Introduction
Clusters of alpine high mountain ecosystems that are isolated by
different environmental conditions in the intervening lowlands can
behave as authentic archipelagos. These sky islands contain unique
diversity and provide natural laboratories to study evolution,
speciation and the effects of habitat fragmentation (Hedberg, 1969;
McCormack, Huang, & Knowles, 2009). However, their extent of isolation
has changed with climatic fluctuations during the Quaternary, in
particular in tropical regions. Colder conditions during glacial periods
led to the expansion of high altitude alpine and montane forest
ecosystems into lower elevations, thus facilitating population expansion
and connectivity between populations previously isolated on mountain
tops (Hewitt, 2000). These cycles and fluctuations in gene flow promoted
differentiation processes that led to exceptionally high levels of
endemism (Williams, Vivero, Spawls, Anteneh, & Ensermu, 2004). On the
other hand, these ecosystems are especially sensitive to future climate
change, and as a result of climatic warming their area is rapidly
diminishing (Moritz & Agudo, 2013), a process which will increase the
isolation and extinction risk of their associated flora and fauna. This
process is expected to be particularly intense in the scarce alpine
environments distributed at high elevations across the tropics. Tropical
mountains are predicted to experience the highest levels of extinctions
and changes to fauna assemblages under future climate change (Lawler et
al., 2009). High altitude species living close to mountain tops may lose
their entire range as their suitable climatic regime and its associated
ecosystem disappears with increasing temperatures (Pimm, 2009; Williams,
Jackson, & Kutzbach, 2007).
This problem is especially acute in under-studied and highly threatened
areas like the Ethiopian Highlands, where accelerated land conversion
and degradation is placing further pressures on biodiversity (Yalden,
Largen, Kock, & Hillman, 1996). The Ethiopian Highlands are a vast
extent of high ground rising up to 4620 masl with a low altitude limit
of 1500 masl. They cover an area of 519,278 km2 in the
otherwise arid zone of the Horn of Africa and include 73% of the
Afroalpine biome (areas above 3200 masl) in Sub-Saharan Africa (Williams
et al., 2004). The Great Rift Valley crosses the Ethiopian central
highlands dividing them into two main blocks, north-east and south-west
(Ebinger et al., 2000).
The Afroalpine biome shows one of the highest rate of endemism in the
world due to a combination of their relative small areas, high isolation
and climatic history (Reyes-Velasco, Manthey, Freilich, & Boissinot,
2018; S. D. Williams et al., 2004). These endemics are either of
Palearctic (e.g. the Ethiopian ibex, Capra walie, the Ethiopian
long-eared bat, Plecotus balensis ) or Afrotropical origin (e.g.
geladas monkeys, Theropithecus gelada, the mountain nyala,Tragelaphus buxtoni ) (Harmsen, Spence, & Mahaney, 1991).
Although the source of colonisers of this truly unique environment is
probably more complex, including also long-distance vagrants like the
endemic plover (Vanellus melanocephala ) (Kingdon, 1990). Rapid
human population growth in Ethiopia over the past 150 years, from
approximately 6.6 million in 1868 (Nyssen et al., 2014) to more than 100
million (UN, 2019), and the corresponding increase in pressure on
natural environments and human encroachment into national parks and
other protected areas has resulted in extensive habitat degradation
(Kidane, Stahlmann, & Beierkuhnlein, 2012). This pressure has been
implicated with biodiversity losses, from the decline of endemic frogs
(Gower et al., 2013) to the decline of large flagship mammal species
such as the endemic Ethiopian wolf, Canis simensis (Stephens,
d’Sa, Sillero-Zubiri, & Leader-Williams, 2001). However, some signs of
vegetation recovery have been observed since the early
21st century following the initiation of environmental
recovery programs in the 1980s and the establishment of new protected
areas closing up to 15% of the country to livestock grazing (Nyssen et
al., 2014).
Recently, a new species of the long-eared bat genus Plecotus was
described in the Ethiopian Highlands above 3000 m, the Bale long-eared
bat, Plecotus balensis , which is endemic to Ethiopia and possibly
Eritrea (Juste et al., 2004; Kruskop & Laverenchenko, 2000), and is
known by only a few specimens from just seven localities (Benda, Kiefer,
Hanák, & Veith, 2004). The genus Plecotus is widely distributed
across the Palearctic, and is characterised by high cryptic
diversification and specific altitudinal and climatic associations
(Spitzenberger, Strelkov, Winkler, & Haring, 2006). Due to their
limited long-distance dispersal abilities and habitat specialisations,Plecotus bats are particularly sensitive to habitat loss (Razgour
et al., 2014) and the effects of future climate change (Razgour et al.,
2013). Bats can be good bio-indicators of environmental change (Jones,
Jacobs, Kunz, Willig, & Racey, 2009) and have been used to test
biogeographical hypotheses on the role of topographic barriers and past
climate change in delimiting species distribution and shaping genetic
composition (e.g. Flanders et al., 2009; Razgour et al., 2013).
We use this recently described high altitude bat to study how sky
islands and historic versus current patterns of environmental
heterogeneity shape the distribution and genetic diversity of their
unique fauna. We project ecological niche models (ENMs) across temporal
scales to track the effect of past climate changes on range suitability
for P. balensis and predict impacts of future changes. We
integrate approximate Bayesian computation inference of demographic
history with landscape genetics analysis and markers with different
mutation rates to disentangle the impact of historic vicariance events
versus recent anthropogenic habitat loss and degradation on population
size, genetic diversity and genetic connectivity of sky island
biodiversity. Our study highlights threats to tropical montane
biodiversity due to the combined effects of multiple stressors, being
squeezed into higher altitudes due to climate change while losing
genetic diversity and suffering population declines due to anthropogenic
land-use change.