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ECOGRAPHY
Ecog aphy
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This is an open access a icle unde he e ms o he C ea i e Commons
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Subjec Edi o :
Jose Alexand e Felizola Diniz-Filho
Edi o -in-Chie :
Dominique G a el
Accep ed 10 Ma ch 2024
doi: 10.1111/ecog.07200
2024
1–11
2024: e07200
© 2024 The Au ho s. Ecog aphy published by John Wiley & Sons L d on behal o No dic Socie y
Oikos
Uni ied models o biological di e si y ac oss o ganiza ional le els (genes, species, com-
muni ies) p o ide key insigh in o undamen al ecological p ocesses. Theo y p edic s
ha he s eng h o he co ela ion be ween species abundance and gene ic di e si y
should be ela ed o communi y age in closed communi ies (i.e. abundan species
accumula e mo e gene ic di e si y o e ime han a e species). Following his a io-
nale, we hypo hesize ha his o ical clima ic e en s a e expec ed o impac assembly
p ocesses, hence a ec ing bo h he species abundance dis ibu ion (SAD) and he spe-
cies gene ic dis ibu ion (SGD) in con inen al communi ies. The e o e, we p edic
ha , i he cong uence be ween SADs and SGDs depends on communi y age, hen
highe cong uence would be obse ed in locali ies whe e clima e has been mo e s able
since he Las Glacial Maximum (LGM). We es ed his p edic ion using ela i e abun-
dance and nucleo ide di e si y (cox1-5′) da a om 20 communi ies o lea bee les
along a la i udinal ansec in he Ibe ian Peninsula. We obse ed ha he cong uence
be ween SAD and SGD cu es, measu ed as he co ela ion be ween he species’ ank
o de s in bo h dis ibu ions, was signi ican ly ela ed o he change in mean annual
empe a u e since he LGM, bu no o cu en clima ic condi ions. Ou esul s sug-
ges ha , despi e he high connec i i y o con inen al communi ies, his o ical clima ic
s abili y is s ill a ele an p edic o o he cong uence be ween species abundance and
gene ic di e si y. Hence, he deg ee o cong uence be ween SADs and SGDs could be
used as a p oxy o communi y s abili y, ela ed no only o his o ical clima ic a ia ion
bu also o any o he dis up ing ac o s, including human p essu e.
Keywo ds: biodi e si y pa e ns, Coleop e a, communi y ba coding, Qua e na y
clima e, species–gene ic di e si y co ela ion (SGDC), uni ied models
In oduc ion
Uni ied mac oecological models ac oss o ganiza ional le els (genes, species, communi-
ies) p o ide p edic i e amewo ks ha open unique oppo uni ies o disce n he ole
o undamen al ecological p ocesses shaping he a ia ion o biological communi ies
Clima ic s abili y p edic s he cong uence be ween species
abundance and gene ic di e si y
Vic o ia Fo moso-F ei e ✉1, And és Baselga 2,* and Ca ola Gómez-Rod íguez 1,*
1Depa men o Func ional Biology (A ea o Ecology), CRETUS, Uni e sidade de San iago de Compos ela, San iago de Compos ela, Spain
2Depa men o Zoology, Gene ics and Physical An h opology, CRETUS, Uni e sidade de San iago de Compos ela, San iago de Compos ela, Spain
Co espondence: Vic o ia Fo moso-F ei e ( ic o ia o moso. ei [email p o ec ed])
Resea ch a icle
*Equally con ibu ed.
10
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(O e cas e al. 2021, Baselga e al. 2022). These models
inhe en ly ecognize he in e play be ween ecological and
e olu iona y p ocesses as key d i e s o popula ion and com-
muni y dynamics (Vellende al. 2014). F om seminal wo ks
sugges ing ha species and gene ic di e si y a e unde he
in luence o he same p ocesses (An ono ics 1976), accumu-
la ed knowledge has shed ligh on he mechanisms ha esul
in pa allel pa e ns o di e si y wi hin and among species
(Vellend 2003, 2005, Vellende al. 2014). A c ucial b eak-
h ough was Vellend’s (2016) syn he ic heo y o ecological
communi ies, wi h he ealiza ion ha he p ocesses go e n-
ing he composi ion and di e si y o biological communi-
ies can be dis illed in o ou high-le el ca ego ies (selec ion,
d i , specia ion, and dispe sal) wi h clea pa allels in popula-
ion gene ics (Vellend 2010, 2016). Impo an ly, he ecogni-
ion ha he same p ocesses go e n di e si y a gene ic and
species le els does no necessa ily imply ha pa e ns a bo h
le els mus be always co ela ed, bu i opens he oppo uni y
o assess he condi ions unde which hese pa allelisms a ise
(Vellend and Gebe 2005, Baselgae al. 2013, 2015, Gómez-
Rod ígueze al. 2019, Schmid e al. 2022). Fu he mo e,
p ocess-based simula ions can be ins umen al in gene a ing
p edic ions abou pa e ns eme ging ac oss hie a chical le els
(genes, genealogies, and species, Baselgae al. 2015). These
simula ions se e as aluable ools o in e ing he p ocesses
ha unde lie he obse ed pa e ns o a ia ion o biologi-
cal communi ies (La ochee al. 2015, O e cas e al. 2021,
Baselgae al. 2022).
In e ing ecological p ocesses om obse ed biodi e si y
pa e ns aces a signi ican challenge gi en ha mos mac-
oecological pa e ns migh po en ially a ise om di e en
mechanisms (McGill 2010, Cab ale al. 2017). An eme ging
ield ha ackles his challenge in ol es he use o mecha-
nis ic eco-e olu iona y models o simula e la ge-scale biodi-
e si y pa e ns a mul iple hie a chical le els (Hagen 2023).
These simula ions a e designed o gene a e es able bench-
ma ks agains which empi ical di e si y pa e ns can be com-
pa ed, hus allowing he in e ence o assembly p ocesses om
whole-communi y gene ic and species da a (Baselga e al.
2022, O e cas e al. 2023b). Fo ins ance, he join neu al
model (O e cas e al. 2019) unde lying he massi e ecoe o-
lu iona y syn hesis simula ions (MESS, O e cas e al. 2021)
p edic s ha , all o he hings being equal, abundan species
would end o accumula e mo e gene ic di e si y han a e
species. While his aligns wi h p e ious empi ical suppo
(McCuske and Ben zen 2010, G undle e al. 2019), i is
essen ial o no e ha , in he con ex o island communi ies,
his p edic ion leads o an addi ional in e ence: he co ela-
ion be ween species abundance and species gene ic di e si y
(SGD) will a y among local communi ies as a unc ion o
communi y age (O e cas e al. 2019, 2023b). I his p e-
dic ion holds, i opens an in e es ing a enue, as i sugges s
ha he co ela ion be ween species abundance and gene ic
di e si y could se e as an es ima o o communi y age o ,
mo e b oadly, communi y s abili y, as we a gue below. He e
we es his p edic ion o con inen al communi ies using a
ully cu a ed da ase o gene ic ba codes and abundance da a
o whole communi ies o lea bee les along a la i udinal g a-
dien in he Ibe ian Peninsula (Baselgae al. 2015).
The concep o communi y age is inhe en ly complex,
owing o he dynamic na u e o biological communi ies. In
gene al e ms, species composi ion changes o e ime (i.e.
empo al u no e ) in esponse o en i onmen al changes,
bio ic in e ac ions, and he a i al o new species, as well as
by andom luc ua ions in demog aphic p ocesses (Magu an
and Hende son 2010). Ne e heless, he age o oceanic
island communi ies has a disce nible maximum limi ied
o he island's o igin and subsequen coloniza ion by di e -
en species. In con as , de e mining he age o con inen al
communi ies p o es e en mo e elusi e due o hei highe
connec i i y and, consequen ly, he la ge in luence o immi-
g a ion p ocesses compa ed o he ela i ely mo e isola ed
island communi ies. In he con ex o con inen al communi-
ies, his o ical clima e change eme ges as a key d i e o com-
muni y econ igu a ion, inducing shi s in bo h he posi ion
and size o species dis ibu ion anges (Tabe le e al. 1998,
Hewi 1999, Da is and Shaw 2001, Jansson 2003), some-
imes un olding o e ex ended ime pe iods (i.e. Milanko i ch
clima ic cycles, Dynesius and Jansson 2000). These shi s in
species anges esul om he in e play be ween niche il e ing
and dispe sal p ocesses (Sko and S enning 2004, S enning
and Sko 2007) and a e he e o e no expec ed o be con-
ce ed ac oss species (S ewa e al. 2010), hus leading o he
eshu ling o communi ies due o clima e change (G aham
and G imm 1990, Williamse al. 2001). Consequen ly, he
mo e s able he clima e, he highe he p obabili y o spe-
cies pe sis ence in a gi en si e (Fjeldsae al. 1999, Dynesius
and Jansson 2000, Jansson 2003), making i mo e p obable
ha he biological communi y has emained unchanged o e
ime. In o he wo ds, clima ic s abili y could se e as a p oxy
o communi y age o , mo e b oadly, communi y s abili y.
Building on he p edic ion by O e cas e al. (2023a), we
would expec a posi i e ela ionship be ween clima ic s abili y
and he co ela ion be ween species abundance and gene ic
di e si y. We hypo hesize ha , i he co ela ion be ween spe-
cies abundance and gene ic di e si y depends on communi y
age, hen highe cong uence would be obse ed in con inen-
al locali ies wi h a mo e s able clima e since he Las Glacial
Maximum (LGM).
Ou aim is o es he p edic ion ha he cong uence
be ween ela i e abundance and gene ic di e si y wi hin
communi ies depends on hei long- e m clima ic s abili y.
To examine his, we ha e assessed he pa allelism be ween
he species abundance dis ibu ion (SAD) and he SGD dis-
ibu ion o whole communi ies o lea bee les (Coleop e a:
Ch ysomelidae) in he Ibe ian Peninsula. This egion o e s
an ideal case s udy, being one o he majo glacial e ugia
in Eu ope. Mo eo e , i is also hough o ha e ha bou ed
mul iple e ugia a e y small scales due o i s b oad opo-
clima ic he e ogenei y (Gómez and Lun 2007). As a con-
sequence, la e Qua e na y clima e changes ha e played an
impo an ole in s uc u ing he spa ial pa e n o endemism
and gene ic s uc u e in he Ibe ian Peninsula (Abellán and
S enning 2014). Lea bee les a e also a good biological g oup
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o add ess his ype o analysis because hei communi ies a e
e y di e se (dozens o species usually coexis locally, associ-
a ed o di e en hos plan s), wi h ma ked a ia ion in bo h
abundance and gene ic di e si y ac oss species.
Ma e ial and me hods
Lea bee le communi y da a
Lea bee le communi ies we e sampled in 20 locali ies along a
sou h–no h ansec (820 km, Fig. 1) in he Ibe ian Peninsula
in Ap il–June 2010 ( o mo e in o ma ion see Baselgae al.
2015). All locali ies we e well-p ese ed a eas (mos ly Na u al
Pa ks o a eas wi h some deg ee o p o ec ion) and co e a
wide al i udinal ange, om 123 m a.s.l. (ALC, see locali y
codes in he Suppo ing in o ma ion and Fig. 2 cap ion) o
1264 m a.s.l. (OMA) as well as a wide clima ic g adien , wi h
mean annual empe a u es om 9.5°C (OMA) o 17.5°C
(ALC) and mean annual p ecipi a ion om 478.7 kg/m2
(HOR) o 1764.5 kg/m2 (EUM, see Suppo ing in o ma ion
o mo e in o ma ion on he sampled locali ies). Each locali y
was in ensi ely sampled by sweeping and bea ing all ypes o
ege a ion, including ees, sh ubs, and he bs, o 20 sampling
pe iods o 30 min (excep 18 sampling pe iods in UBG). All
specimens we e p ese ed in 100% e hanol o DNA ex ac-
ion and ampli ica ion o a 655 base pai egion om he 5′
end o mi ochond ial cox1 (sequence da a n = 4531, published
in Baselgae al. 2015). All specimens we e also iden i ied o
species le el by an expe axonomis (A. Baselga), mos ly using
he axonomic monog aphs o he Eu opean (Wa chalowski
2003) and Ibe ian (Pe i pie e 2000) lea bee le aunas. To
assess he cong uence be ween gene ic di e si y and ela i e
species abundance a he communi y le el, in each locali y we
ha e conside ed only species wi h an abundance o a leas
h ee indi iduals (Tajima 1983).
Figu e1. Spa ial a ia ion o he ank cong uence be ween he species abundance dis ibu ion (SAD) and he species gene ic di e si y (SGD)
cu es (SAD–SGD ank cong uence). On he le , Pea son’s co ela ion alues be ween species SAD and SGD anks a e shown o each local-
i y, ep esen ed by he size o he ci cles. On he igh , he SADs (le ) and SGDs ( igh ) o wo example locali ies wi h he la ges (Anca es,
ANC) and lowes (Delei osa, DEL) co ela ions. No e ha he colou g adien in SAD and SGD plo s always e lec s he ank posi ion in he
SAD, so i SAD–SGD cong uence is high, he same colou s should appea in a simila o de in he SGD, bu no i cong uence is low.
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Local species abundance dis ibu ions
We buil he SAD cu e in each locali y, wi h he x-axis ep e-
sen ing he ank o each species om mos abundan o leas
abundan , and he y-axis ep esen ing he local ela i e abun-
dance o each species. Thus, om he ec o o abundances,
we compu ed he ank o de o each species wi hin he dis-
ibu ion ( anked abundance dis ibu ion, RAD, Whi ake
1965), which in o ms abou hei ela i e commonness (low
ank alues) o a i y (high ank alues) in he communi y.
When wo o mo e species had he same ela i e abundance
wi hin a communi y, hey we e assigned he same ank o de
(i.e. minimum ank).
Local species gene ic di e si y dis ibu ions
Analogously o SADs, we compu ed local SGD dis ibu-
ions based on he species nucleo ide di e si y (π, Nei and Li
1979) in each locali y (i.e. nucleo ide di e si y o each popu-
la ion). To calcula e he nucleo ide di e si y o each popula-
ion we used he nuc.di () unc ion in he ‘pegas’ package
(Pa adise al. 2023) in R (www. -p ojec .o g). So ing spe-
cies based on hei nucleo ide di e si y p o ides hei ank
o de wi hin he communi y acco ding o hei gene ic a i-
abili y. This SGD ank o de was compa ed o he ank o de
in he SAD o assess he cong uence be ween bo h le els
(sec ion ‘Cong uence be ween SADs and SGDs and clima ic
p edic o s’).
Fo each communi y, we also summa ized gene ic di e si y
ac oss species using he SGD mean (gene ic di e si y mean,
GDM) and i s e enness (gene ic di e si y e enness, GDE).
GDM is he a e age nucleo ide di e si y ac oss species. GDE
is based on Shannon en opy and co esponds o he i s -
o de Hill numbe o nucleo ide di e si y (measu ed as expo-
nen ial Shannon’s di e si y o 1D) s anda dized by species
ichness (i.e. 1D / S) (F enche al. 2023). GDE in o ms abou
he a iabili y in gene ic di e si y among species wi hin a
communi y (i.e. high alues o GDE indica e simila gene ic
di e si y among species in a locali y). Analogous measu es o
di e si y we e compu ed a he species le el: species ichness
(S) and abundance dis ibu ion e enness measu ed as expo-
nen ial Shannon’s di e si y s anda dized by species ichness
(i.e. 1D / S).
Cong uence be ween SADs and SGDs and clima ic
p edic o s
To assess he cong uence be ween species abundance and
SGD in each locali y, we compu ed he Pea son’s co ela ion
be ween he species ank o de in he SAD and in he SGD.
This SAD–SGD ank cong uence in o ms abou species ank
shi s be ween he wo le els, so high posi i e cong uence al-
ues would indica e ha he mos abundan species a e also
he ones wi h highe gene ic di e si y, as expec ed o olde
communi ies acco ding o O e cas e al. (2023a).
We also assessed he ela ionship be ween SAD–SGD ank
cong uence and bo h cu en and pas clima ic condi ions,
as well as he long- e m clima ic s abili y in each locali y,
using linea eg ession models. We ob ained cu en clima e
da a om he CHELSA 2.1. da abase (Ka ge e al. 2017)
and pas clima e da a om he CHELSA da abase (PMIP3,
CCSM4 model) o he LGM (Ka ge e al. 2021). We
selec ed he ollowing clima ic a iables as majo desc ip o s
o local clima ic condi ions: mean annual empe a u e (bio1),
mean maximum empe a u e o he wa mes mon h (bio5),
mean minimum empe a u e o he coldes mon h (bio6),
annual p ecipi a ion (bio12), mean p ecipi a ion o he we -
es qua e (bio16), and mean p ecipi a ion o he d ies
qua e (bio17). We measu ed long- e m clima ic s abili y
as he di e ence be ween he cu en and he LGM mean
annual empe a u e ( emp_di = bio1.p esen – bio1.LGM)
and, independen ly, as he di e ence be ween he cu en and
he LGM annual p ecipi a ion (p ec_di = bio12.p esen –
bio12.LGM). We also included al i ude, spa ial coo dina es
(la i ude and longi ude), and species ichness as po en ial p e-
dic o s o con ol o al e na i e spa ially s uc u ed ac o s as
well as po en ial biases due o he di e si y o communi ies.
The bes eg ession model was iden i ied ollowing a o wa d
s epwise p ocess based on AIC. Addi ionally, we buil equi a-
len eg ession models using s anda d di e si y measu es as
esponse a iables: species ichness (S) and abundance dis i-
bu ion e enness (1D / S) o he species le el and GDM and
GDE o he gene ic le el. See Suppo ing in o ma ion o
complemen a y eg ession models.
Resul s
Lea bee le communi y da a
A o al o 5100 specimens and 209 species we e collec ed o
his s udy, wi h local species ichness anging om 27 (HOR)
o 67 (ANC). The mos abundan species in he da ase we e
Longi a sus juncicola, Gonioc ena oli acea, and Calomic us
ci cum usus, p esen in 7, 18, and 13 locali ies, espec i ely.
The ba code egion (cox1-5′) o he mi ochond ial genome
was success ully ampli ied o 4531 specimens (88.8% o he
o al). Once he less equen species (n < 3) we e emo ed
om each locali y, he o al numbe o specimens o u -
he analyses was 4091, co esponding o 140 species. Lea
bee le communi ies showed a wide ange o a ia ion in bo h
gene ic di e si y and species abundances (Fig. 2).
Local species abundance dis ibu ions and species
gene ic di e si y cu es
Mean ela i e abundance anged om 0.026 ± 0.013 (SD)
in ANC o 0.067 ± 0.064 (SD) in ALC and 0.067 ± 0.033
(SD) in HOR (Table 1), wi h he mos locally dominan
species being L. juncicola (53 specimens) and L. do salis (34
specimens), bo h in ALC. The locali y wi h he mos e en
abundance dis ibu ion was ANC (1D / S = 0.745) while ALC
showed he mos unbalanced abundance dis ibu ion (1D /
S = 0.509, see Table 1). Con as ing esul s we e obse ed
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Page 5 o 10
Figu e2. Spa ial a ia ion in ela i e abundance and gene ic di e si y among he s udied communi ies. (a) Gene ic di e si y mean (GDM) and
mean ela i e abundance o each locali y. (b) Gene ic di e si y e enness (GDE) and abundance dis ibu ion e enness, measu ed as exponen ial
Shannon’s di e si y s anda dized by species ichness (1D / S) o each locali y. The alues o all a iables we e s anda dised (z-sco es) o allow a
isual compa ison o he gene ic di e si y and abundance a ibu es o communi ies. Locali y codes: A ibes del Due o-No e (ADN), A ibes
del Due o-Su (ADS), Alco nocales (ALC), Anca es (ANC), Co nal o (COR), Delei osa (DEL), F agas do Eume (EUM), Sie a de F ancia
(FRN), Ho nachos (HOR), Je ez de los Caballe os (JCB), La ouco (LAR), Las a (LAS), Macizo Cen al (MAC), Omaña (OMA), Sanab ia
(SAN), Sie a No e de Se illa (SNS), Sie a de San Ped o (SSP), Valle del Tuéja (TUE), Ub ique-G azalema (UBG), La Ve a (VER).
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Page 6 o 10
o nucleo ide di e si y, wi h UBG being he locali y wi h
he lowes GDM (0.004 ± 0.005 [SD]) and OMA wi h he
la ges GDM (0.012 ± 0.022 [SD]). The locali y wi h he
mos e en gene ic di e si y was HOR (GDE = 0.807), while
OMA (GDE = 0.310) showed he mos unbalanced gene ic
di e si y dis ibu ion.
Fo each locali y, we ep esen ed SADs and SGDs by so -
ing species acco ding o hei ela i e abundance and nucleo-
ide di e si y, espec i ely. These plo s g aphically ep esen
he ank shi be ween he gene ic and species le el and hence
he cong uence be ween SADs and SGDs (see Fig. 1 o illus-
a i e pu poses, and Suppo ing in o ma ion o he SAD
and SGD plo s o all si es). SAD–SGD ank cong uence
anged om Pea son’s = −0.25 (DEL) o Pea son’s = 0.48
(ANC) (Fig. 1 and Table 1). The a e age Pea son’s co ela ion
ac oss locali ies was = 0.14 ± 0.21 (SD), wi h only one co -
ela ion being signi ican (ANC).
SAD–SGD ank cong uence and clima ic s abili y
The bes mul iple eg ession model o explaining SAD–
SGD ank cong uence included bo h empe a u e s abili y
( he di e ence be ween cu en and LGM mean annual em-
pe a u e) and cu en mean empe a u e (bio1) (R2 = 0.32,
F2, 17 o m = 4.01, p = 0.037), al hough only empe a u e
s abili y was signi ican (Fig. 3; see Suppo ing in o ma-
ion o pa ame e de ails). Clima ic s abili y a ied among
locali ies, om ela i ely low empe a u e change in ALC
(∆T = 2.7°C) o he la ges a ia ion in DEL (∆T = 6.4°C).
See Suppo ing in o ma ion o esul s o models o
species ichness, abundance dis ibu ion e enness, GDM,
and GDE.
Discussion
Ou esul s show ha he impac o long- e m clima ic s abil-
i y on biological communi ies can be de ec ed when e alua -
ing di e si y pa e ns simul aneously a bo h he species and
gene ic le el. Long- e m clima ic s abili y se es as an indica-
o o abio ic condi ions expe ienced by he biological com-
muni y bu , mo e impo an ly, i also unc ions as a p oxy
o communi y age. This associa ion is g ounded in he ac
ha na owe clima ic oscilla ions esul in smalle changes in
Table 1. Di e si y measu es and ank cong uence be ween he species abundance dis ibu ion (SAD) and he species gene ic di e si y (SGD)
cu es (SAD–SGD ank cong uence) o each locali y. See Fig. 2 cap ion o explana ion o Locali y codes.
Locali y Richness E enness (1D/S) Rela i e abundance (Mean ± SD) GDM1 (Mean ± SD) GDE2Cong uence3
ADN 42 0.707 0.040 ± 0.020 0.005 ± 0.008 0.568 −0.048
ADS 41 0.733 0.037 ± 0.021 0.006 ± 0.005 0.690 0.039
ALC 30 0.509 0.067 ± 0.064 0.006 ± 0.006 0.606 0.412
ANC 67 0.745 0.026 ± 0.013 0.005 ± 0.007 0.525 0.476
COR 34 0.603 0.053 ± 0.029 0.006 ± 0.005 0.735 0.402
DEL 41 0.640 0.050 ± 0.030 0.007 ± 0.006 0.757 −0.252
EUM 41 0.678 0.048 ± 0.025 0.005 ± 0.006 0.592 0.375
FRN 43 0.628 0.042 ± 0.026 0.005 ± 0.005 0.614 −0.013
HOR 27 0.696 0.067 ± 0.033 0.007 ± 0.005 0.807 −0.134
JCB 36 0.732 0.048 ± 0.018 0.007 ± 0.000 0.587 0.060
LAR 40 0.663 0.040 ± 0.028 0.008 ± 0.012 0.470 0.292
LAS 56 0.684 0.030 ± 0.017 0.007 ± 0.015 0.340 0.035
MAC 49 0.691 0.043 ± 0.023 0.008 ± 0.013 0.429 −0.072
OMA 45 0.711 0.034 ± 0.023 0.012 ± 0.022 0.310 −0.055
SAN 47 0.642 0.045 ± 0.023 0.006 ± 0.008 0.497 0.367
SNS 35 0.640 0.056 ± 0.041 0.006 ± 0.005 0.670 0.291
SSP 35 0.647 0.050 ± 0.034 0.006 ± 0.006 0.637 0.090
TUE 48 0.684 0.038 ± 0.018 0.006 ± 0.011 0.445 0.075
UBG 34 0.692 0.056 ± 0.026 0.004 ± 0.005 0.611 0.138
VER 41 0.676 0.038 ± 0.026 0.006 ± 0.005 0.674 0.253
1GDM: gene ic di e si y mean.2GDE: gene ic di e si y e enness.3Cong uence: Pea son’s co ela ion be ween he species ank o de in he
SAD and he SGD dis ibu ion. The only signi ican co ela ion alue is highligh ed in bold (p = 0.002).
Figu e3. Rela ionship be ween he ank cong uence o he species
abundance dis ibu ion (SAD) and he species gene ic di e si y
(SGD) (SAD–SGD ank cong uence) and clima ic s abili y since
he Las Glacial Maximum (LGM; di e ence be ween cu en mean
annual empe a u e and mean annual empe a u e a he LGM).
Colou s co espond o he locali ies in he map o Fig. 1. Do size is
p opo ional o species ichness.
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Page 7 o 10
species’ ange posi ions and sizes (Dynesius and Jansson 2000,
B owne al. 2020), hus esul ing in inc eased s abili y o
biological communi ies o e ime. The e o e, ou s udy sup-
po s he p edic ion o a posi i e ela ionship be ween com-
muni y age and he co ela ion be ween species abundance
and gene ic di e si y (O e cas e al. 2023a). While his p e-
dic ion was made in he con ex o island biogeog aphy, ou
esul s ex end his expec a ion o any biological communi y,
as he legacy o clima ic s abili y is obse ed in he deg ee o
co ela ion be ween species abundance and gene ic di e si y
o con inen al communi ies. Consequen ly, ou s udy unde -
sco es he ele ance o uni ied models o biological di e si y
ac oss o ganiza ional le els (genes, species, communi ies) o
unde s and undamen al ecological p ocesses (Vellende al.
2014, Vellend 2016). In pa icula , he e we show ha he
impac o his o ical clima ic e en s in assembly p ocesses
condi ions ou abili y o p edic communi y s uc u e a he
gene ic le el (i.e. he dis ibu ion o gene ic di e si y among
species in he communi y) based on obse a ions a he spe-
cies le el (i.e. he dis ibu ion o abundance among species in
he communi y).
We obse e highe cong uence be ween abundance and
gene ic di e si y dis ibu ions in locali ies ha ha e expe i-
enced g ea e clima ic s abili y, measu ed as empe a u e di -
e ence since he LGM. In hese locali ies (e.g. ALC, ANC,
COR, o EUM), he mos abundan species end o be he
ones wi h highe nucleo ide di e si y as well, as would be
expec ed o communi ies ha ha e emained s able o e
an ex ended pe iod o ime (O e cas e al. 2019, 2023b).
Con e sely, he co ela ion be ween species abundance and
gene ic di e si y dec eases in locali ies ha ha e unde gone
la ge empe a u e changes since he LGM. This aligns wi h
expec a ions o communi ies ha ha e ecen ly eassembled,
so abundan species may ha e no accumula ed gene ic di e -
si y, al hough o he ac o s such as compe i ion may also be
a play. Ou compa ison o communi y s uc u e a wo o ga-
niza ional le els complemen s p e ious s udies e idencing
he imp in o pas clima ic e en s on con empo a y di e si y
pa e ns a ei he he species (A aújoe al. 2008, O donez
and S enning 2015, S enning e al. 2015) o he gene ic
(Tabe le e al. 1998, Hewi 2000) le el. Fu he mo e, i
con ibu es new e idence suppo ing he signi ican impac
o long- e m clima ic s abili y on biological communi ies
(Pe i e al. 2003, Ca na ale al. 2009, B owne al. 2020).
F om a heo e ical s andpoin , cu en ecological heo y, as
p oposed by Vellend (2016), asse s ha he same unda-
men al p ocesses shape ecological communi ies a bo h he
species and molecula le els: selec ion, d i , dispe sal (gene
low), and specia ion (mu a ion). Howe e , i is impo an o
no e ha he exis ence o analogous p ocesses does no neces-
sa ily imply he exis ence o iden ical pa e ns a bo h le els
(La ochee al. 2015), as ou s udy also demons a es. In ac ,
we highligh ha communi y s abili y is key o explaining he
co ela ion (o lack he eo ) be ween species abundance and
gene ic di e si y dis ibu ions. In o he wo ds, clima ic s a-
bili y is a majo d i e o a mac oecological p ope y eme g-
ing ac oss o ganiza ional le els: he deg ee o cong uence
be ween communi y s uc u es a he gene ic and species
le els.
Ou esul s suppo he no ion ha clima ic s abili y
se es as a p edic o o he co ela ion be ween abundance
and gene ic di e si y. This eme ges e en in he ace o gene -
ally low co ela ion alues be ween abundance and gene ic
di e si y, along wi h subs an ial a ia ions obse ed ac oss
di e en locali ies. No ably, low SAD–SGD ank co ela ions
a e expec ed in con inen al communi ies gi en hei highe
connec i i y, which inc eases he likelihood o species immi-
g a ion. Despi e his inhe en ecological dynamism, bo h he
a iabili y in local SAD–SGD ank co ela ion alues and
i s ela ionship wi h clima ic s abili y unde sco e he po en-
ial o assessing di e si y pa e ns ac oss hie a chical le els,
om gene ic a ian s o clades and o species (Vellend 2003,
Vellend and Gebe 2005, Baselgae al. 2013, Vellende al.
2014, Baselgae al. 2015). Fo ins ance, a spa io- empo al
con inuum o biodi e si y becomes appa en when he same
p ocesses ope a e wi h equal s eng h a bo h he species and
gene ic le els (Baselgae al. 2013). Gi en ha haplo ypes and
in aspeci ic lineages a e delimi ed using neu al molecula
ma ke s, which a e no subjec o selec ion p ocesses (Diniz-
Filho and Bini 2011), he exis ence o such a spa io- empo al
con inuum has allowed he in e ence o dispe sal p ocesses
playing a majo ole in shaping di e si y pa e ns a he
species le el (Baselga e al. 2015, Gómez-Rod íguez e al.
2019, A ibas e al. 2020). O he s udies ha e also con-
as ed pa e ns a bo h le els o de ec a dominan e ec o
en i onmen al cons ain s (Mú ia e al. 2017) o his o i-
cal ac o s (Robuchone al. 2019), as well as o a gue abou
hei impo an implica ions in biodi e si y conse a ion
(Kahilainene al. 2014). Recen ad ances in he ield, such
as me aba coding o whole communi ies (A ibase al. 2020,
Nogue alese al. 2021) o communi y-scale eco-e olu iona y
simula ions (O e cas e al. 2019, 2021, Baselgae al. 2022),
hold p omise o expedi ing he in e ence o ecological and
e olu iona y p ocesses om he simul aneous assessmen o
species and gene ic di e si y pa e ns (Gillespiee al. 2023,
O e cas e al. 2023b). Howe e , he e we ha e bene i ed om
he a ailabili y o a ully cu a ed DNA ba coding da ase o
whole communi ies along a la i udinal g adien (Baselgae al.
2015). While axonomic iden i ica ion and DNA ba coding
o all specimens o comple e assemblages may be cos ly com-
pa ed o me aba coding app oaches, i also o e s wo main
ad an ages o es he p edic ion o O e cas e al. (2019,
2023a): 1) i p o ides di ec measu es o ela i e abundance
o each species, and 2) in his pa icula s udy, species iden i-
ica ion is based on mo phological cha ac e is ics and hence
is independen o he molecula da a used o es ima e nucleo-
ide di e si y.
Ou s udy elies on assessing he dis ibu ion o ela-
i e abundance and, independen ly, o nucleo ide di e si y
wi hin biological communi ies. The dis ibu ion o abun-
dance wi hin a communi y (SAD) s ands as one o he mos
s udied pa e ns in ecology (Magu an and Hende son 2011,
McGill 2011). I has p o en mos ly use ul o assess changes
in biodi e si y s uc u e ac oss communi ies, space o ime
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Page 8 o 10
(An ãoe al. 2017, Ma hewse al. 2019). Fo ins ance, em-
po al changes in biological communi ies can be assessed by
acking he shi s o species in SADs om one ime pe iod
o ano he (Do nelas 2010, Tsaie al. 2014). He e we assess
analogous shi s bu , ins ead o compa ing he empo al
shi s in communi ies’ SADs (SAD in ime 1 e sus SAD in
ime 2), we compa e o ganiza ional le els wi hin communi-
ies (SAD e sus SGD) in a wide spa ial con ex . The geo-
g aphic a ia ion o SADs has ecen ly ga ne ed a en ion,
wi h s udies showing how hei shape depends on spa ial
scale (An ãoe al. 2017) o a ies along la i udinal g adien s
(Qiaoe al. 2015, Ul iche al. 2016). In con as , SGDs ha e
no ecei ed compa able a en ion in a biogeog aphical con-
ex (G i i hs and Ta a e 1994). Al e na i ely, he bu geon-
ing ield o ‘mac ogene ics’ is p o iding in e es ing insigh
in o how in aspeci ic gene ic di e si y a ies ac oss mul iple
communi ies a la ge spa ial scales, as well as he e olu ion-
a y p ocesses ha gene a e, main ain, and e ode biodi e si y
(Mi aldoe al. 2016, Leighe al. 2021, Schmid e al. 2023).
P e ious con ibu ions o mac ogene ics ha e p edominan ly
ocused on a e age measu es o gene ic di e si y, a he han
he comple e dis ibu ion o nucleo ide di e si y ac oss spe-
cies wi hin communi ies. Howe e , a pa icula ly no ewo hy
s udy on insec mac ogene ics demons a es ha nucleo ide
di e si y is mo e une en ac oss species in a eas ha we e gla-
cia ed du ing he LGM (F enche al. 2023). Hence, using
a summa y me ic, his s udy poin s o his o ical clima ic
e en s shaping he cu en dis ibu ion o gene ic di e si y
wi hin a communi y. Ou s udy akes a s ep u he , analyz-
ing Ibe ian lea bee les o in es iga e whe he he dis ibu-
ion o gene ic di e si y is co ela ed wi h he dis ibu ion
o abundance and how his may be media ed by his o ical
clima ic e en s.
In conclusion, con inen al lea bee le communi ies exhibi
low co ela ion alues be ween species abundance and gene ic
di e si y, as expec ed om he highe connec i i y o con i-
nen al communi ies compa ed o insula ones. The con inen-
al se ing is expec ed o aise he likelihood o no el species
a i ing o local communi ies, he eby inc easing he a iabil-
i y o species abundances o e ime. Howe e , despi e he ela-
i ely modes SGD–SAD co ela ions, hei a ia ion ac oss
locali ies is linked o he magni ude o clima e change since
he LGM. This e idences he key ole o his o ical clima ic s a-
bili y in shaping biological communi ies om he molecula
o he species le el. These esul s ca y wo impo an implica-
ions. Fi s , he deg ee o cong uence be ween SADs and SGDs
could be used as a p oxy o communi y s abili y, no only
ela ed o his o ical clima ic change bu also o o he dis up -
ing ac o s, including human p essu e. Second, in clima ically
s able locali ies, species abundance could be used as a p oxy
o gene ic di e si y, which is a key ace o biological di e si y
and should he e o e be con empla ed in conse a ion plan-
ning (Ca alhoe al. 2017, Hansone al. 2021, Schmid e al.
2023). I gene ic di e si y da a we e a ailable, de ia ions om
SAD–SGD cong uence could also be le e aged o in e ecen
coloniza ions, hus p o iding aluable insigh s in o his o ical
biodi e si y dynamics and conse a ion e o s.
Acknowledgemen s – We a e g a e ul o he e iewe D Isaac O e cas
and o wo anonymous e iewe s o insigh ul and cons uc i e
sugges ions o a p e ious e sion o his pape .
Funding – This wo k was suppo ed by he Spanish Minis y
o Science and Inno a ion h ough g an no. PID2020-
112935GB-I00/AEI/10.13039/501100011033 and no. CGL2009-
10111, and a FPI schola ship ( e . no. PRE2021-098920) o VF-F.
Au ho con ibu ions
Vic o ia Fo moso-F ei e: Fo mal analysis (lead); W i ing –
o iginal d a (equal); W i ing – e iew and edi ing (equal).
And és Baselga: Da a cu a ion (equal); Fo mal analysis (sup-
po ing); Funding acquisi ion (equal); In es iga ion (equal);
Me hodology (equal); W i ing – o iginal d a (equal);
W i ing – e iew and edi ing (equal). Ca ola Gómez-
Rod íguez: Concep ualiza ion (lead); Da a cu a ion (equal);
Fo mal analysis (suppo ing); Funding acquisi ion (equal);
In es iga ion (equal); Me hodology (equal); W i ing – o igi-
nal d a (equal); W i ing – e iew and edi ing (equal).
Da a a ailabili y s a emen
Da a a e a ailable om he D yad Digi al Reposi o y: h ps://
doi.o g/10.5061/d yad.db 15 8d (Fo moso-F ei e e al.
2024). See Suppo ing in o ma ion o he R code.
Suppo ing in o ma ion
The Suppo ing in o ma ion associa ed wi h his a icle is
a ailable wi h he online e sion.
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