Discussion
Through combining ecological niche modelling, ABC inference of
demographic history and landscape genetics we show how historic climatic
changes during the Quaternary have shaped the population structure and
patterns of genetic variation of the biodiversity in Afromontane and
Afroalpine sky islands. We further show the impact of recent
anthropogenic land-use change and habitat degradation on population
declines and loss of genetic diversity in species that are also
threatened by disappearing suitable niche under future climate change in
one of the most endemism rich and endangered ecosystem in the world
(Williams et al., 2004).
Effects of climate change past and
future
Ecological niche models support the restricted distribution of P.
balensis in Afroalpine moorland and Afromontane grassland and woodland
high elevation regions of the Ethiopian highlands, and show that its
distribution is primarily limited by temperatures. Models projected
across temporal scales show that climatic suitability for P.
balensis has been progressively decreasing since the LGM and will
continue to decrease with increasing temperatures over the next few
decades, with a direct effect on population fragmentation and isolation.
The genus Plecotus is of Palearctic origin and is found primarily
across temperate and Mediterranean habitats (Spitzenberger et al.,
2006). As such, it is not surprising that climatic conditions in the
tropics were more suitable for this bat when temperatures were lower
during the LGM. Increased climatic suitability during LGM and
displacement of the Afroalpine and ericaceous zone to lower elevations
(Bonnefille, Roeland, & Guiot, 1990) allowed high altitude species to
extend their range (Gottelli, Marino, Sillero-Zubiri, & Funk, 2004) and
likely led to contact between isolated sky island populations (McCormack
et al., 2009). This can explain the observed limited differentiation
between mountain ranges not separated by the substantially lower Rift
Valley.
Sky islands are sensitive to future climate change because the high
montane and alpine habitats could contract into higher elevations with
even minor temperature increases, reducing the habitat available for
their associated endemic taxa (McCormack et al., 2009). Tropical montane
forests, in particular, are some of the most threatened habitats under
climate warming (Moritz & Agudo, 2013). Tropical montane regions are
predicted to experience highest levels of disappearing climates, and
consequently species extinctions and community disruptions (Williams,
Jackson, & Kutzbach, 2007). In Ethiopia, Nyssen et al. (2014) already
identified evidence of upper shifts of the high elevation treeline in
response to climatic changes in the past century. This ecotone is
located between the Afromontane and Afroalpine zones and is particularly
rich in biodiversity (Kidane et al., 2012). Indeed our models predict
that only a quarter of the current range of P. balensis will
remain climatically suitable by the end of the century. These
predictions are relevant to other high altitude Afromontane
biodiversity, and therefore are particularly worrying given the high
levels of endemism found in this ecoregion, in particular among
vertebrates (Williams et al., 2004) and vascular plants (Gizaw et al.,
2016).
Effects of geographical barriers – Rift Valley and sky
islands
The Ethiopian Rift Valley was identified as the main barrier to
contemporary gene flow shaping the population structure of P.
balensis . The Great Rift Valley, extending from Lebanon through the Red
Sea to the Zambezi River, is less than 100 km wide across the Ethiopian
central highlands (Ebinger et al., 2000), dividing them into two massifs
from northwest to southeast. It played a major role in structuring
biodiversity across Eastern Africa, from the Afroalpine plantsArabis alpine (Asefa, Ehrich, Taberlet, Nemomissa, & Brochmann,
2007) and Lobelia giberroa (Kebede, Ehrich, Taberlet, Namomissa,
& Brochmann, 2007) to most of Ethiopian anurans (Freilich et al.,
2016), including the high altitude African clawed frogs, Xenopussp. (Evans, Bliss, Mendel, & Tinsley, 2011) and the forest tree frogs
(Reyes-Velasco et al., 2018). Interestingly, amphibians found at
elevations below 2500 masl did not show differences between the northern
and southern highland massifs (Freilich et al., 2016). As P.
balensis is associated with low temperatures and montane ecosystems
above 2000 m (Benda et al., 2004), the much warmer and drier
savannah-like habitats at low elevation along the Rift Valley are very
likely to be inhospitable for this bat. In fact, according to our data,
the main split along the Rift Valley, can be traced to the last
interglacial period when conditions were even warmer and drier than in
the Holocene (Adams, Maslin, & Thomas, 1999). Evidence of limited
allele sharing between both sides of the Rift Valley is most probably
related to the short time that elapsed since the last contact between
Afromontane habitats across the Rift Valley, rather than present day
gene flow.
The complex geological history of the Ethiopian highlands is partially
responsible for its high biodiversity and endemism. The highlands do not
constitute a single unit, but instead are formed by various massifs of
different areas, origins, ages and degrees of isolation (Reyes-Velasco
et al., 2018). Genomic differentiation in highland species, like the
river frog, Amietia nutti , is explained not only by the Rift
Valley but also by other major geographical barriers, the Blue Nile
Valley and the Omo River (Manthey, Reyes-Velasco, Freilich, &
Boissinot, 2017). This geographical and historical complexity is
expected to affect the phylogeography of P. balensis . The
isolation of sky islands is supported by the deep genetic structure
found in the mtDNA markers and the fact no haplotypes were shared
between mountain ranges and all mountain ranges formed separate clades
in the mtDNA tree. All clades, except the Bale population that included
deeply divergent basal lineages, could be the result of isolation
processes relating to older glacial cycles during the Pleistocene. These
episodes of allopatric isolation appear as the main driver of
differentiation in Ethiopian highland vertebrates (Reyes-Velasco et al.,
2018). The phylogeographic structure of P. balensis is consistent
with that of the Ethiopian wolf (Gottelli et al., 2004), whereby three
main clusters are present corresponding to the three well-defined
mountain areas: the southern Chilalo/Bale, the central Guassa/Abune
Yosef and the northern isolated Siemen Massifs. This strong structure at
the mtDNA level indicates that sky islands have acted as historic
barriers to gene flow in P. balensis . Sky islands are strong
isolating mechanism in limited dispersal species. For example, the
endemic high altitude spider Microhexura montivaga in the
southern Appalachians is divided into separate clades corresponding to
mountain ranges, though this species shows strong population subdivision
also at the nuclear level (Hedin, Carlson, & Coyle, 2015). In contrast,
in P. balensis the nuclear microsatellite dataset only identified
a split into two clusters, corresponding to the populations on either
side of the Rift Valley.
More limited population structure based on bi-parentally inherited
markers suggests that gene flow between mountain ranges is primarily
male-mediated, a common pattern in temperate bat species (Moussy et al.,
2013; Razgour, Salicini, Ibáñez, Randi, & Juste, 2015). However, as
extensive contemporary gene flow between mountain ranges is unlikely
given the extent of habitat conversion across the Ethiopian highlands
(Lemenih & Kassa, 2014), the shallow genetic structure at the nuclear
level, may instead indicate habitat connectivity during the Holocene,
possibly through montane forest bridges during episodes of increased
moisture (Umer et al., 2007). However, other Ethiopian highland species
do show strong structure and limited gene flow in bi-parentally
inherited markers, including the mountain nyala (Atickem et al., 2013)
and Ethiopian wolf, in which current gene flow is limited to
geographically close populations (Gottelli, Sillero-Zubiri, Marino,
Funk, & Wang, 2013). Alternatively, genetic differentiation may be
driven by local adaptations and environmental dissimilarity and
therefore its signature cannot be identified in neutral markers (Manthey
& Moyle, 2015).
Effects of anthropogenic land-use
change
Although ENMs identified that P. balensis is primarily associated
with Afroalpine moorland and grassland and Afromontane woodland
ecoregions, reproductive females and sub-adults were only found in high
altitude Afromontane woodlands, highlighting the importance of this
habitat for the species’ reproductive success. A similar pattern of
elevational segregation was observed in other Palearctic bats such as
the European noctules (Ibáñez et al., 2009) and the congeneric alpine
long-eared bat Plecotus macrobullaris (Alberdi, Aizpurua,
Aihartza, & Garin, 2014), whereby maternity colonies in colder regions
of the distribution are found below the treeline. Alberdi et al. (2014)
attribute this segregation to restrictions on facultative heterothermy
and use of torpor in pregnant and lactating females.
The Afromontane woodland habitat is highly threatened and disappearing
due to extensive deforestation and overgrazing (Yalden et al., 1996).
Deforestation rates in the Ethiopian Highlands are severe following
centuries of landscape changes due to subsistence farming, settlement
and demands for fuelwood (Lemenih & Kassa, 2014). Native forest cover
has declined in the past 100 years from 45% to only 5% of the country,
and currently most of the native forest cover in the highlands is
concentrated in small patches surrounding orthodox churches, known as
church forests (Abbott, 2019). The mountain forest belt has been pushed
upwards and fragmented due to extensive agriculture (Kebede et al.,
2007). Some of the forests where bats were caught south of the Rift
Valley were degraded, fragmented and showed limited evidence of
recruitment due to overgrazing of ground vegetation cover. This
represents a broader trend of forest degradation in the Bale Mountains
region, including inside the National Park, due to logging, fuelwood
collection and livestock grazing (Asefa, Mengesha, Shimelis, & Mamo,
2015), which has been linked with the recent declines of most large wild
mammals populations within the park (Stephens et al., 2001).
The recent decline of the south-eastern P. balensis population
identified in our ABC model-based inference appears to coincide with a
period of accelerated forest loss and degradation and the expansion of
agriculture, though causal mechanisms behind the decline were not tested
here. No evidence of decline in the north-western population could be
attributed to the general higher density of montane forests in the
wetter north, as well as the buffering effect of the thousands of church
forests containing native trees that are spread across the north-western
highlands (Klepeis et al., 2016). However, small sample sizes may have
limited the inference power of the ABC analysis when it comes to
identifying more moderate bottlenecks. Genetic diversity in the
Ethiopian wolf was also higher in the northern highlands (Gottelli et
al., 2004), indicating that habitat degradation in the south is having a
detrimental effect on Afroalpine and Afromontane mammals in general.
Although native forest loss has been more limited in the northern
highlands over the past 150 years, degradation is on-going in the more
recently settled Simien mountains (Nyssen et al., 2014), suggesting that
the northern highlands Afromontane biodiversity is also at risk.
Despite the strong effect of anthropogenic land-use change on genetic
diversity and population decline in P. balensis , indicators of
anthropogenic impact, like artificial lights at night and human
footprint index, did not affect gene flow. Low sample size (five
populations) may have reduced the power of the landscape genetics
statistical analysis, in particular when considering the combined impact
of more than one variable, and therefore this limitation may have
obscured the importance of some drivers of landscape resistance.
Although native church forest patches and small community-managed forest
reserves offer some level of landscape connectivity across the
agricultural and human settlement landscape, percent tree cover did not
affect genetic connectivity. However, this may be attributed to the tree
cover map used, which does not distinguish between native forests and
eucalyptus plantations (Hansen et al., 2013), and therefore could not
capture the effect of the landscape on the movement of P.
balensis . Instead, the landscape genetics analysis highlights the
importance of altitude and Afroalpine and Afromontane habitats. The
best-supported model gave lowest resistance costs to the high altitude
alpine moorland ecoregion, rather than the montane forest ecoregion,
perhaps due to the more restricted distribution of native montane forest
than the ecoregion classification suggests because of extensive
deforestation in the past century. Alternatively, this may reflect
temperature or other climatic limitations on the movement of P.
balensis , as is the case with other cold-adapted high altitude mammals,
like the American pika, Ochotona princeps (Castillo, Epps, Davis,
& Cushman, 2014). Altitude was also identified as the main landscape
element limiting gene flow in high altitude salamanders, alongside pond
network structure. However, genetic connectivity in these more limited
dispersal species was primarily affected by geographic distance
presumably due to the rarity of dispersal events in the extreme high
altitude environment (Savage, Fremier, & Bradley, 2010).
Conclusions
Using a combination of ecological niche models, landscape genetics and
ABC model-based inference of demographic history we show how historic
climate change and geographic barriers interact with recent
anthropogenic habitat loss and degradation to shape the population size,
structure, diversity and connectivity of tropical montane biodiversity.
Focusing on the endemic Ethiopian Highlands bat, P. balensis , we
found that despite strong associations with high altitude environments
and mtDNA pattern associated with sky island structure, some level of
genetic connectivity is maintained among sky islands, and only
substantially lower altitudes, like the Rift Valley, form a true barrier
to gene flow. Of particular concern are evidence of recent population
decline, likely in response to deforestation and land conversion, the
decline in genetic diversity with increasing arable land cover, and the
importance of Afroalpine and Afromontane ecoregions for both range
suitability and genetic connectivity between sky islands. Given that
similar patterns of genetic population structure have been recorded in
other high altitude mammals and amphibians, such losses of genetic
diversity and population declines may be widespread in tropical montane
ecosystems. The situation described for this bat epitomises a wider
trend in high altitude Afromontane and Afroalpine biodiversity, which is
under threat from extensive deforestation, agricultural conversion and
overgrazing following rapid human population expansion (Yalden et al.,
1996). These threats are not likely to be reversed in the future in
countries like Ethiopia where accelerated human population growth is
projected to continue until the end of the century (UN, 2019). These
immediate threats will interact with future climate change and the
projected disappearance of suitable climates and their associated
ecoregions in tropical montane regions (Williams et al., 2007), which
will increase the likelihood of extinction of high altitude species.
This study presents alarming predictions for the fate of tropical
montane and alpine biodiversity, projected to be squeezed to higher
altitudes (or even disappear) due to climate change while already losing
genetic diversity and suffering population declines due to anthropogenic
land-use change. The combination of these different threats can push
these ecosystems beyond their resilience limits. We conclude that
assessments of threats to biodiversity under global change should adopt
a holistic approach, simultaneously studying the effects of multiple
threats and considering the impacts of past events, present stressors
and future projections based on genetic, ecological and geographic
information.