Written by Andrew Harrington.
The lesser horseshoe bat (Rhinolophus hipposideros) is one of the smallest of Ireland’s nine resident bat species, weighing only about 7 grams, roughly the same as a two-euro coin. The little lesser horseshoe is unusual among Irish bats in that it is our only resident member of the horseshoe bat family, so named for the rounded protrusion around its nose. It uses this odd-shaped nose almost like a small trumpet to focus the sonar-like echolocation calls it makes (yes, it echolocates through its nose!) to allow it to navigate and to detect its insect prey. All other Irish bats are members of the vesper bat family, which echolocate through their mouths and so lack the horseshoe’s extravagant nose. It remains to be seen whether the greater horseshoe bat (Rhinolophus ferrumequinum), which was recently discovered in Ireland in County Wexford, is indeed breeding here and can be considered a true “native”, or if it is a vagrant or coloniser which strayed from its usual home in Wales or France.
From their western outpost of their global range in Ireland, they are present across Europe and North Africa into the Middle East and into Central Asia as far east as Pakistan, usually inhabiting woodland and scrub habitat. However, despite this broad geographical spread the lesser horseshoe bat is in decline in many parts of their range, becoming extinct in the Netherlands, Luxembourg, many parts of Germany and other areas of Central Europe in the 1960s and ‘70s due to the use of DDT, and experiencing severe population declines in other areas due to pesticide use and habitat loss. For this reason, the lesser horseshoe has the highest level of protection that an individual wildlife species can get in European Union law, being listed on “Annex 2” of the Habitats Directive. In Ireland, the lesser horseshoe bat is confined to the counties of the western seaboard from West Cork to Mayo. Although it has a restricted range in Ireland, our national population of about 12,500 lesser horseshoes is one of the largest known in Europe.
Sadly, although the number of lesser horseshoe bats in Europe is relatively stable they are still declining in some areas, and they are very slow to recolonise areas where they have become extinct due to human interference. Lesser horseshoe bats are small, are fairly weak and slow flyers by bat standards and they are also home birds, much preferring to live their entire lives in the area of their birth, if not the very roost site where they were born (although enough adventurous bats do allow the species to spread to suitable new areas, albeit very slowly).
However, the lesser horseshoe bat hides a more shadowy past, where great invasions and wanderings across vast expanses of Eurasia contrast with its slow pace of life in the present day. This saga has been revealed by a new paper by Dool et al. (2013), which looks at the patterns of diversity and distribution of different genes in the DNA of the lesser horseshoe bat and allowed the authors to look deep into the species’ history, revealing a fascinating story.
Dool and her co-authors examined several genes in the horseshoe bat genome for this study using samples from across the species’ range, including both mitochondrial and nuclear DNA genes. This allowed them to look into different stages of the horseshoe bat’s evolutionary history and in the process obtain insights into their geographical origin and how they later spread out from this homeland to populate their present range.
Their story begins before the great Pleistocene ice ages, sometime in the Pliocene (5.3- 2.6 million years ago). Nuclear intron DNA mutates at a very slow rate, leaving a signature of this distant time. Bats from the eastern part of the horseshoe’s range, from Tajikstan to Turkey, showed the highest diversity of this gene, indicating that the species most likely originated here sometime in the Pliocene. The first horseshoe colonisers at some point then crossed from Turkey into Europe and thereafter spread across the new continent. It is probable that only a small number of pioneers made the crossing, carrying a small set of nuclear intron haplotypes (varieties) with them to leave to their present-day descendants, in striking contrast to the haplotype diversity seen in their oriental relatives in this marker.
The newcomers gradually spread across Europe and from there even crossed into Morocco and Algeria via the straits of Gibraltar, but they arrived in a continent that was soon to be subjected to the encroachment of enormous glaciers with the onset of the ice ages during the Pleistocene (2.6 million to 11 thousand years ago). As the climate in the Pliocene was several degrees warmer than today, lesser horseshoe bats probably occupied a significant area of Europe, which would probably have looked broadly similar ecologically to today. However, they would have been unable to survive in northern areas and as the climate cooled they would have been forced ever further south as ice sheets began to form and advance across the continent. Eventually, they would have been backed into several “refugia” in the furthest south of Europe where a temperate climate persisted during the height of the cold when the rest of Europe was covered in ice, tundra and steppe, and the bats would have held on in these areas completely isolated from the rest of their species.
A picture of this period of the lesser horseshoe’s history can be gained by examining mitochondrial DNA, which evolves at a faster rate than nuclear introns and so gives population information on more recent times, up to about 1 million years ago. This gives us a snapshot of the mid to late Pleistocene, during the height of the cycles of alternating extreme cold and warmer conditions of the ice age. While the lesser horseshoes that had remained behind in their original homeland in Asia had no major barriers to their move south to follow the shift of their favoured habitat and avoid the encroaching ice sheets, the European bats periodically had to retreat to Iberia, Italy and the Balkan peninsula. They could move no further due to the Mediterranean Sea, and it was these refugia that provided the source of bats for the periodic re-population of Europe when the ice sheets temporarily retreated. This pattern can be clearly seen in the highly different mitochondrial DNA haplotypes seen in lesser horseshoes from Iberia, southern Italy and the Balkans, and the origins of the present-day populations in the rest of Europe can be traced back to their founder populations by examining their mitochondrial haplotypes.
However, the story at this point is not so simple. As the ice age has consisted of repeated cycles of extreme cold (glaciations) and intervening warm periods (interstadials), the process of retreat and re-population has happened again and again- the last 750 thousand years alone have witnessed at least eight major glaciations. Therefore, the pattern of mitochondrial haplotypes also show evidence of migration of bats across the continent, for example showing that bats from the Iberian refugium were able to migrate right across Europe to the Balkans probably during an interstadial, where their descendants survive today. Smaller refugia existed on Mediterranean islands like Crete, in North Africa and surprisingly there appears to have been two separate refugia within Iberia, in the north and the south.
Unusually, all of the present populations of lesser horseshoes in mainland Europe outside of Iberia and far southern Italy appear to be descended from Balkan ancestors. The more usual pattern seen in European mammals shows a more even mix of animals descended from Iberian, Italian and Balkan refugia, but not the lesser horseshoe! Balkan bats are even present in northern Italy, seemingly blocking southern Italian bats from spreading north, or alternatively some ecological barrier prevented Italian and Iberian bats from spreading north in this most recent interstadial. This rather complex pattern of echoes from the ice age is perhaps unsurprising when we remember that this is a small animal with rather specific habitat preferences, so even minor unsuitability of areas of habitat could have cut off even nearby populations from each other, as happened in Iberia.
The final genetic marker gives an insight into the present day gene flow between populations of lesser horseshoe bats. Microsatellites are genes present in nuclear DNA and are very fast evolving, so they are used to differentiate individual animals and give an idea of interbreeding or isolation of populations over the last few hundred years. Microsatellite diversity is high across most of the lesser horseshoe’s range, but decreases towards the north-western edge of its range in the British Isles. There appear to be distinct populations of lesser horseshoe bats in the Asian part of its range, in Morocco, and most of mainland Europe. But most interestingly, it appears that Spanish lesser horseshoes are not only cut off from their relatives in the rest of Europe, but that in fact northern and southern lesser horseshoes are also cut off from each other! This is a somewhat surprising result, and in light of the mitochondrial DNA it seems that the ice age pattern of small “islands” of lesser horseshoes in Iberia has persisted into the present day. There must be some impermeable and long-lasting hurdles that these bats cannot cross to reach their neighbours, which have lasted for tens of thousands of years. That they have survived for so long in isolation is reassuring, but with climate change causing warming and pressure on many Mediterranean species to move north such barriers could block an escape route for these populations and lead to their possible extinction in the future.
Serena Dool’s paper has partially lifted the mist of time and revealed some of the long and convoluted history of the lesser horseshoe bat over the last 3 million years- from the early colonisers of Europe, to survivors of the harsh ice ages, to today’s lesser horseshoes marooned in Iberia just out of reach of their relatives: a real odyssey. Although they appear small and vulnerable, lesser horseshoes have proved their toughness by surviving through one of the most turbulent periods of change in Earth’s history. They still face challenges from human activity and climate change, but with some luck they will continue their wanderings for a long time yet.
Dool SE, Puechmaille SJ, Dietz C, Juste J, Ibáñez C, Hulva P, Roué SG, Petit EJ, Jones G, Russo D, Toffoli R, Viglino A, Martinoli A, Rossiter SJ, & Teeling EC (2013). Phylogeography and postglacial recolonization of Europe by Rhinolophus hipposideros: evidence from multiple genetic markers. Molecular ecology, 22 (15), 4055-70 PMID: 23889545