1 INTRODUCTION
Throughout history, humans have had a considerable impact on the
distribution and viability of wild animal populations. This influence
has become increasingly prominent during the last centuries due to, for
example, overexploitation and habitat destruction (Newton, 2003; Dirzoet al. , 2014). As a result, many populations have become small,
fragmented, or even extinct (Young et al. , 2016). The drastic
declines in population sizes are known as population bottlenecks.
Population bottlenecks have profound consequences for the genetic
viability, adaptability, and long-term viability of species (Frankhamet al. , 2010). Small population size leads to genetic drift, loss
of genetic variation, increased risks of inbreeding depression, and
overall higher genetic load (Amos & Balmford, 2001; Díez-del-Molinoet al. , 2018). The extent of these consequences depends on the
severity of the population bottleneck: how fast the decline happens (in
generations) and how many individuals are left (Amos & Balmford, 2001).
Therefore, while some species are confronted with alarming rates of
inbreeding and loss of genetic variation as a result of a sharp
population contraction (e.g., Ewing et al. , 2008), others have
been thriving for hundreds and thousands of years despite small
population sizes and low genetic diversity (e.g., Milot et al. ,
2007; Johnson et al. , 2009).
Multiple factors may affect the viability of species and the outcomes of
population bottlenecks. For instance, a long generation time has been
argued to have a profound influence on buffering the deleterious effects
of bottlenecks and long-persistent small populations by reducing the
impact of genetic drift (Amos & Balmford, 2001). Furthermore,
populations on the edge of the species’ distribution commonly exhibit
lower genetic diversity compared to populations near the core of the
distribution due to smaller effective population sizes
(Ne), reduced gene flow, and stronger geographical
isolation (Vucetich & Waite, 2003; Eckert et al. , 2008). Lower
genetic diversity and greater differentiation of peripheral populations
are the main features of the central-marginal hypothesis (CMH), which
has been confirmed in many studies (e.g., Schwartz et al. , 2003;
Eckert et al. , 2008; Langin et al. , 2017; Rönkä et
al. , 2019), but also contradictory evidence exits (e.g., Sagarin &
Gaines, 2002; De Kort et al. , 2021). Another important
geographical aspect that influences genetic diversity is proximity to
the past glacial refugia. Glacial refugia served as havens for species
that were affected by climate cooling by providing favorable habitats
which allowed populations to survive and maintain genetic variation. As
a result of postglacial expansion, populations in close proximity to the
refugia typically show higher levels of genetic diversity, whereas
populations on the expansion frontier have lower genetic diversity
(Hewitt, 2000). Finally, for many species, greater intraspecific genetic
variation has been found in southern regions compared to northern ones,
because of a more stable environment and larger population sizes in the
lower latitudes (Smith et al. , 2017; Fonseca et al. ,
2023).
The golden eagle (Aquila chrysaetos ) is a long-lived raptor with
a wide Holarctic distribution (BirdLife International, 2023). As a
predator of game animals and domestic livestock, the species has been
heavily persecuted across Europe and North America (e.g., Watson, 2010).
In addition to direct persecution, golden eagles have suffered from
urban growth and forestry due to their sensitivity to anthropogenic
disturbances (Watson, 2010). Altogether, these have resulted in local
extinctions of golden eagles in various parts of their range (e.g.,
Ireland, southern Finland, and lowlands of central Europe), and in
overall population declines across the Holarctic region during the
19th–20th centuries (e.g.,
Bielikova et al. , 2010; Nebel et al. , 2015; Ollila, 2019;
Starikov, 2020). Golden eagles were protected in most parts of their
distribution by the end of the 20th century (e.g.,
Below, 2000; Whitfield et al. , 2008; Sato et al. , 2017).
As a consequence of conservation efforts and the species’ extensive
range, the golden eagle is currently classified as Least Concernby the International Union for Conservation of Nature (IUCN) both
globally, and in Europe (BirdLife International, 2023). The
classification reflects the overall stability, but regional populations
continue to face local threats, such as habitat destruction, human
disturbances, use of lead bullets and pesticides, collisions with wind
turbines, and illegal trade (e.g., Watson, 2010; D’Addario et
al. , 2019; Slabe et al. , 2022). Unfortunately, some vast regions
within the species’ distribution, such as Russia and much of Asia, are
lacking data on golden eagles, limiting conservation efforts. For
example, only a few small-scale scientific expeditions have been
organized to collect information on breeding, ecology, and distribution
of golden eagles in Russia, Kazakhstan, and Mongolia (e.g.,
Shagdarsuren, 1964; Smelansky et al. , 2020; Isaev et al. ,
2021). These expeditions have revealed that the species is generally
rare in many parts of Russia and Kazakhstan, and that there has been a
noticeable decline in their numbers in several regions in recent times
(e.g., Kerdanov & Nikolaev, 2019; Kazansky & Babushkin, 2021).
Nevertheless, the first studies that used population genetic tools for
golden eagles revealed interesting insights of their population history
(e.g., Bourke et al. , 2010; Judkins & van den Bussche, 2017;
Naito-Liederbach et al. , 2021; Nebel et al. , 2019, 2023).
For example, using global golden eagle data, Nebel et al. (2015)
identified two distinct mitochondrial lineages: a Mediterranean and a
Holarctic. Holarctic haplotypes were found across Europe, Asia and North
America, while the Mediterranean lineage was restricted to the
Mediterranean region (Nebel et al. , 2015; Judkins & van den
Bussche, 2017). A subsequent study using microsatellites demonstrated
genetic differentiation between Northern (Norway, Finland and Estonia)
and Southern (Mediterranean and Alpine regions) Europe, with a distinct
population in Scotland (Nebel et al. , 2019). However, the
detected nuclear differentiation was not identical to the
differentiation of the mitochondrial lineages (Nebel et al. ,
2019). Meanwhile, genetic research on golden eagles in Asia remains
sparse, with the exception of the extensive works on Japanese golden
eagles (Masuda et al. , 1998; Sato et al. , 2017;
Naito-Liederbach et al. , 2021) and a recent study in the
Mongol-Altai region (Nebel et al. , 2015, 2023).
Here we aimed to improve the knowledge on phylogeography of Eurasian
golden eagles by incorporating previously undersampled regions, such as
Russia and Central Asia. Using a combination of mitochondrial and
nuclear genetic markers, we re-evaluated population structure and
genetic differences between golden eagle populations in the Palearctic.
In addition, we studied demographic history and the effects of the
recent population bottleneck on the genetic variation of this species.