Today marks the release of the genome for Pteropus rufus, the Madagascar flying fox. ‘Flying foxes’ is the term used to describe Old World Fruit Bats of the family Pteropodidae, a unique family of pollen-, nectar- and fruit-eating bats belonging to the suborder Yinpterochiroptera (previously known as the ‘megabats’) [1]. Because these bats use sight instead of echolocation to track their food resources, they lack the elongated ears of their insectivorous bat cousins (suborder Yangterochiroptera) and instead, have dog – or fox! – like faces. In Malagasy, the native language of Madagascar, the word for fruit bat is “fanihy”, and we call our research group – based out of UC Berkeley, the University of Antananarivo, and Institut Pasteur of Madagascar – ‘Ekipa Fanihy’ for ‘Team Fruit Bat’.
Old World Fruit Bats are found only in Asia, Africa, Australia, and the Indian Ocean islands [1]. Because many pteropodid species are island endemics with small population sizes vulnerable to environmental stressors [2], these bats are highly endangered. The International Union for the Conservation of Nature (IUCN) classifies 35% of Old World Fruit Bats as threatened, nearly three times the extent (12%) for all other bat species combined [3].
The island-nation of Madagascar is home to three endemic pteropodids—the IUCN-listed ‘Vulnerable’ Madagascar flying fox (Pteropus rufus) and Madagascar fruit bat (Eidolon dupreanum), as well as the ‘Near-threatened’ Madagascar rousette (Rousettus madagascariensis) [4]. These bats offer important ecosystem services as pollinators and seed dispersers across the island [5,6], but they are also hunted widely as a source of human food [7].
A 2003 field survey estimated about 300,000 Pteropus rufus to inhabit Madagascar [8], but recent roost site reassessments suggest this number may have declined by as much as 40% in recent years [9]. Pteropus rufus is the largest and most heavily hunted of the three Malagasy fruit bats, and bat hunting is legal during the Malagasy winter (1 May – 1 September), which directly precedes the P. rufus birth season [10]. Ekipa Fanihy’s population modeling suggests that the species is undergoing serious population decline [11]. We’re currently engaged in active conservation and restoration efforts designed to reconstruct fruit bat roosting habitat in an effort to pull this species back from the brink.
Ekipa Fanihy has been studying the dynamics of viral infection in Malagasy fruit bats since 2013. Old World Fruit Bats have been disproportionately linked to the emergence of human viruses in the past two decades, serving as reservoir hosts for rabies and related lyssaviruses, Hendra and Nipah henipaviruses, Ebola and Marburg filoviruses and SARS coronavirus [12,13]. Several genomic analyses have demonstrated unique adaptations related to the evolution of flight which appear to have elongated bat lifespans and also made them resilient to many of the pathogenic effects of viral hosting [14–16].
In collaboration with DNA Zoo, we are assembling Madagascar fruit bat genomes in order to learn more about the mechanisms which underlie these bats’ unique viral tolerance. Our work has demonstrated that several zoonotic virus families circulate in our Malagasy bats [17]. Collaborators in Australia [18] have shown that stressed bats in poor nutritional condition actually shed more viruses than healthier individuals, heightening the risk of cross-species transmission. We hope that by restoring Pteropus rufus habitat and improving these bats’ nutritional conditions, we can find a ‘win-win’ solution for both conservation and public health alike.
Assembly of this genome was financed by DNA Zoo and an NIH grant (R01-AI129822-01) administered by Dr. Jean-Michel Héraud of Institut Pasteur of Madagascar and Dr. Cara Brook of UC Berkeley (link: http://grantome.com/grant/NIH/R01-AI129822-01).
Bibliography
[1] E.C. Teeling, M.S. Springer, O. Madsen, P. Bates, S.J. O’brien, W.J. Murphy, A molecular phylogeny for bats illuminates biogeography and the fossil record., Science (80-. ). 307 (2005) 580–4. doi:10.1126/science.1105113.
[2] C.C. Voigt, T. Kingston, Bats in the Anthropocene: Conservation of Bats in a Changing World, 2016. doi:10.1007/978-3-319-25220-9.
[3] Species IUCN Red List Threat., IUCN 2018. Version 2018-2., (n.d.).
[4] S.M. Goodman, Les chauves-souris de Madagascar [in French], Association Vahatra, Antananarivo, Madagascar, 2011.
[5] A. Bollen, L. Van Elsacker, Feeding ecology of Pteropus rufus (Pteropodidae) in the littoral forest of Sainte Luce, SE Madagascar, Acta Chiropterologica. 4 (2002) 33–47.
[6] M. Picot, R.K.B. Jenkins, O. Ramilijaona, P.A. Racey, S.M. Carrie, The feeding ecology of Eidolon dupreanum (Pteropodidae) in eastern Madagascar, Afr. J. Ecol. 45 (2007) 645–650. doi:10.1111/j.1365-2028.2007.00788.x.
[7] R.K.B. Jenkins, P.A. Racey, Bats as bushmeat in Madagascar, Madagascar Conserv. Dev. 3 (2008) 22–30.
[8] J.L. MacKinnon, C.E. Hawkins, P.A. Racey, Pteropodidae, Fruit Bats, Fanihy, Angavo, in: S.M. Goodman, J.P. Benstead (Eds.), Nat. Hist. Madagascar, The Universit of Chicago Press, 2003: pp. 1299–1302.
[9] R. Oleksy, P.A. Racey, G. Jones, High-resolution GPS tracking reveals habitat selection and the potential for long-distance seed dispersal by Madagascan flying foxes Pteropus rufus, Glob. Ecol. Conserv. (2015). doi:10.1016/j.gecco.2015.02.012.
[10] H.C. Ranaivoson, J.-M. Héraud, H.K. Goethert, S.R. Telford III, L. Rabetafika, C.E. Brook, Babesial infection in the Madagascan flying fox, Pteropus rufus É. Geoffroy, 1803, Parasit. Vectors. (2019) 1–13.
[11] C.E. Brook, H.C. Ranaivoson, D. Andriafidison, M. Ralisata, J. Razafimanahaka, J. Héraud, A.P. Dobson, C.J. Metcalf, Population trends for two Malagasy fruit bats, Biol. Conserv. 234 (2019) 165–171. doi:10.1016/j.biocon.2019.03.032.
[12] C.H. Calisher, J.E. Childs, H.E. Field, K. V Holmes, T. Schountz, Bats: Important reservoir hosts of emerging viruses, Clin. Microbiol. Rev. 19 (2006) 531–45. doi:10.1128/CMR.00017-06.
[13] C.E. Brook, A.P. Dobson, Bats as “special” reservoirs for emerging zoonotic pathogens, Trends Microbiol. 23 (2015) 172–180. doi:10.1016/j.tim.2014.12.004.
[14] S.S. Pavlovich, S.P. Lovett, G. Koroleva, J.C. Guito, C.E. Arnold, E.R. Nagle, K. Kulcsar, A. Lee, F. Thibaud-Nissen, A.J. Hume, E. Mühlberger, L.S. Uebelhoer, J.S. Towner, R. Rabadan, M. Sanchez-Lockhart, T.B. Kepler, G. Palacios, The Egyptian Rousette genome reveals unexpected features of bat antiviral immunity, Cell. 173 (2018) 1–13. doi:10.1016/j.cell.2018.03.070.
[15] G. Zhang, C. Cowled, Z. Shi, Z. Huang, K. a Bishop-Lilly, X. Fang, J.W. Wynne, Z. Xiong, M.L. Baker, W. Zhao, M. Tachedjian, Y. Zhu, P. Zhou, X. Jiang, J. Ng, L. Yang, L. Wu, J. Xiao, Y. Feng, Y. Chen, X. Sun, Y. Zhang, G. a Marsh, G. Crameri, C.C. Broder, K.G. Frey, L.-F. Wang, J. Wang, Comparative analysis of bat genomes provides insight into the evolution of flight and immunity, Science. 339 (2013) 456–60. doi:10.1126/science.1230835.
[16] I. Seim, X. Fang, Z. Xiong, A. V Lobanov, Z. Huang, S. Ma, Y. Feng, A. a Turanov, Y. Zhu, T.L. Lenz, M. V Gerashchenko, D. Fan, S. Hee Yim, X. Yao, D. Jordan, Y. Xiong, Y. Ma, A.N. Lyapunov, G. Chen, O.I. Kulakova, Y. Sun, S.-G. Lee, R.T. Bronson, A. a Moskalev, S.R. Sunyaev, G. Zhang, A. Krogh, J. Wang, V.N. Gladyshev, Genome analysis reveals insights into physiology and longevity of the Brandt’s bat Myotis brandtii., Nat. Commun. 4 (2013) 2212. doi:10.1038/ncomms3212.
[17] C.E. Brook, H.C. Ranaivoson, C.C. Broder, A.A. Cunningham, J.-M. Héraud, A.J. Peel, L. Gibson, J.L.N. Wood, C.J. Metcalf, A.P. Dobson, Disentangling serology to elucidate henipa- and filovirus transmission in Madagascar fruit bats, J. Anim. Ecol. 00 (2019) 1– 16. doi:10.1111/1365-2656.12985.
[18] R.K. Plowright, P. Eby, P.J. Hudson, I.L. Smith, D. Westcott, W.L. Bryden, D. Middleton, P. a Reid, R. a McFarlane, G. Martin, G.M. Tabor, L.F. Skerratt, D.L. Anderson, G. Crameri, D. Quammen, D. Jordan, P. Freeman, L.-F. Wang, J.H. Epstein, G. a Marsh, N.Y. Kung, H. McCallum, Ecological dynamics of emerging bat virus spillover., Proc. R. Soc. B. 282 (2015). doi:10.1098/rspb.2014.2124.