences wi h gamma dis ibu ion p io s
o θ and τ – G(2, 2000) and G(2, 2000); and (3) la ge Ne
and shallow di e gences, wi h gamma dis ibu ion p io s
o θ and τ – G(1, 10) and G(2, 2000) (Smi h e al.,2013).
As a guide ee, we used he phylogene ic hypo hesis gen-
e a ed by BI desc ibed abo e, unning Ma ko chains o
100,000 gene a ions, and sampling e e y i e gene a ions.
BPP es s di e en opologies, collapsing nodes o he
guide ee and coun ing suppo alues. Specia ion p oba-
bili ies a e es ima ed om he sum o he p obabili ies o
all models o specia ion e en s a each node o he ee
guide. Daugh e lineages ( e minal axa) om nodes ha
had specia ion p obabili ies >0.95 unde all h ee p io
scena ios we e classi ied as species (Smi h e al.,2013).
2.7
|
Molecula da ing and species ee
To es ima e he di e gence ime among S. c is a us line-
ages e ealed by he BI phylogeny es ima es, we ca ied
ou a species ee app oach using he mul ilocus da ase
(m and nucDNA) in *BEAST (Heled & D ummond,2010).
We also es ima ed a sepa a e ime ee using m DNA in
he BEAST 2.4.7 package (Bouckae e al.,2014). Fo each
mul ilocus and mi ochond ial ime ee, we pe o med
wo independen uns o 1 × 107 gene a ions, sampling he
pa ame e s o he Ma ko chain e e y 10,000 gene a ions,
un il he ESS o all pa ame e s eached sco es o 200. We
se o he m DNA da ase (Cy b and ND2) he mu a ion
a e o 2.1% o nucleo ide subs i u ions pe million yea s
(Wei & Schlu e ,2008), whe eas ha o he nuclea locus
(G3PDH) was es ima ed in compa ison o ha o he
m DNA a e unde elaxed clock and unco ela ed log-
no mal op ions and a Yule p ocess as a specia ion p io .
Based on he ob ained esul s, he i s 1000 samples o
each un we e disca ded as bu n- in. We es ima ed alues
o pos e io p obabili y and di e gence imes h ough a
majo i y ule consensus o he emaining samples.
2.8
|
His o ical demog aphy
To in es iga e he his o ical demog aphy o S. c is a us
lineages we used he Ex ended Bayesian Skyline Plo
(EBSP; Heled & D ummond,2008) unde a linea model
in BEAST 2.4.7 (Bouckae e al.,2014). EBSP es ima es
changes in e ec i e popula ion sizes o e ime unde
a mul ilocus app oach by using he imes o coalescen
e en s among gene ees. We used his me hod o es
demog aphic p edic ions expec ed unde he Re ugia
Hypo hesis o Pleis ocene clima ic oscilla ions and o
e alua e o cong uence be ween his o ical demog aphy
and ange size changes scena ios p edic ed by ecological
niche modelling o each lineage du ing he d ies pe i-
ods. We an he analysis o 1 × 107 gene a ions unde an
unco ela ed logno mal molecula clock wi h a subs i u-
ion a e o 2.1% pe million yea s applied o he m DNA
da ase (Wei & Schlu e ,2008), using his a e o es ima e
compa a i ely ha o he nuclea locus.
2.9
|
Ecological niche modelling (ENM)
To es ima e he clima ic niche dynamics o he di e en
S. c is a us lineages in he las 120 ka we used 19 biocli-
ma ic laye s a 30 a c- seconds (~1 km2) o he ollowing
empo al window scena ios (see TableS8 o de ails o bi-
oclima ic laye s): (1) cu en clima ic scena io a ailable
om he Wo dClim da abase (h p:// www. wo ld clim.
o g/ cu en , Hijmans e al.,2005); (2) Middle Holocene
(~6 ka) and Las Glacial Maximum (LGM, ~21 ka) ob-
ained om Ecoclima e (h p:// www. ecocl ima e. o g/ ,
Lima- Ribei o e al.,2015; Va ela e al.,2015); and (3)
Las In e glacial (LIG, ~120 ka) da a ob ained ollowing
p ocedu es desc ibed in O o- Bliesne e al.(2006). The
clima ic da a used was based on he same gene al ci -
cula ion model (GCM) a ailable o all paleoscena ios:
he Communi y Clima e Sys em Model (CCSM). We
pe o med a Pea son's co ela ion es o all bioclima ic
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CERQUEIRA e al.
a iables and emo ed he mos highly co ela ed
( > 0.8) o a oid collinea i y and model o e i ing.
The ea e , we selec ed six bioclima ic a iables o use
in models: Mean Diu nal Range (BIO2), Tempe a u e
Seasonali y (BIO4), Annual P ecipi a ion (BIO12),
P ecipi a ion Seasonali y (BIO15), P ecipi a ion o
Wa mes Qua e (BIO18) and P ecipi a ion o Coldes
Qua e (BIO19). Ou occu ence da a was pa i ioned
ollowing he ‘checke boa d’ me hod (Musca ella
e al.,2014; Vala i e al.,2018), whe eby he occu ence
da a is di ided in geog aphic g ids o maximize he en i-
onmen al independence and simila i y among subse s.
We used a ROC's h eshold o cu he sui abili y ma i-
ces modelled, which equalizes he omission and com-
mission e o s (Ba be - Massin e al.,2012).
We e alua ed he ENMs using he T ue Skill S a is ic
(TSS; Allouche e al., 2006), a h eshold dependen
me hod anging om −1 o 1. Nega i e and posi-
i e alues close o ze o a e no be e han expec ed
by chance; alues be ween 0.6 and 0.8 deno e ea-
sonable i models, whe eas good i models a e indi-
ca ed by alues g ea e han 0.8, wi h 1 deno ing bes
model i (Allouche e al.,2006; Coe zee e al.,2009).
We used a combined esul o he ollowing ou di -
e en algo i hms o model he species dis ibu ion and
ob ain a mo e eliable es ima e o he en i onmen-
al niche (Rocchini e al., 2011): Gene alized Linea
Model (GLM), Maximum En opy (Maxen ), Suppo
Vec o Machines (SVM) and Random Fo es (RF; Guo
e al., 2005, Phillips e al., 2006, P asad e al., 2006,
Schölkop e al.,2001, Tax & Duin,2004).
The inal model o cu en ime and hose p ojec ed
o each paleoclima e scena io we e ob ained using a con-
sensus model o each S. c is a us lineage. We conside ed
only esul s wi h TSS alues highe han 0.6 ac oss he
ou algo i hms used, p esen ing maps wi h he sui abil-
i y mean o he es ima ed en i onmen al niche, named
‘ensemble’. We pe o med all p ocedu es and model i -
ing desc ibed abo e using he package ‘ENMTML’ (de
And ade e al.,2020) in R so wa e e sion 4.3.1 (R Co e
Team, 2023), a ailable a Gi Hub (h ps:// gi hub. com/
and e aa/ ENMTML).
To es o niche di e gence, we pe o med a
niche o e lap analysis be ween he wo eco e ed
Sakespho oides lineages o e i y whe he clima e has
in luenced hei G innellian niches (Sobe ón,2007). We
used he same 19 bioclima ic a iables and occu ence
da a om he ENM analysis and pe o med a calib a ed
PCA (PCA- en ) on he en i onmen al space o bo h
lineages, including all occu ences. We calcula ed he
niche o e lap using Schoene 's D simila i y me ic ang-
ing om 0 (no o e lap) o 1 ( o al o e lap; B oennimann
e al.,2012). We also pe o med an iden i y es o check
he s a is ical signi icance o he ob ained niche o e -
lap me ics h ough 1000 eplica es o gene a e a null
dis ibu ion h ough simila i y and equi alency es s. I
he alues o niche o e lap me ics anged wi hin 95%
o he simula ed null dis ibu ion, he null hypo hesis
(niche o e lap) canno be ejec ed. We ca ied ou he
analysis using a se o packages (‘ecospa ’, ‘ geos', ‘ as-
e ’, ‘ idy e se’ and ‘geoda a’) in R so wa e e sion 4.3.1
(R Co e Team,2023).
3
|
RESULTS
3.1
|
Plumage and mo phome ic
analyses
O he 1079 indi iduals (skins and pho og aphs) analysed,
we could no iden i y any diagnos ic plumage di e ences
among males (n = 818), bu wo main plumage pa e ns in
emales (n = 261) we e diagnosed mos ly ac oss he SFR
(Figu e1).
The i s pa e n (he ea e plumage pa e n 1) is cha -
ac e ized by emales wi h ails showing la ge black and
whi e bands and some ‘ u ous- ches nu ’ only on he edges
o ec ices and nea he whi e bands, in addi ion o an
Ambe c es and oli e b own back. In con as , emales
sha ing he second pa e n (he ea e plumage pa e n
2) ha e en i ely ‘ u ous- ches nu ’ ails, wi h weak da k
b own ma ks, plus Ches nu c es s and Cinnamon- B own
backs (Table1; Figu eS1).
We could no de ec sexual dimo phism in S. c is a-
us o he mo phome ic cha ac e s measu ed acco d-
ing o ANOVA es s. Howe e , when bo h emale and
male specimens belonging o he wo dis inc g oups
de ined based on he plumage o emales a e con as ed,
ail leng h (TaiL) and bill leng h om c anium inse ion
(BL1) we e he only mo phome ic cha ac e s ha a -
ied signi ican ly (p < .05; Table2). Despi e hese s a is i-
cal di e ences nei he measu emen can be ega ded as
diagnos ic be ween he wo g oups due o b oad o e lap
(Table2).
Based on wing size and shape a ibu es, we ound
no di e ences in in e ed dispe sal abili y be ween
Sakespho oides and o he an bi d species om bo h d y
and we en i onmen s (Figu eS2), including species wi h
ecognized low dispe sal ea u es and gene ic di e en ia-
ion ac oss Amazonian i e s (Figu eS2). The PCA anal-
ysis explained 99.8% o o al a iance in he i s wo axes
(PC1: 65.28%, PC2: 34.51%), wi h Sakespho oides ha ing a
g ea o e lap in space wi h o he species om bo h d y and
we en i onmen s (Figu eS2a–c). While a iables ela ed
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CERQUEIRA e al.
o wing size we e posi i ely co ela ed wi h PC1, he Hand-
wing index was highly and nega i ely co ela ed wi h PC2
(TableS9). Specimens o Sakespho oides clus e ed on
he op le co ne o he PCA g aph and, he e o e, we e
cha ac e ized by smalle wing size and Hand- wing Index
alues, ypically associa ed wi h species o lowe dispe sal
capaci y. To ein o ce his pa e n, we ound a signi ican
di e ence in Hand- wing Index be ween axa om dis inc
d y and we habi a s (p < .05; Figu eS2 ), wi h d y habi a
species (which includes Sakespho oides) showing signi i-
can ly smalle Hand- wing Index alues han we habi a
species (Figu eS2d,e).
3.2
|
Vocal analyses
Based on spec og ams o 95 sound eco dings classi ied
as loudsongs, we also de ec ed wo diagnosable ocal pa -
e ns oughly sepa a ed by he SFR in bo h males and
emales, consis en wi h di e ences de ec ed in emale
plumage pa e ns (Figu e2).
No sexual dimo phism was iden i ied in spec og ams
o eco dings ela i e o sound s uc u e and no e shape.
The i s diagnos ic loudsong ype (he ea e ocal pa e n
1), is cha ac e ized by an ini ial se ies o sha p no es wi h
equency modula ion ( apid inc ease and dec ease, like an
FIGURE 1 Geog aphic dis ibu ion o diagnos ic plumage cha ac e s in Sakespho oides c is a us emales. G een and blue ci cles
ep esen diagnos ic pa e ns numbe ed 1 and 2, espec i ely, eco e ed om plumage analyses using s udy skins and digi al pho og aphs
(see ex o de ails). The da k- blue line ep esen s he mode n cou se o he São F ancisco Ri e (SFR), wi h he ed dashed lines
ep esen ing he es ima ed posi ion o abandoned meande s o a La e Pleis ocene paleocou se o he SFR. The colou g adien ep esen s
al i udinal a ia ion. C edi pho os: Rocílio Ribei o Rocha (pa e n 1) and Obe dan Nunes (pa e n 2).
Pa e n 1 Pa e n 2
C own Ambe (Colou 36) Ches nu (Colou 32)
Back Oli e b own (Colou 28) Cinnamon- B own (Colou 33)
Th oa Pale ho n Colou (Colou 92) Pale ho n Colou (Colou 92)
B eas Bu (Colou 124) Bu (Colou 124)
Belly Bu (Colou 124) Bu (Colou 124)
Tail Je Black (Colou 89), Whi e and
Ambe (Colou 36) bands
Ambe (Colou 36) and da k
Ambe
TABLE 1 Diagnos ic body- pa colou
compa isons o emale skins belonging o
wo dis inc plumage pa e ns eco e ed
in Sakespho oides c is a us. Colou
nomencla u e ollows Smi he(1975).
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CERQUEIRA e al.
Cha ac e sa
Pa e n 1 Pa e n 2
(n = 59) (n = 19)
Mean SD Min- Max Mean SD Min–Max
LW 66.95 (a) 2.06 63–72 67.79 (a) 1.65 64–71
Ta L 25.28 (a) 0.93 23.46–26.85 25.32 (a) 1.04 23.69–27.33
TaiL 57.03 (b) 4.04 48–68 61.74 (a) 2.86 56–67
BL1 17.75 (a) 0.73 15.14–19.23 16.87 (b) 0.9 14.63–18.59
BL2 10.09 (a) 0.53 9.08–11.81 10.02 (a) 0.39 9.09–10.67
BW 4.08 (a) 0.38 3.4–4.95 4.26 (a) 0.32 3.61–4.75
BD 5.18 (a) 0.31 4.71–6.08 5.29 (a) 0.28 4.77–5.80
No e: Males we e assigned o each g oup based on he geog aphic loca ion o emales (Figu e1). All
measu emen s a e in millime es (mm), wi h epo ed sample sizes (n), mean plus s anda d de ia ion
(±SD), ollowed by minimum- maximum alues. Mean alues ollowed by di e en le e s in pa en hesis
on he same line di e signi ican ly by p < .05 (in bold).
aMo phome ic cha ac e s: BD, bill dep h a an e io edge o nos ils; BL1, bill leng h om c anium
inse ion; BL2, bill leng h om an e io edge o nos ils; BW, bill wid h a an e io edge o nos ils; LW,
leng h o la ened wing; TaiL, ail leng h; Ta L, a sus leng h.
TABLE 2 Measu emen s o
mo phome ic cha ac e s and s a is ical
compa isons among male and emale
specimens o Sakespho oides c is a us
belonging o wo dis inc plumage g oups
diagnosed only in emales (see ex o
de ails).
FIGURE 2 Geog aphic dis ibu ion o diagnos ic loudsong ypes o Sakespho oides c is a us eco e ed du ing ocal analyses. G een and
blue iangles ep esen he dis ibu ion o pa e ns 1 and 2, espec i ely. (a) Spec og am o ype 1 loudsong showing he sha p no es wi h
ascending–descending equency modula ion (in e ed ‘U' shape), accession numbe : XC320806; see de ailed iews o bo h sha p and aspy
no es unde he spec og am; (b) Spec og am o ype 2 loudsong showing he sha p no es wi h ascending–descending- s able- descending
equency modula ion ( u ned ‘S' shape), accession numbe : XC229164; see unde he spec og am de ailed iews o bo h sha p and aspy
no es. The da k- blue line ep esen s he cu en cou se o he São F ancisco Ri e (SFR), wi h ed dashed lines ep esen ing he es ima ed
posi ion o abandoned meande s o a la e Pleis ocene paleocou se o he SFR. The colou g adien ep esen s al i udinal a ia ion.
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495
CERQUEIRA e al.
in e ed ‘U’ in shape), ollowed by a sho se ies o inal aspy
no es (Figu e2). The second loudsong ype eco e ed (he e-
a e ocal pa e n 2), has he ini ial se ies o sha p no es
wi h a di e en ype o equency modula ion (i.e. apid in-
c ease, dec ease, sho du a ion s able and dec ease again, in
a sigmoid shape), and sho inal aspy no es (Figu e2).
Compa isons using ANOVA es e ealed se en ocal
cha ac e s wi h s a is ically signi ican di e ences be-
ween loudsong pa e ns 1 and 2: numbe o no es in o al
song (NN), du a ion o o al song (DTS), pace o o al song
(PTS), numbe o sha p no es (NN1), du a ion o all sha p
no es (DS1), highes equency o all sha p no es (HF1),
and del a equency o all sha p no es (DF1) (Table3).
Despi e hese s a is ical di e ences, none o he ocal
cha ac e s abo e can be used as diagnos ic be ween he
wo ocal ypes due o o e lap (Table3). In summa y,
loudsong pa e n 1 is signi ican ly longe , ye slowe and
lowe pi ched han loudsong pa e n 2.
3.3
|
Phylogene ic analyses
Ou esul s based on BI phylogenies o he combined
m DNA and nuclea da ase s eco e ed wi h high
s a is ical suppo ha Sakespho oides c is a us is no
ela ed o o he Sakespho us species, consis en wi h
he opologies in B um ield and Edwa ds (2007) and
B a o e al.(2021). Despi e he o e all unce ain y wi h
espec o he ue S. c is a us ou g oup, ou phylog-
eny es ima es eco e ed his species as monophyle ic
(Figu e3).
Wi hin he monophyle ic S. c is a us, wo s a is-
ically well suppo ed independen gene ic g oups
we e eco e ed oughly eplacing each o he ac oss
he SFR (Figu e3; Figu eS3), wi h clade 1 ound o
he mos pa wes and no h o he i e and clade 2
mos ly eas and sou h o i . Bo h clades a e in close
and di ec con ac on he wes bank o he mid-
dle SFR in Wes e n Bahia. The unco ec ed gene ic
dis ance be ween clades 1 and 2 is 1.8% (s anda d
e o ± 0.3%), whe eas ha wi hin each clade is 0.2%
(s anda d e o ± 0.1%). This a e age pai wise gene ic
dis ance is simila o hose ound be ween some pai s
o closely ela ed ‘biological’ species o an bi ds such
as Rhegma o hina be lepschi/Rhegma o hina ho -
mannsi (1%) and He psilochmus a icapillus/He p-
silochmus pilea us (1.7%; see TableS7 o comple e
compa ison).
TABLE 3 Va ia ion in loudsong cha ac e s and s a is ical compa isons be ween wo song ypes in Sakespho oides c is a us.
Measu emen a
Pa e n 1 Pa e n 2
(n = 19) (n = 30)
Mean SD Min–Max Mean SD Min–Max
NN 12.74 (a) 1.33 10–15 11.1 (b) 1.42 08–14
DTS 3.04 (a) 0.39 2.35–3.56 2.47 (b) 0.29 1.76–3.06
Pace 4.21 (b) 0.37 3.65–5.09 4.51 (a) 0.39 3.61–5.42
PeakF 1707.94 (a) 97.38 1485.8–1938.0 1669.55 (a) 117.35 1442.7–1894.9
NN1 10 (a) 1.10 08–12 8.8 (b) 1.54 06–13
DS1 2.37 (a) 0.34 1.69–2.87 1.95 (b) 0.28 1.37–2.52
Pace1 4.25 (a) 0.45 3.58–5.20 4.51 (a) 0.47 3.64–5.62
HighF1 2186.44 (b) 210.78 1817.2–2626.0 2380.9 (a) 188.74 1964.4–2778.0
LowF1 576.12 (a) 141.29 368.5–934.2 553.11 (a) 125.85 341.9–788.9
DF1 1610.32 (b) 216.54 1110.0–1975.0 1834.84 (a) 232.75 1175.6–2243.5
PeakF1 1707.94 (a) 97.38 1485.8–1938.0 1662.37 (a) 119.20 1442.7–1894.9
NN2 2.74 (a) 0.93 1–4 2.3 (a) 0.84 1–5
DS2 0.6 (a) 0.22 0.22–1.06 0.6 (a) 0.76 0.14–4.51
Pace2 4.69 (a) 0.92 2.66–6.04 5.07 (a) 1.23 0.22–7.41
PeakF2 1712.46 (a) 198.96 1162.8–1981.1 1689.65 (a) 107.85 1507.3–1938.0
No e: F equency is p esen ed in he z (Hz) and du a ion a iables in seconds (s). Pace o no es pe second is he o al numbe o no es coun ed wi hin a
pa icula ime in e al. Sample sizes (n), mean ± SD, ollowed by minimum- maximum alues a e p esen ed o each cha ac e . Fo each cha ac e , any means
in bold ollowed by di e en le e s in pa en hesis depic signi ican di e ences a p < .05.
aMeasu emen keys: DF1, del a equency o sha p no e sec ion (HighF1 − LowF1); DS1, du a ion o all sha p no es including in e al no es; DS2, du a ion o
all aspy no es including in e al no es; DTS, du a ion o o al song; HighF1, highes equency o sha p no e sec ion; LowF1, lowes equency o sha p no e
sec ion; NN, numbe o no es along he en i e song; NN1, numbe o sha p no es; NN2, numbe o aspy no es; Pace, pace o o al song; Pace1, pace o sha p
no es sec ion; Pace2, pace o aspy no es sec ion; PeakF, peak equency along he whole song; PeakF1, peak equency o sha p no es sec ion; PeakF2, peak
equency o aspy no es sec ion.
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CERQUEIRA e al.
con idence in e als do no ule ou a La e Pleis ocene
da e (1.313–0.366 Mya), pa icula ly ha ob ained wi h
he coalescen species ee app oach (Figu e3). Du ing
he Middle Pleis ocene, he SFR cou se became in e -
up ed o he no h, whe e i connec ed o he Piauí and
Pa naíba i e s, and u ned in o a lacus ine/palus ine
sys em (Mabesoone,1994; Po e ,2003). Acco ding o he
paleolacus ine hypo hesis, du ing he Middle Pleis ocene,
he SFR became an endo heic d ainage emp ying in o
a lu io- lacus ine en i onmen in i s middle po ion
be ween Remanso and Pe olina (Mabesoone, 1994;
Rod igues, 1986, 2006; T ica , 1974). The changing pa-
leo- SFR cou se and he la ge swampy en i onmen in he
Remanso – Pe olina a ea could ha e played a ole in isola -
ing he ances o o S. c is a us and S. niedeguidonae in wo
popula ions. Subsequen ly, du ing he Mindel glacia ion
(~450 kya), he paleo- SFR cou se shi ed adically sou h-
eas wa d in o he A lan ic Ocean, e en ually eaching i s
cu en posi ion a e some ex ensi e meande ing sou h o
he mode n mou h, as e ealed by se e al su aces in e -
p e ed as paleochannels (King,1956; Mabesoone,1994).
The con idence in e als o ou es ima e o he spli ing
imes be ween bo h Sakespho oides species ma ch his pe-
iod o ex ensi e changes in he SFR cou se and could be
ela ed o hei o igin.
Indeed, he con igu a ion o he lowe SFR La e
Pleis ocene cou se sou h o i s mode n posi ion is cong u-
en wi h he geog aphic a ia ion in pheno ypic cha ac e s
documen ed be ween S. c is a us and S. niedeguidonae,
such as loudsong and plumage, known o be impo -
an ea u es in ma e ecogni ion (Isle e al.,1998, 2007;
Remsen J .,1984). Subsequen o i s majo shi sou heas -
wa d, a second d ainage shi e en p obably media ed by
e osional p ocesses and clima e change mo ed he SFR
lowe mos cou se no hwa d o i s cu en posi ion; e i-
dence ound in sedimen s sugges s he es ima ed posi ion
o his ecen paleocou se be ween he mode n cou ses o
he I apicu u and Vaza- Ba is i e s (King,1956). This led
o he es ablishmen o a a he ecen seconda y con ac
zone be ween S. niedeguidonae popula ions om ‘Raso da
Ca a ina’ egion (which could ha e been passi ely ans-
e ed om he le o he igh bank o he SFR) and hose
o S. c is a us, which we e p e alen on he igh bank
o he i e ( o simila pa e n in o he species see also
We neck e al.,2015). This pa e n o pu a i e ecen sec-
onda y con ac o he wo Sakespho oides species is co -
obo a ed by ou molecula phylogeny (mainly based on
he mi ochond ial da ase , wi h he only nuclea gene se-
quenced p o iding inconclusi e e idence), which g oups
specimens S. niedeguidonae om Raso da Ca a ina in he
S. c is a us clade. The incong uence be ween geno ype
and pheno ype can esul ei he om mi ochond ial in-
og ession due ecen seconda y con ac o e en ion o
ances al polymo phism due o incomple e lineage so ing
(Dias e al.,2018; Fe ei a e al.,2018). We did no ob ain
any e idence o ac ual gene low analysing plumage and
ocal pa e ns, bu ei he a o me selec i e mi ochon-
d ial sweep o pas /cu en gene low migh explain he
obse ed misma ch be ween gene ic and pheno ypic cha -
ac e s in S. niedeguidonae Raso da Ca a ina popula ions.
Fu u e s udies should add ess he dynamics o his con-
ac zone by inc easing he numbe o molecula loci and
indi iduals sampled.
Bo h S. c is a us and S. niedeguidonae a e also in
appa en con ac in Wes e n Bahia Region (WBR, see
Figu eS6 o de ailed iews), whe e S. c is a us has
‘c ossed’ on o he le bank o he middle SFR p obably
media ed by changes in i e low caused by e osion and
sedimen a ion (Ba e o,1996; T ica ,1974). This p ocess
c ea ed o saken meande s ha ans e ed popula ions
ac oss i e banks o e en connec ed bo h banks in d ie
pe iods du ing he es ablishmen o a lacus ine sys em
down i e in he Middle Pleis ocene (Ba e o,1996; see
also below). Ou sampling om his pa icula a ea in-
dica es cong uency be ween molecula and pheno ypic
a ia ion in bo h S. c is a us and S. niedeguidonae, in
con as o wha we documen ed in he Raso da Ca a ina
egion. Addi ionally, we ound ha S. c is a us and S.
niedeguidonae a e no syn opic in WBR, bu ins ead sep-
a a ed by ca. 40 km ac oss an a ea domina ed by Ce ado
and an an h opogenic landscape esembling a o me i-
pa ian ege a ion. Ce ado /Caa inga eco ones a e com-
mon in his egion, and we could no ind any sui able
habi a and indi iduals o bo h species on his na ow
Ce ado pa ch, concluding ha i could wo k as an en-
i onmen al ba ie p e en ing hei di ec con ac and
possibly gene low. Ne e heless, occu ence o hyb ids
o in og ession e en s in hese egions canno be com-
ple ely uled ou .
Recen ly, some s udies ha e ound pa e ns cong u-
en wi h gene ic s uc u e media ed by he SFR in mam-
mals, liza ds, insec s, and ogs (B uschi e al., 2019;
Cou inho- Ab eu e al.,2008; Fa ia e al.,2013; We neck
e al.,2015). The ole o i e s as ba ie s and specia ion
d i e s is be e unde s ood in he Amazon Fo es , and
he SFR ep esen s a new sys em o s udy complex pa -
e ns o specia ion wi h mechanisms including mul iple
changes in i e cou ses, Qua e na y clima e change,
and neo ec onism. In ou compa isons using he Hand-
wing index as a p oxy o dispe sal abili y, we e i ied
ha Sakespho oides spp. a e low agili y an bi ds like
o he species li ing in he unde s o y o Amazonian
o es , which is cong uen wi h hei habi a selec ion
and beha iou pa e ns (e.g. small e i o ies and mo e-
men s h ough sho ligh s in middle o dense low eg-
e a ion). The gene ic, pheno ypic, and mo phome ic
14636409, 2024, 5, Downloaded om h ps://onlinelib a y.wiley.com/doi/10.1111/zsc.12672 by Capes, Wiley Online Lib a y on [25/06/2025]. See he Te ms and Condi ions (h ps://onlinelib a y.wiley.com/ e ms-and-condi ions) on Wiley Online Lib a y o ules o use; OA a icles a e go e ned by he applicable C ea i e Commons License
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503
CERQUEIRA e al.
e idence shown he e suppo he hypo hesis ha he
SFR es ablishmen played a e y impo an ole in he
di e si ica ion o Sakespho oides by ac ing as a s ong
ba ie o dispe sion, whose e ec s a ied in ime and
di e en loca ions.
4.2
|
The in luence o qua e na y
clima ic oscilla ions
We also e alua ed he in luence o Qua e na y clima ic
oscilla ions in Sakespho oides using paleodis ibu ion
modelling and in e ences o pas popula ion sizes h ough
ime (EBSP). Ou esul s a e pa ially consis en wi h
p edic ions o he Re ugia Hypo hesis o D y Fo es s
(Ha e ,1969; Ha e & P ance,2001), suppo ing bo h de-
mog aphic and paleodis ibu ion ange expansions du ing
and sho ly a e he LGM (~22 kya), p eceded by smalle
popula ion sizes and mo e es ic ed dis ibu ion anges
du ing LIG (~120 kya; Figu e4). The eco e ed pa e n
o sympa y be ween bo h species in WBR was likely a
seconda y con ac as suppo ed by paleoen i onmen-
al e idence indica ing a educ ion in wa e le els o he
middle SFR esul ing in inc easing sand deposi ion du -
ing ho and d y pe iods ha could ha e p omo ed con-
nec ions and a s epping- s one dispe sion ac oss opposi e
banks (Ba e o,1996). So, we hypo hesized ha clima ic
oscilla ions a e di e si ica ion e en s media ed by he
SFR could ha e shi ed he anges o bo h Sakespho oides
species, possibly p omo ing seconda y con ac by expan-
sion du ing d ie pe iods and isola ion again by e ac ion
du ing mesic pe iods, ein o cing hei gene ic and phe-
no ypic di e en ia ion in a eas o sympa y, as in WBR
(B uschi e al.,2019).
The Qua e na y clima ic oscilla ions p omo ed niche
e olu ion in some species, mainly in o ganism wi h as
li e cycles like bees (Sil a e al.,2014). Bu we did no ind
e idence o G innellian niche e olu ion o di e gence
be ween bo h species o Sakespho oides, he small niche
o e lap eco e ed was no s a is ically signi ican indica -
ing ha bo h species canno be di e en ia ed by occupied
niche. Specia ion is no commonly associa ed wi h an eco-
logical inno a ion o niche e olu ion and appea s o be
mo e no iceable a he in o he pas as in gene a o amily
le els (Pe e son,2011; Pe e son e al.,1999).
The Re ugia Hypo hesis has been es ed in he
Neo opical egion mos ly using humid o es axa
(Ba alha- Filho e al.,2013; Ba alha- Filho & Miyaki,2016;
Menezes e al., 2017; San os e al., 2018; Solomon
e al.,2008). S udies ocused on Caa inga axa ound e -
idence o popula ion and/o ange expansions as we did
o Sakespho oides (Cae ano e al.,2008; Cou inho- Ab eu
e al., 2008; Fa ia e al., 2013; Nascimen o e al., 2013;
Oli ei a e al.,2015; Thomé e al.,2016). Recen ly, Geha a
e al.(2017) eco e ed a s ong signal o synch onous pop-
ula ion expansion in he La e Pleis ocene o ep iles and
amphibians wi h qui e di e en ecological adap a ions
and li e his o y s a egies, indica ing a s ong ole o cli-
ma ic oscilla ions in p omo ing e ec i e popula ion size
changes a e di e si ica ion e en s in he Caa inga auna.
Bo h Sakespho oides species ha e also expanded a con-
g uen imes in he La e Pleis ocene, as ound in Geha a
e al.(2017).
Fu u e s udies should es hese same spa io- empo al
pa e ns o expansion in o he Caa inga bi ds o e alua e
o sha ed esponses o clima e change among Caa inga
o ganisms.
ACKNOWLEDGEMENTS
We hank he cu a o s and cu a o ial assis an s o al-
lowing us he use o skins and issues held in he ol-
lowing ins i u ions: Museu Pa aense Emílio Goeldi
(MPEG), Uni e sidade Fede al de Pe nambuco (UFPE),
Uni e sidade Fede al do Rio G ande do No e (UFRN),
Uni e sidade Es adual de Fei a de San ana (UEFS)
and Museu de Zoologia da Uni e sidade de São Paulo
(MZUSP). We hanks Paul R. Swee and Thomas J.
T ombone om he Ame ican Museum o Na u al
His o y (AMNH) o p o iding high quali y pho o-
g aphs o he ype specimens. Ins i u o Chico Mendes
de Conse ação da Biodi e sidade (ICMBio) issued col-
lec ing pe mi s (#52349- 3). We a e especially g a e ul
o Gus a o Gonsio oski, Ci o Albano, C is ine P a es,
Chico Ras a, Fi mino Filho, And é Adeoda o and
‘Seu' Ca melo o all suppo du ing ou ieldwo k. To
Fe nando Pacheco o he aluable in o ma ion and ich
discussion abou Wied's i ine a y and Gus a o B a o
o discussions and sha ing unpublished da a du ing
he ea ly s ages o his p ojec . Thanks o Ma cos Pé sio
o he aluable ma e ial collec ed in he Caa inga du -
ing many yea s and all suppo be o e and du ing he
p ojec and o Andy and Gill Swash o discussions and
sugges ion o English names. We also hank ield e-
co dis s and bi de s who sha ed sound eco dings and
pho og aphs in he ollowing ci izen science pla o ms:
WikiA es, Xenocan o and Macaulay Lib a y (Co nell
Uni e si y). PC wa mly hanks all bi d wa che s ha
acqui ed his bi ding ou s se ices making possible he
ealiza ion o ieldwo k, as hey indi ec ly unded his
esea ch. Labo a o y wo k ela ed o his pape was
unded by a FINEp g an (# 0118003100). PC and GRG
we e suppo ed by Coo denação de Ape eiçoamen o
de Pessoal de Ní el Supe io – B asil (CAPES) Doc o al
ellowships (#1537057 and #1537056, espec i ely). AA
is suppo ed by a p oduc i i y ellowship om CNPq
(309243/2023- 8).
14636409, 2024, 5, Downloaded om h ps://onlinelib a y.wiley.com/doi/10.1111/zsc.12672 by Capes, Wiley Online Lib a y on [25/06/2025]. See he Te ms and Condi ions (h ps://onlinelib a y.wiley.com/ e ms-and-condi ions) on Wiley Online Lib a y o ules o use; OA a icles a e go e ned by he applicable C ea i e Commons License
504
|
CERQUEIRA e al.
ORCID
Pablo Ce quei a h ps://o cid.o g/0000-0002-7311-6229
Gab iela R. Gonçal es h ps://o cid.
o g/0000-0002-3581-4392
Tânia F. Qua esma h ps://o cid.
o g/0000-0001-8192-064X
Ma celo Sil a h ps://o cid.o g/0000-0003-0642-8246
Mau o Picho im h ps://o cid.
o g/0000-0002-9340-9010
Alexand e Aleixo h ps://o cid.
o g/0000-0002-7816-9725
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