Fig 1 PSMC plots: A) NW Europe (Red line) and S Europe (Blue line)
sampled European nightjar, as well as pseudo-diploid genome of NW/S
Europe birds (dashed line), depicting demographic history
(Ne change) over the last ~5
million years (bp), scaled with a mutation rate of 4.6 × 10−9 per site
and generation time of 2 years. The x-axis depicts time (in years) on a
log scale, with the y-axis showing effective population size. B)
Estimated Ne for pseudo-diploid genome only
(dashed line). Approximate timings of significant periods of global
climate change are shown by shading along the x-axis. Light blue shading
= last glacial period (LGP), orange shading = Mid-Brunhes event (MBE),
and dark blue shading = Mid-Pleistocene Revolution (MPR).
Overall, historic nightjar N e in Europe decreased
and increased during periods of cooling and warming respectively (Fig
1a). Nightjar are insectivorous habitat specialists requiring clear
fell, heathland, or woodland edge to breed
(Cleere, 1998),
feeding primarily on Lepidoptera
(Mitchell et al.,
2022). With reductions in temperature and glacial expansion, prey and
habitat availability will have been constrained to more southerly
latitudes (Schmitt,
2007), likely corresponding with a reduction in nightjar distribution
and thus N e. For example, the decrease in
nightjar N e ~1.2 Mya –
~ 600 Kya (Fig1a) overlapped the MPR (~1
Mya - 450 Kya), which was characterised by shortened interglacial
periods and cooler average temperatures which restricted the northward
resurgence of temperate animal and plant communities
(Pisias and Moore,
1981; Head and Gibbard, 2015). Conversely, warmer temperatures will
have likely increased the availability of suitable habitat across
northerly latitudes
(Schmitt, 2007; Candy
et al., 2010). Indeed the stable climate of the late Pliocene and early
Pleistocene (Head and
Gibbard, 2015), as well as the short glacial and warm interglacial
periods of the MBE
(Candy et al., 2010;
Barth et al., 2018) associated with increases in nightjarN e in our study (Fig 1a). Similarly, the dramaticN e increase during the late Pleistocene prior to
the LGP (Fig 1a) coincided with the Eemian warm phase
(~127 Kya;
Bergoeing, 2017),
which was characterised by the expansion and persistence of temperate
plant communities into northerly latitudes
(Van Andel and
Tzedakis, 1996; Sánchez Goñi et al., 1999; Lisiecki and Raymo, 2005).
Following similar trends exhibited by other Afro-Palearctic migrants
(i.e Ficedcula flycatchers;
Nadachowska-Brzyska et
al., 2016), N e of both nightjar populations
greatly decreased as the LGP continued, likely restricting nightjar to
Southern European refugia
(Schmitt, 2007;
Lombardo et al., 2022) or North Africa
(Thorup et al.,
2021). Bootstrapping indicates caution is required regarding exact
timings of N e fluctuations (Supporting
Information). However, PSMC analysis in other Caprimulgids (i.e.:
Chuck-will’s-widow) and Afro-Palearctic migrants (i.e.: Common cuckoo,Cuculus canorus )
(Nadachowska-Brzyska
et al., 2015), have shown similar fluctuating trends inN e over the same timeframe, suggesting that the
estimated timings of N e change with paleoclimatic
events in our study are reasonable.
Population Structure and Divergence in Nightjar
When applied to a pseudo-diploid genome derived from two different
populations, PSMC analysis can be used to determine the timing of
population divergence. This is signalled by the pseudo-diploidN e diverging from the two parent populations and
tending towards infinity
(Prado-Martinez et
al., 2013). This occurs because coalescence events between the two
populations were severely reduced or ceased, leading to an increase inN e as interpreted by the analysis. In our
analysis, the pseudo-diploid N e trend appeared to
diverge from the NWE and SE populations ~1.2 Mya (Fig
1a). However, true divergence (the point at whichN e tends to infinity) does not occur until
~40 Kya (Fig 1b).Even taking into account f the
~35Ky error window suggested by the bootstrapping
(Supporting Information), the main divergence event between the NWE and
SE populations occurred within the LGP (Fig 1b).
The two modern populations used in this study are spatially distant and
behaviorally distinct as they exhibit different migration strategies
(Evens et al., 2017).
Nightjars breeding in Western Europe typically migrate through Iberia
during spring migration, with Eastern breeders migrating through Italy
and SE Europe (Evens
et al., 2017; Norevik et al., 2017). In other trans-Saharan migrants,
such migratory behaviour is thought to be ancestral and ‘hard wired’
into populations, likely predating the Pleistocene
(Thorup et al.,
2021). Although the SE bird in our study was trapped during the spring
migration period
(Secomandi et al.,
2021), it is probable that the individual’s breeding population was
located within Central to Eastern Europe as suggested by recent tracking
studies (e.g., Norevik
et al., 2017).
As in other migratory Palearctic birds (e.g., Lesser whitethroatSylvia curruca ;
Olsson et al., 2013;
Pied wagtail Motacilla alba ;
Li et al., 2016), we
suggest that nightjar may exhibit East-West genetic structuring, but
investigation is required. Results from MtDNA analysis have suggested
that nightjar can be divided into Eastern and Western lineages, with
divergence being deeper (c. 2.9 Mya)
(Schweizer et al.,
2020) than that suggested by our PSMC analysis (initial divergence
~1.2 Mya, cessation of gene flow ~40 Kya
± 35 Ky; Fig 1). However, the samples contributing to Schweizer et al.’s
(2020) work spanned a much broader latitudinal range (encompassing W
Europe to Asia) than those in our study and likely represented a deeper
divergence. Much of the structure in contemporary Palearctic and
Nearctic animal populations are fundamentally linked to past glacial and
interglacial cycles, which have led to the contraction of temperate
breeding populations into Southern refugia, and subsequent northward
recolonisation during warmer interglacial periods
(Hewitt, 2004;
Nadachowska-Brzyska et al., 2016; Yao et al., 2022; de Greef et al.,
2022). Previously panmictic populations may become isolated from one
another in different refugia, during periods of glaciation, leading to
genetic differentiation post-interglacial expansion
(Hewitt et al.,
2001).
Considering the timings of gene flow reduction and divergence between
the two populations it is likely that the ancestral states of both
populations utilised different refugia over historic glacial periods and
most recently the LGM. Owing to the apparent divide in contemporary
migration routes we suggest that the NWE population will have utilised
the Iberia refugium and the SE sampled population the Italian refugia
during glacial periods. Whilst most Western Palearctic avifauna (117 out
of 131 studied by
Pârâu and Wink, 2021)
show admixture among populations, our study suggests that nightjar
exhibit genetic structure within their Eurasian breeding range. With the
sampling information available our results tentatively reflect East-West
structuring in the European nightjar population, likely diverging during
isolation in different glacial refugia during periods of glaciation.
However, it should be noted that the SE individual may belong to the
Southern European C.e.meridionalis subspecies and instead our
results might reflect divergence between C.e.meridionalis and the
nominate C.e.europaeus (NWE individual) subspecies. Nevertheless,
validity of the C.e.meridionalis subspecies remains questionable,
with as yet no genetic evidence to support the subspecies status
(Del Hoyo et al.,
2014; BirdLife International, 2022). Nightjars of the nominate raceC.e.europaeus migrate through Italy and SE Europe
(Evens et al., 2017;
Norevik et al., 2017). Given the individual used in this study was
sampled during spring migration, it is likely that the bird was
migrating to breeding grounds at a higher latitude and belongs toC.e.europaeus . However, further work is required to resolve
population genetic structure across the species range, and there is a
wider need to resolve the molecular phylogeny of European nightjar and
its subspecies.
Evolution of Migratory Behaviour in Nightjar
Following the timeline proposed by our study (Fig 1), it seems unlikely
that nightjar migratory behaviour developed post-LGM as suggested by
Larsen et al.,
(2007). The dramatically fluctuating N e prior to
the LGM throughout the Pleistocene may reflect periods of significant
population expansion and contraction associated with climate driven
changes in temperate breeding habitat availability
(Ponti et al., 2020).
If nightjar had exhibited a sedentary Afrotropic distribution prior to
the LGM we might expect to see less severe fluctuation inN e relative to global climate change
(Kimmitt et al.,
2023; but see Speckled mousebird; Colius striatus in
Nadachowska-Brzyska et
al., 2015). Similarly, if migratory behaviour had not developed until
~20,000 ya, we would expect divergence between
populations to occur exclusively post-LGM. However, our results
highlight that whilst gene flow appeared to cease between the NWE and SE
populations towards the LGM (Fig 1b), population divergence occurred as
early as ~1.2 Mya (Fig 1a), with subsequent episodes of
mixing ensued during periods of range expansion. Our results suggest
that long-distance migratory behaviour in nightjar evolved prior to the
LGM and was maintained throughout the Pleistocene, likely predating the
initial divergence 1.2Mya recorded in our study (Fig 1a). This is
corroborated by the deeper divergence (2.9Mya) between range-wide
East-West lineages recorded by
Schweizer et al.,
(2020), which may indicate a migratory divide. Our results contribute
to the growing consensus that long distance migratory behaviour in
contemporary Western-Palearctic avifauna predates the LGM (i.e.
Ponti et al., 2020;
Ralston et al., 2021; Thorup et al., 2021; Kimmitt et al., 2023).
Limitations of PSMC analysis
Results of PSMC analysis are influenced by the scaling applied to plots,
determined by mutation rate and generation time
(Li and Durbin, 2011;
Mather et al., 2019). However), the overall pattern ofN e change will remain the same independent of
scaling parameters
(Nadachowska-Brzyska
et al., 2016). Data on both of these parameters are often limited for
study species (e.g. see
Sato et al., 2020;
Chattopadhyay et al., 2019; Ericson et al., 2022), including nightjar.
Thanks to the wealth of PSMC studies over a multitude of avian taxa
(e.g.,
Nadachowska-Brzyska et
al., 2015, 2016; Kozma et al., 2018; Sato et al., 2020; Brüniche-Olsen
et al., 2021) parameters suited to a wide range of avifauna can be
selected, such as those used in our study as per
Sato et al., (2020).
Therefore, whilst caution must be applied concerning the timings and
magnitudes of N e change, as highlighted by
bootstrapping (see Supporting Information), we believe that PSMC
analysis provides a valuable method to associate broadN e trends concurrent climate cycles.
Conclusion
PSMC is a useful tool to characterise past demography and resolve timing
of species and population differentiation, processes which underlie
contemporary genetic and demographic patterns. Results from our PSMC
analysis suggest that nightjar were highly susceptible to climatic
variation, increasing in number during warm interglacials and long
periods of relative climate stability. The historical context provided
by our research suggests that the current climate best suits nightjar.
Limitations on population size are likely primarily anthropogenic, with
humans responsible for the mass deforestation and agriculturalisation of
Europe from 8.2 Kya (Kaplan et al. 2009). Habitat loss, fragmentation,
degradation and disturbance are reported as the primary drivers of
contemporary population reduction in nightjar
(Langston et al.,
2007; Lowe et al., 2014; Ashpole et al., 2015). Although nightjar have
been shown to persist through historic climate change, contemporary
anthropogenic pressures may reduce the ability of the species to adapt
to the current rapidly changing climate.
As in multiple other Palearctic and Nearctic birds, our analysis
suggests that restriction to different refugia during glacial cycles may
have driven divergence within the European population of nightjar. Our
analysis suggests a complete cessation of gene flow between the two
populations by ~14 Kya during the LGM, although mixing
under current interglacial conditions is likely. Genetic structure
within the European population has significant conservation
implications, potentially delimiting the current population into smaller
conservation units. Our results also suggest that migratory behaviour in
nightjar evolved prior to the LGM, persisting throughout the
Pleistocene. However, further research is needed to understand the
spatial context of this apparent range-wide genetic structure, as well
as to clarify timing of long-distance migration evolution, as well as
current taxonomic assignations. We recommend a range-wide molecular
analysis, including population genetics, of nightjar to better
understand the extent and origins of divergence within the species. Such
research would also aid ongoing taxonomic uncertainties surrounding
subspeciation in nightjar
(Schweizer et al.,
2020). Finally, while caution is needed, here PSMC analysis has
provided a useful insight into the demographic past of nightjar in
Europe, which has highlighted the nightjar population genetics as a
valuable future research direction.
References
Allendorf, F.W., 2017.
Genetics and the conservation of natural populations: allozymes to
genomes. Mol. Ecol. 26, 420–430. https://doi.org/10.1111/mec.13948
Ashpole, J., Burfield,
I., Ieronymidou, I., Pople, R., Wheatley, H., Wright, L., 2015.
Caprimulgus europaeus – Linnaeus, 1758. BirdLife International.
Bairlein, F., 2016.
Migratory birds under threat. Science 354, 547–548.
https://doi.org/10.1126/science.aah6647
Barth, A.M., Clark,
P.U., Bill, N.S., He, F., Pisias, N.G., 2018. Climate evolution across
the Mid-Brunhes Transition. Clim. Past 14, 2071–2087.
https://doi.org/10.5194/cp-14-2071-2018
Bergoeing, J.P., 2017.
Geomorphology and volcanology of Costa Rica. Elsevier, Oxford.
BirdLife
International, 2022. European Nightjar (Caprimulgus europaeus) -
BirdLife species factsheet [WWW Document]. URL
http://datazone.birdlife.org/species/factsheet/european-nightjar-caprimulgus-europaeus
(accessed 1.19.23).
Brüniche-Olsen, A.,
Kellner, K.F., Belant, J.L., DeWoody, J.A., 2021. Life-history traits
and habitat availability shape genomic diversity in birds: implications
for conservation. Proc. R. Soc. B Biol. Sci. 288, 20211441.
https://doi.org/10.1098/rspb.2021.1441
Bürger, R., Lynch, M.,
1995. Evolution and extinction in a changing environment: A
quantitative-genetic analysis. Evolution 49, 151–163.
https://doi.org/10.1111/j.1558-5646.1995.tb05967.x
Candy, I., Coope,
G.R., Lee, J.R., Parfitt, S.A., Preece, R.C., Rose, J., Schreve, D.C.,
2010. Pronounced warmth during early Middle Pleistocene interglacials:
Investigating the Mid-Brunhes Event in the British terrestrial sequence.
Earth-Sci. Rev. 103, 183–196.
https://doi.org/10.1016/j.earscirev.2010.09.007
Case, M.J., Lawler,
J.J., Tomasevic, J.A., 2015. Relative sensitivity to climate change of
species in northwestern North America. Biol. Conserv. 187, 127–133.
https://doi.org/10.1016/j.biocon.2015.04.013
Chattopadhyay, B.,
Garg, K.M., Ray, R., Rheindt, F.E., 2019. Fluctuating fortunes: genomes
and habitat reconstructions reveal global climate-mediated changes in
bats’ genetic diversity. Proc. R. Soc. B Biol. Sci. 286, 20190304.
https://doi.org/10.1098/rspb.2019.0304
Cleere, N., 1998.
Nightjars: a guide to nightjars, nighthawks, and their relatives. Yale
University Press, New Haven.
Cleere, N., Christie,
D., Rasmussen, P.C., 2021. Eurasian nightjar (Caprimulgus europaeus),
version 1.1 [WWW Document]. Birds World. URL
https://birdsoftheworld.org/bow/species/eurnig1/cur/introduction
(accessed 1.19.23).
Conway, G., Wotton,
S., Henderson, I., Langston, R., Drewitt, A., Currie, F., 2007. Status
and distribution of European nightjars Caprimulgus europaeus in the UK
in 2004. Bird Study 54, 98–111.
Cramp, S., Simmons,
K.E.L. (Eds.), 1985. The Birds of the Western Palearctic. Vol. IV. Terns
to Woodpeckers, First Edition. ed. Oxford University Press, Oxford.
de Greef, E.,
Brashear, W., Delmore, K.E., Fraser, K.C., 2022. Population structure,
patterns of natal dispersal and demographic history in a declining
aerial insectivore, the Purple martin Progne subis. J. Avian Biol. 2022,
e02929. https://doi.org/10.1111/jav.02929
Del Hoyo, J., Elliott,
A., Sargatal, J., Christie, D.A., de Juana, E., 2014. Handbook of the
birds of the world alive. Lynx Editions, Barcelona.
Denton, G.H., Hughes,
T.J., 1981. The last great ice sheets. Wiley Interscience, New York.
Ericson, P.G.P.,
Irestedt, M., Qu, Y., 2022. Demographic history, local adaptation and
vulnerability to climate change in a tropical mountain bird in New
Guinea. Divers. Distrib. 28, 2565–2578.
https://doi.org/10.1111/ddi.13614
Ericson, P.G.P., Qu,
Y., Blom, M.P.K., Johansson, U.S., Irestedt, M., 2017. A genomic
perspective of the Pink-headed duck Rhodonessa caryophyllacea suggests a
long history of low effective population size. Sci. Rep. 7, 16853.
https://doi.org/10.1038/s41598-017-16975-1
Evens, R., Conway,
G.J., Henderson, I.G., Cresswell, B., Jiguet, F., Moussy, C., Sénécal,
D., Witters, N., Beenaerts, N., Artois, T., 2017. Migratory pathways,
stopover zones and wintering destinations of Western European nightjars
Caprimulgus europaeus. Ibis 159, 680–686.
https://doi.org/10.1111/ibi.12469
Frankham, R., Ballou,
J.D., Briscoe, D.A., 2010. Introduction to conservation genetics.
Cambridge University Press, Cambridge.
https://doi.org/10.1017/CBO9780511809002
Han, K.-L., Robbins,
M.B., Braun, M.J., 2010. A multi-gene estimate of phylogeny in the
Nightjars and Nighthawks (Caprimulgidae). Mol. Phylogenet. Evol. 55,
443–453. https://doi.org/10.1016/j.ympev.2010.01.023
Hanna, Z.R.,
Henderson, J.B., Wall, J.D., Emerling, C.A., Fuchs, J., Runckel, C.,
Mindell, D.P., Bowie, R.C.K., DeRisi, J.L., Dumbacher, J.P., 2017.
Northern spotted owl (Strix occidentalis caurina) genome: Divergence
with the Barred owl (Strix varia) and Characterization of
light-associated genes. Genome Biol. Evol. 9, 2522–2545.
https://doi.org/10.1093/gbe/evx158
Hansson, B.,
Hasselquist, D., Tarka, M., Zehtindjiev, P., Bensch, S., 2008.
Postglacial colonisation patterns and the role of Isolation and
expansion in driving diversification in a passerine bird. PLOS ONE 3,
e2794. https://doi.org/10.1371/journal.pone.0002794
Head, M.J., Gibbard,
P.L., 2015. Early–Middle Pleistocene transitions: Linking terrestrial
and marine realms. Quat. Int. 389, 7–46.
https://doi.org/10.1016/j.quaint.2015.09.042
Hewitt, C.D.,
Broccoli, A.J., Mitchell, J.F.B., Stouffer, R.J., 2001. A coupled model
study of the Last Glacial Maximum: Was part of the North Atlantic
relatively warm? Geophys. Res. Lett. 28, 1571–1574.
https://doi.org/10.1029/2000GL012575
Hewitt, G.M., 2004.
Genetic consequences of climatic oscillations in the Quaternary. Philos.
Trans. R. Soc. Lond. B. Biol. Sci. 359, 183–195.
https://doi.org/10.1098/rstb.2003.1388
Hewitt, G.M., 1999.
Post-glacial re-colonization of European biota. Biol. J. Linn. Soc. 68,
87–112. https://doi.org/10.1111/j.1095-8312.1999.tb01160.x
Hohenlohe, P.A., Funk,
W.C., Rajora, O.P., 2021. Population genomics for wildlife conservation
and management. Mol. Ecol. 30, 62–82.
https://doi.org/10.1111/mec.15720
Kimmitt, A.A., Pegan,
T.M., Jones, A.W., Wacker, K.S., Brennan, C.L., Hudon, J., Kirchman,
J.J., Ruegg, K., Benz, B.W., Herman, R., Winger, B.M., 2023. Genetic
evidence for widespread population size expansion in North American
boreal birds prior to the Last Glacial Maximum. Proc. R. Soc. B Biol.
Sci. 290, 20221334. https://doi.org/10.1098/rspb.2022.1334
Kozma, R., Lillie, M.,
Benito, B.M., Svenning, J.-C., Höglund, J., 2018. Past and potential
future population dynamics of three grouse species using ecological and
whole genome coalescent modelling. Ecol. Evol. 8, 6671–6681.
https://doi.org/10.1002/ece3.4163
Kozma, R., Melsted,
P., Magnússon, K.P., Höglund, J., 2016. Looking into the past - the
reaction of three grouse species to climate change over the last million
years using whole genome sequences. Mol. Ecol. 25, 570–580.
https://doi.org/10.1111/mec.13496
Langston, R.H.W.,
Wotton, S.R., Conway, G.J., Wright, L.J., Mallord, J.W., Currie, F.A.,
Drewitt, A.L., Grice, P.V., Hoccom, D.G., Symes, N., 2007. Nightjar
Caprimulgus europaeus and Woodlark Lullula arborea- recovering species
in Britain?: Recovery of Nightjar and Woodlark. Ibis 149, 250–260.
https://doi.org/10.1111/j.1474-919X.2007.00709.x
Larsen, C., Speed, M.,
Harvey, N., Noyes, H.A., 2007. A molecular phylogeny of the nightjars
(Aves: Caprimulgidae) suggests extensive conservation of primitive
morphological traits across multiple lineages. Mol. Phylogenet. Evol.
42, 789–796. https://doi.org/10.1016/J.YMPEV.2006.10.005
Li, H., Durbin, R.,
2011. Inference of human population history from individual whole-genome
sequences. Nature 475, 493–496. https://doi.org/10.1038/nature10231
Li, X., Dong, F., Lei,
F., Alström, P., Zhang, R., Ödeen, A., Fjeldså, J., Ericson, P.G.P.,
Zou, F., Yang, X., 2016. Shaped by uneven Pleistocene climate:
mitochondrial phylogeographic pattern and population history of White
wagtail Motacilla alba (Aves: Passeriformes). J. Avian Biol. 47,
263–274. https://doi.org/10.1111/jav.00826
Lisiecki, L.E., Raymo,
M.E., 2005. A Pliocene-Pleistocene stack of 57 globally distributed
benthic δ18O records. Paleoceanogr Paleoclimatol 20.
https://doi.org/10.1029/2004PA001071
Lombardo, G., Rambaldi
Migliore, N., Colombo, G., Capodiferro, M.R., Formenti, G., Caprioli,
M., Moroni, E., Caporali, L., Lancioni, H., Secomandi, S., Gallo, G.R.,
Costanzo, A., Romano, A., Garofalo, M., Cereda, C., Carelli, V.,
Gillespie, L., Liu, Y., Kiat, Y., Marzal, A., López-Calderón, C.,
Balbontín, J., Mousseau, T.A., Matyjasiak, P., Møller, A.P., Semino, O.,
Ambrosini, R., Bonisoli-Alquati, A., Rubolini, D., Ferretti, L.,
Achilli, A., Gianfranceschi, L., Olivieri, A., Torroni, A., 2022. The
mitogenome relationships and phylogeography of Barn swallows (Hirundo
rustica). Mol. Biol. Evol. 39. https://doi.org/10.1093/molbev/msac113
Lowe, A., Rogers,
A.C., Durrant, K.L., 2014. Effect of human disturbance on long-term
habitat use and breeding success of the European Nightjar, Caprimulgus
europaeus. Avian Conserv. Ecol. 9.
Mather, N., Traves,
S.M., Ho, S.Y.W., 2019. A practical introduction to sequentially
Markovian coalescent methods for estimating demographic history from
genomic data. Ecol. Evol. 10, 579–589.
https://doi.org/10.1002/ece3.5888
Mitchell, L.J.,
Horsburgh, G.J., Dawson, D.A., Maher, K.H., Arnold, K.E., 2022.
Metabarcoding reveals selective dietary responses to environmental
availability in the diet of a nocturnal, aerial insectivore, the
European nightjar (Caprimulgus europaeus). Ibis 164, 60–73.
https://doi.org/10.1111/ibi.13010
Nadachowska-Brzyska,
K., Burri, R., Smeds, L., Ellegren, H., 2016. PSMC analysis of effective
population sizes in molecular ecology and its application to
black-and-white Ficedula flycatchers. Mol. Ecol. 25, 1058–1072.
https://doi.org/10.1111/mec.13540
Nadachowska-Brzyska,
K., Li, C., Smeds, L., Zhang, G., Ellegren, H., 2015. Temporal dynamics
of avian populations during Pleistocene revealed by whole-genome
sequences. Curr. Biol. CB 25, 1375–1380.
https://doi.org/10.1016/j.cub.2015.03.047
Norevik, G., Åkesson,
S., Hedenström, A., 2017. Migration strategies and annual space-use in
an Afro-Palaearctic aerial insectivore – the European nightjar
Caprimulgus europaeus. J. Avian Biol. 48, 738–747.
https://doi.org/10.1111/jav.01071
Olsson, U., Leader,
P.J., Carey, G.J., Khan, A.A., Svensson, L., Alström, P., 2013. New
insights into the intricate taxonomy and phylogeny of the Sylvia curruca
complex. Mol. Phylogenet. Evol. 67, 72–85.
https://doi.org/10.1016/j.ympev.2012.12.023
Pârâu, L.G., Wink, M.,
2021. Common patterns in the molecular phylogeography of western
palearctic birds: a comprehensive review. J. Ornithol. 162, 937–959.
https://doi.org/10.1007/s10336-021-01893-x
Patil, A.B., Vijay,
N., 2021. Repetitive genomic regions and the inference of demographic
history. Heredity 127, 151–166.
https://doi.org/10.1038/s41437-021-00443-8
Pisias, N.G., Moore,
T.C., 1981. The evolution of Pleistocene climate: A time series
approach. Earth Planet. Sci. Lett. 52, 450–458.
https://doi.org/10.1016/0012-821X(81)90197-7
Ponti, R., Arcones,
A., Ferrer, X., Vieites, D.R., 2020. Lack of evidence of a Pleistocene
migratory switch in current bird long-distance migrants between Eurasia
and Africa. J. Biogeogr. 47, 1564–1573.
https://doi.org/10.1111/jbi.13834
Prado-Martinez, J.,
Sudmant, P.H., Kidd, J.M., Li, H., Kelley, J.L., Lorente-Galdos, B.,
Veeramah, K.R., Woerner, A.E., O’Connor, T.D., Santpere, G., Cagan, A.,
Theunert, C., Casals, F., Laayouni, H., Munch, K., Hobolth, A., Halager,
A.E., Malig, M., Hernandez-Rodriguez, J., Hernando-Herraez, I., Prüfer,
K., Pybus, M., Johnstone, L., Lachmann, M., Alkan, C., Twigg, D., Petit,
N., Baker, C., Hormozdiari, F., Fernandez-Callejo, M., Dabad, M.,
Wilson, M.L., Stevison, L., Camprubí, C., Carvalho, T., Ruiz-Herrera,
A., Vives, L., Mele, M., Abello, T., Kondova, I., Bontrop, R.E., Pusey,
A., Lankester, F., Kiyang, J.A., Bergl, R.A., Lonsdorf, E., Myers, S.,
Ventura, M., Gagneux, P., Comas, D., Siegismund, H., Blanc, J.,
Agueda-Calpena, L., Gut, M., Fulton, L., Tishkoff, S.A., Mullikin, J.C.,
Wilson, R.K., Gut, I.G., Gonder, M.K., Ryder, O.A., Hahn, B.H., Navarro,
A., Akey, J.M., Bertranpetit, J., Reich, D., Mailund, T., Schierup,
M.H., Hvilsom, C., Andrés, A.M., Wall, J.D., Bustamante, C.D., Hammer,
M.F., Eichler, E.E., Marques-Bonet, T., 2013. Great ape genetic
diversity and population history. Nature 499, 471–475.
https://doi.org/10.1038/nature12228
Ralston, J.,
FitzGerald, A.M., Burg, T.M., Starkloff, N.C., Warkentin, I.G.,
Kirchman, J.J., 2021. Comparative phylogeographic analysis suggests a
shared history among eastern North American boreal forest birds.
Ornithology 138, ukab018. https://doi.org/10.1093/ornithology/ukab018
Sambrook, J., Fritsch,
E.F., Maniatis, T., 1989. Molecular cloning: a laboratory manual. Cold
Spring Harbor Laboratory Press.
Sánchez Goñi, M.F.,
Eynaud, F., Turon, J.L., Shackleton, N.J., 1999. High resolution
palynological record off the Iberian margin: direct land-sea correlation
for the Last Interglacial complex. Earth Planet. Sci. Lett. 171,
123–137. https://doi.org/10.1016/S0012-821X(99)00141-7
Sato, Y., Ogden, R.,
Kishida, T., Nakajima, N., Maeda, T., Inoue-Murayama, M., 2020.
Population history of the Golden eagle inferred from whole-genome
sequencing of three of its subspecies. Biol. J. Linn. Soc. 130,
826–838. https://doi.org/10.1093/biolinnean/blaa068
Schmitt, T., 2007.
Molecular biogeography of Europe: Pleistocene cycles and postglacial
trends. Front. Zool. 4, 11. https://doi.org/10.1186/1742-9994-4-11
Schweizer, M.,
Etzbauer, C., Shirihai, H., Töpfer, T., Kirwan, G.M., 2020. A molecular
analysis of the mysterious Vaurie’s nightjar Caprimulgus centralasicus
yields fresh insight into its taxonomic status. J. Ornithol. 161,
635–650. https://doi.org/10.1007/s10336-020-01767-8
Secomandi, S., Spina,
F., Formenti, G., Gallo, G.R., Caprioli, M., Ambrosini, R., Riello, S.,
Wellcome Sanger Institute Tree of Life programme, Wellcome Sanger
Institute Scientific Operations: DNA Pipelines collective, Tree of Life
Core Informatics collective, Darwin Tree of Life Consortium, 2021. The
genome sequence of the European nightjar, Caprimulgus europaeus
(Linnaeus, 1758). Wellcome Open Res. 6, 332.
https://doi.org/10.12688/wellcomeopenres.17451.1
Smeds, L., Qvarnström,
A., Ellegren, H., 2016. Direct estimate of the rate of germline mutation
in a bird. Genome Res. 26, 1211–1218.
https://doi.org/10.1101/gr.204669.116
Termignoni-Garcia, F.,
Kirchman, J.J., Clark, J., Edwards, S.V., 2022. Comparative population
genomics of cryptic speciation and adaptive divergence in Bicknell’s and
Gray-cheeked thrushes (Aves: Catharus bicknelli and Catharus minimus).
Genome Biol. Evol. 14, evab255. https://doi.org/10.1093/gbe/evab255
Thorup, K., Pedersen,
L., da Fonseca, R.R., Naimi, B., Nogués-Bravo, D., Krapp, M., Manica,
A., Willemoes, M., Sjöberg, S., Feng, S., Chen, G., Rey-Iglesia, A.,
Campos, P.F., Beyer, R., Araújo, M.B., Hansen, A.J., Zhang, G., Tøttrup,
A.P., Rahbek, C., 2021. Response of an Afro-Palearctic bird migrant to
glaciation cycles. Proc. Natl. Acad. Sci. 118, e2023836118.
https://doi.org/10.1073/pnas.2023836118
Väli, Ü., Treinys, R.,
Bergmanis, U., Daroczi, S., Demerdzhiev, D., Dombrovski, V., Dravecký,
M., Ivanovski, V., Kicko, J., Langgemach, T., Lontkowski, J.,
Maciorowski, G., Poirazidis, K., Rodziewicz, M., Meyburg, B.-U., 2022.
Contrasting patterns of genetic diversity and lack of population
structure in the Lesser spotted eagle Clanga pomarina (Aves:
Accipitriformes) across its breeding range. Biol. J. Linn. Soc. 136,
506–519. https://doi.org/10.1093/biolinnean/blac065
Van Andel, T.H.,
Tzedakis, P.C., 1996. Palaeolithic landscapes of Europe and environs,
150,000-25,000 years ago: An overview. Quat. Sci. Rev. 15, 481–500.
https://doi.org/10.1016/0277-3791(96)00028-5
Yao, H., Zhang, Y.,
Wang, Z., Liu, G., Ran, Q., Zhang, Z., Guo, K., Yang, A., Wang, N.,
Wang, P., 2022. Inter-glacial isolation caused divergence of
cold-adapted species: the case of the Snow partridge. Curr. Zool. 68,
489–498. https://doi.org/10.1093/cz/zoab075