吸血蝙蝠食性特化及其研究现状
|
摘要
翼手目动物(蝙蝠)的食性多样性丰富,其食物包括昆虫、鱼类、两栖动物、爬行动物、鸟类、哺乳动物、植物果实、花、花粉、花蜜、叶片和血液等。其中,大约70%的蝙蝠主要以昆虫为食,而以血液为食的吸血蝙蝠只有3种,它们是哺乳动物中唯一的仅以血液为食的动物类群。因此,吸血蝙蝠是研究动物食性演化的重要模式动物。本文综述了吸血蝙蝠在形态学、生理学、行为学、感觉系统和肠道微生物等方面的研究,指出了吸血蝙蝠食性特化的适应性特征。随着普通吸血蝠高质量基因组的公布,我们将有机会探究食性相关基因在吸血蝙蝠中的功能改变,阐明动物食性转变的分子机理。本文将为吸血蝙蝠和其它动物食性转变的研究提供有益的参考。
Members of Chiroptera(i.e. bats) possess a huge diversity of diets, which include insects, fish, amphibians, reptiles, birds, mammals, fruits, flowers, nectar, pollen, foliage, and blood.Of bats, approximately 70% of bat species are insectivorous, while only three species of bats(i.e. vampire bats) feed exclusively on blood.Vampire bats are the only group in mammals that drink blood, which appear to be unique and have become an attractive animal model to study dietary shift of mammals.Here we review studies on morphology, physiology, behavior, sensory systems, and gut microbiota in vampire bats, and highlight their adaptive traits of dietary specializations.Following the release of a high-quality genome sequence of the common vampire bat, we will have opportunities to explore functional changes of diet-related genes in vampire bats, aiming to dissect the molecular basis of dietary shift in animals.This review will be helpful in future studies of dietary changes in vampire bats and other animals.
Members of Chiroptera(i.e. bats) possess a huge diversity of diets, which include insects, fish, amphibians, reptiles, birds, mammals, fruits, flowers, nectar, pollen, foliage, and blood.Of bats, approximately 70% of bat species are insectivorous, while only three species of bats(i.e. vampire bats) feed exclusively on blood.Vampire bats are the only group in mammals that drink blood, which appear to be unique and have become an attractive animal model to study dietary shift of mammals.Here we review studies on morphology, physiology, behavior, sensory systems, and gut microbiota in vampire bats, and highlight their adaptive traits of dietary specializations.Following the release of a high-quality genome sequence of the common vampire bat, we will have opportunities to explore functional changes of diet-related genes in vampire bats, aiming to dissect the molecular basis of dietary shift in animals.This review will be helpful in future studies of dietary changes in vampire bats and other animals.
引文
Altringham J D.1996.Bats: Biology and Behavior.Oxford:Oxford University Press.
Bachmanov A A, Beauchamp G K.2007.Taste receptor genes.Annual Review of Physiology,27:389-414.
Benavides J A,Valderrama W, Streicker D G.2016.Spatial expansions and travelling waves of rabies in vampire bats.Proceedings of the Royal Society B: Biological Sciences,283:20160328.
Bhatnagar K P.1988.Ultrastructure of the pineal body of the common vampire bat, Desmodus rotundus.Developmental Dynamics,181:163-178.
Bobrowiec P E D, Lemes M R, Gribel R.2015.Prey preference of the common vampire bat (Desmodus rotundus, Chiroptera) using molecular analysis.Journal of Mammalogy,96:54-63.
Bohmann K, Gopalakrishnan S, Nielsen M,Nielsen L D S B, Jones G, Streicker D G, Gilbert M T P.2018.Using DNA metabarcoding for simultaneous inference of common vampire bat diet and population structure.Molecular Ecology Resources,18:1050-1063.
Breidenstein C P.1982.Digestion and assimilation of bovine blood by a vampire bat (Desmodus rotundus).Journal of Mammalogy,63:482-484.
Carter G, Leffer L.2015.Social grooming in bats:are vampire bats exceptional?PLoS ONE,10:e0138430.
Carter G, Wilkinson G.2013.Does food sharing in vampire bats demonstrate reciprocity?Communicative & Integrative Biology,6:e25783.
Caterina M J, Schumacher M A,Tominaga M, Rosen T A, Levine J D, Julius D.1997.The capsaicin receptor: a heat-activated ion channel in the pain pathway.Nature,389:816-824.
Damak S, Rong M Q, Yasumatsu K,Kokrashvili Z, Pérez C A, Shigemura N, Yoshida R, Mosinger B Jr, Glendinning J I, Ninomiya Y, Margolskee R F.2006.Trpm5 null mice respond to bitter, sweet, and umami compounds.Chemical Senses,31:253-264.
Delpietro H A, Russo R G, Carter G G,Carter G G, Lord R D, Delpietro G L.2017.Reproductive seasonality, sex ratio and philopatry in Argentina’s common vampire bats.Royal Society Open Science,4:160959.
Edwards M A, Kaufman M L, Storvick C A.1957.Microbiologic assay for the thiamine content of blood of various species of animals and man. American Journal of Clinical Nutrition,5:51-55.
Escalera-Zamudio M, Zepeda-Mendoza M L, Loza-Rubio E,Rojas-Anaya E, Méndez-Ojeda M L, Arias C F, Greenwood A D.2015.The evolution of bat nucleic acid-sensing Toll-like receptors.Molecular Ecology,24:5899-5909.
Fry B G, Roelants K,Champagne D E, Scheib H, Tyndall J D, King G F, Nevalainen T J, Norman J A, Lewis R J, Norton R S, Renjifo C, de la Vega R C.2009.The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms.Annual Review of Genomics and Human Genetics,10:483-511.
Gonzalez-Fernandez F.2003.Interphotoreceptor retinoid-binding protein-an old gene for new eyes.Vision Research,43:3021-3036.
Gracheva E O, Cordero-Morales J F,González-Carcacía J A, Ingolia N T, Manno C, Aranguren C I, Weissman J S, Julius D.2011.Ganglion-specific splicing of TRPV1 underlies infrared sensation in vampire bats.Nature,476:88-91.
Greenhall A M.1988.Feeding behavior.In:Greenhall A M,Schmidt U eds.Natural History of Vampire Bats.Boca Raton, FL:CRC Press,111-131.
Hand S J, Weisbecker V,Beck R M, Archer M, Godthelp H, Tennyson A J, Worthy T H.2009.Bats that walk: a new evolutionary hypothesis for the terrestrial behaviour of New Zealand’s endemic mystacinids.BMC Evolutionary Biology,9:169.
Herness M S, Gilbertson T A.1999.Cellular mechanisms of taste transduction.Annual Review of Physiology,61:873-900.
Hombach S, Janssen-Bienhold U,S?hl G, Schubert T, Büssow H, Ott T, Weiler R, Willecke K.2004.Functional expression of connexin 57 in horizontal cells of the mouse retina.European Journal of Neuroscience,19:2633-2640.
Hong W, Zhao H.2014.Vampire bats exhibit evolutionary reduction of bitter taste receptor genes common to other bats.Proceedings of the Royal Society B-Biological Sciences,281:20141079.
Huguin M, Arechiga-Ceballos N, Delaval M, Guidez A, de Castro I J, Lacoste V, Salmier A, Setién A A, Silva C R, Lavergne A, de Thoisy B.2018.How social structure drives the population dyna-mics of the common vampire bat (Desmodus rotundus, Phyllostomidae) Journal of Heredity,109:393-404.
Ito F, Bernard E, Torres R A.2016.What is for Dinner? First report of human blood in the diet of the hairy-legged vampire bat Diphylla ecaudata.Acta Chiropterologica,18:509-515.
Johnson N, Arechiga-Ceballos N, Aguilar-Setien A.2014.Vampire bat rabies: ecology, epidemiology and control.Viruses,6:1911-1928.
Kinnamon S C, Margolskee R F.1996.Mechanisms of taste transduction.Current Opinion in Neurobiology,6:506-513.
Kishida R, Goris R C, Terashima S,Dubbeldam J L.1984.A suspected infrared-recipient nucleus in the brainstem of the vampire bat, Desmodus rotundus.Brain Research,322:351-355.
Koopman K F.1988.Systematics and distribution.In:Greenhall A M,Schmidt U eds.Natural history of Vampire Bats.Boca Raton,FL:CRC Press,7-17.
Kürten L, Schmidt U.1982.Thermoperception in the common vampire bat (Desmodus rotundus).Journal of Comparative Physiology,146:223-228.
Kürten L, Schmidt U.1984.Warm and cold receptors in the nose of the vampire bat Desmodus rotundus.Naturwissenschaften,71:327-328.
Leone A M, Crawshaw G J, Garner M M, Frasca S Jr, Stasiak I, Rose K, Neal D, Farina L L.2016.A retrospective study of the lesions associated with iron storage disease in captive egyptian fruit bats (Rousettus aegyptiacus).Journal of Zoo and Wildlife Medicine,47:45-55.
Lindemann B.1996.Taste reception.Physiological Reviews,76:718-766.
Lord R D.1992.Seasonal reproduction of vampire bats and its relation to seasonality of bovine rabies.Journal of Wildlife Diseases,28:292-294.
Low D H W,Sunagar K,Undheim E A,Ali S A,Alagon A C, Ruder T, Jackson T N, Pineda Gonzalez S, King G F, Jones A, Antunes A, Fry B G.2013.Dracula’s children:molecular evolution of vampire bat venom.Journal of Proteomics,89:95-111.
Macdonald D.1984.Encyclopedia of Mammals.New York: Facts on File.
Pan F, Keung J, Kim I B, Snuggs M B, Mills S L, O’Brien J, Massey S C.2012.Connexin 57 is expressed by the axon terminal network of B-type horizontal cells in the rabbit retina.Journal of Comparative Neurology,520:2256-2274.
Roper S D.1989.The cell biology of vertebrate taste receptors.Annual Review of Physiology,12:329-353.
Schafer K, Braun H A,Kürten L.1988.Analysis of cold and warm receptor activity in vampire bats and mice.Pflugers Archiv,412:188-194.
Schutt W A Jr, Altenbach J S, Chang Y H, Cullinane D M, Hermanson J W, Muradali F, Bertram J E.1997.The dynamics of flight-initiating jumps in the common vampire bat Desmodus rotundus.Journal of Experimental Biology,200:3003-3012.
Simmons N B.2005.Order Chiroptera.In: Wilson D E, Reeder D M eds.Mammal Species of the World: A Taxonomic and Geographic Reference.Washington, DC:Smithsonian Institution Press.
Shen B, Fang T,Dai M, Jones G, Zhang S.2013.Independent losses of visual perception genes Gja10 and Rbp3 in echolocating bats (Order: Chiroptera).PLoS ONE,8:e68867.
Sohl G, Joussen A,Kociok N, Willecke K. 2010.Expression of connexin genes in the human retina.BMC Ophthalmol,10:27.
Stasiak I M,Smith D A,Ganz T,Crawshaw G J, Hammermueller J D, Bienzle D, Lillie B N.2018.Iron storage disease (hemochromatosis) and hepcidin response to iron load in two species of pteropodid fruit bats relative to the common vampire bat.Journal of Comparative Physiology B,188:683-694.
Taruno A,Vingtdeux V,Ohmoto M,Ma Z,Dvoryanchikov G,Li A,Adrien L,Zhao H,Leung S,Abernethy M,Koppel J,Davies P,Civan M M,Chaudhari N,Matsumoto I,Hellekant G,Tordoff M G,Marambaud P,Foskett J K.2013.CALHM1 ion channel mediates purinergic neurotransmission of sweet,bitter and umami tastes.Nature,495:223-226.
Thompson R D, Elias D J, Shumake S A, Gaddis S E.1982.Taste preferences of the common vampire bat (Desmodus rotundus).Journal of Chemical Ecology,8:715-721.
Turner D.1975.The Vampire Bat,A Field Study in Behavior and Ecology.Baltimore and London: The Johns Hopkins University Press.
Volokhov D, Becker D,Bergner L,Camus M S,Orton R J,Chizhikov V E,Altizer S M,Streicker D G.2017.Novel hemotropic mycoplasmas are widespread and genetically diverse in vampire bats.Epidemiol Infect,145:3154-3167.
Zepeda Mendoza M L, Xiong Z, Escalera-Zamudio M,Runge A,Gilbert M.2018.Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat.Nature Ecology and Evolution,2:659-668.
Zhang Y, Hoon M, Chandrashekar J, Mueller K L, Cook B, Wu D, Zuker C S, Ryba N J.2003.Coding of sweet, bitter, and umami tastes:different receptor cells sharing similar signaling pathways.Cell,112:293-301.
Zhao H, Li J, Zhang J.2015.Molecular evidence for the loss of three basic tastes in penguins.Current Biology,25:R141-R142.
Zhao H, Xu D, Zhang S, Zhang J.2012.Genomic and genetic evidence for the loss of umami taste in bats.Genome Biology and Evolution,4:73-79.
Zhao H, Zhou Y, Pinto C, Charles-Dominique P, Galindo-González J, Zhang S, Zhang J.2010.Evolution of the sweet taste receptor gene Tas1r2 in bats.Molecular Biology and Evolution,27:2642-2650.
Bachmanov A A, Beauchamp G K.2007.Taste receptor genes.Annual Review of Physiology,27:389-414.
Benavides J A,Valderrama W, Streicker D G.2016.Spatial expansions and travelling waves of rabies in vampire bats.Proceedings of the Royal Society B: Biological Sciences,283:20160328.
Bhatnagar K P.1988.Ultrastructure of the pineal body of the common vampire bat, Desmodus rotundus.Developmental Dynamics,181:163-178.
Bobrowiec P E D, Lemes M R, Gribel R.2015.Prey preference of the common vampire bat (Desmodus rotundus, Chiroptera) using molecular analysis.Journal of Mammalogy,96:54-63.
Bohmann K, Gopalakrishnan S, Nielsen M,Nielsen L D S B, Jones G, Streicker D G, Gilbert M T P.2018.Using DNA metabarcoding for simultaneous inference of common vampire bat diet and population structure.Molecular Ecology Resources,18:1050-1063.
Breidenstein C P.1982.Digestion and assimilation of bovine blood by a vampire bat (Desmodus rotundus).Journal of Mammalogy,63:482-484.
Carter G, Leffer L.2015.Social grooming in bats:are vampire bats exceptional?PLoS ONE,10:e0138430.
Carter G, Wilkinson G.2013.Does food sharing in vampire bats demonstrate reciprocity?Communicative & Integrative Biology,6:e25783.
Caterina M J, Schumacher M A,Tominaga M, Rosen T A, Levine J D, Julius D.1997.The capsaicin receptor: a heat-activated ion channel in the pain pathway.Nature,389:816-824.
Damak S, Rong M Q, Yasumatsu K,Kokrashvili Z, Pérez C A, Shigemura N, Yoshida R, Mosinger B Jr, Glendinning J I, Ninomiya Y, Margolskee R F.2006.Trpm5 null mice respond to bitter, sweet, and umami compounds.Chemical Senses,31:253-264.
Delpietro H A, Russo R G, Carter G G,Carter G G, Lord R D, Delpietro G L.2017.Reproductive seasonality, sex ratio and philopatry in Argentina’s common vampire bats.Royal Society Open Science,4:160959.
Edwards M A, Kaufman M L, Storvick C A.1957.Microbiologic assay for the thiamine content of blood of various species of animals and man. American Journal of Clinical Nutrition,5:51-55.
Escalera-Zamudio M, Zepeda-Mendoza M L, Loza-Rubio E,Rojas-Anaya E, Méndez-Ojeda M L, Arias C F, Greenwood A D.2015.The evolution of bat nucleic acid-sensing Toll-like receptors.Molecular Ecology,24:5899-5909.
Fry B G, Roelants K,Champagne D E, Scheib H, Tyndall J D, King G F, Nevalainen T J, Norman J A, Lewis R J, Norton R S, Renjifo C, de la Vega R C.2009.The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms.Annual Review of Genomics and Human Genetics,10:483-511.
Gonzalez-Fernandez F.2003.Interphotoreceptor retinoid-binding protein-an old gene for new eyes.Vision Research,43:3021-3036.
Gracheva E O, Cordero-Morales J F,González-Carcacía J A, Ingolia N T, Manno C, Aranguren C I, Weissman J S, Julius D.2011.Ganglion-specific splicing of TRPV1 underlies infrared sensation in vampire bats.Nature,476:88-91.
Greenhall A M.1988.Feeding behavior.In:Greenhall A M,Schmidt U eds.Natural History of Vampire Bats.Boca Raton, FL:CRC Press,111-131.
Hand S J, Weisbecker V,Beck R M, Archer M, Godthelp H, Tennyson A J, Worthy T H.2009.Bats that walk: a new evolutionary hypothesis for the terrestrial behaviour of New Zealand’s endemic mystacinids.BMC Evolutionary Biology,9:169.
Herness M S, Gilbertson T A.1999.Cellular mechanisms of taste transduction.Annual Review of Physiology,61:873-900.
Hombach S, Janssen-Bienhold U,S?hl G, Schubert T, Büssow H, Ott T, Weiler R, Willecke K.2004.Functional expression of connexin 57 in horizontal cells of the mouse retina.European Journal of Neuroscience,19:2633-2640.
Hong W, Zhao H.2014.Vampire bats exhibit evolutionary reduction of bitter taste receptor genes common to other bats.Proceedings of the Royal Society B-Biological Sciences,281:20141079.
Huguin M, Arechiga-Ceballos N, Delaval M, Guidez A, de Castro I J, Lacoste V, Salmier A, Setién A A, Silva C R, Lavergne A, de Thoisy B.2018.How social structure drives the population dyna-mics of the common vampire bat (Desmodus rotundus, Phyllostomidae) Journal of Heredity,109:393-404.
Ito F, Bernard E, Torres R A.2016.What is for Dinner? First report of human blood in the diet of the hairy-legged vampire bat Diphylla ecaudata.Acta Chiropterologica,18:509-515.
Johnson N, Arechiga-Ceballos N, Aguilar-Setien A.2014.Vampire bat rabies: ecology, epidemiology and control.Viruses,6:1911-1928.
Kinnamon S C, Margolskee R F.1996.Mechanisms of taste transduction.Current Opinion in Neurobiology,6:506-513.
Kishida R, Goris R C, Terashima S,Dubbeldam J L.1984.A suspected infrared-recipient nucleus in the brainstem of the vampire bat, Desmodus rotundus.Brain Research,322:351-355.
Koopman K F.1988.Systematics and distribution.In:Greenhall A M,Schmidt U eds.Natural history of Vampire Bats.Boca Raton,FL:CRC Press,7-17.
Kürten L, Schmidt U.1982.Thermoperception in the common vampire bat (Desmodus rotundus).Journal of Comparative Physiology,146:223-228.
Kürten L, Schmidt U.1984.Warm and cold receptors in the nose of the vampire bat Desmodus rotundus.Naturwissenschaften,71:327-328.
Leone A M, Crawshaw G J, Garner M M, Frasca S Jr, Stasiak I, Rose K, Neal D, Farina L L.2016.A retrospective study of the lesions associated with iron storage disease in captive egyptian fruit bats (Rousettus aegyptiacus).Journal of Zoo and Wildlife Medicine,47:45-55.
Lindemann B.1996.Taste reception.Physiological Reviews,76:718-766.
Lord R D.1992.Seasonal reproduction of vampire bats and its relation to seasonality of bovine rabies.Journal of Wildlife Diseases,28:292-294.
Low D H W,Sunagar K,Undheim E A,Ali S A,Alagon A C, Ruder T, Jackson T N, Pineda Gonzalez S, King G F, Jones A, Antunes A, Fry B G.2013.Dracula’s children:molecular evolution of vampire bat venom.Journal of Proteomics,89:95-111.
Macdonald D.1984.Encyclopedia of Mammals.New York: Facts on File.
Pan F, Keung J, Kim I B, Snuggs M B, Mills S L, O’Brien J, Massey S C.2012.Connexin 57 is expressed by the axon terminal network of B-type horizontal cells in the rabbit retina.Journal of Comparative Neurology,520:2256-2274.
Roper S D.1989.The cell biology of vertebrate taste receptors.Annual Review of Physiology,12:329-353.
Schafer K, Braun H A,Kürten L.1988.Analysis of cold and warm receptor activity in vampire bats and mice.Pflugers Archiv,412:188-194.
Schutt W A Jr, Altenbach J S, Chang Y H, Cullinane D M, Hermanson J W, Muradali F, Bertram J E.1997.The dynamics of flight-initiating jumps in the common vampire bat Desmodus rotundus.Journal of Experimental Biology,200:3003-3012.
Simmons N B.2005.Order Chiroptera.In: Wilson D E, Reeder D M eds.Mammal Species of the World: A Taxonomic and Geographic Reference.Washington, DC:Smithsonian Institution Press.
Shen B, Fang T,Dai M, Jones G, Zhang S.2013.Independent losses of visual perception genes Gja10 and Rbp3 in echolocating bats (Order: Chiroptera).PLoS ONE,8:e68867.
Sohl G, Joussen A,Kociok N, Willecke K. 2010.Expression of connexin genes in the human retina.BMC Ophthalmol,10:27.
Stasiak I M,Smith D A,Ganz T,Crawshaw G J, Hammermueller J D, Bienzle D, Lillie B N.2018.Iron storage disease (hemochromatosis) and hepcidin response to iron load in two species of pteropodid fruit bats relative to the common vampire bat.Journal of Comparative Physiology B,188:683-694.
Taruno A,Vingtdeux V,Ohmoto M,Ma Z,Dvoryanchikov G,Li A,Adrien L,Zhao H,Leung S,Abernethy M,Koppel J,Davies P,Civan M M,Chaudhari N,Matsumoto I,Hellekant G,Tordoff M G,Marambaud P,Foskett J K.2013.CALHM1 ion channel mediates purinergic neurotransmission of sweet,bitter and umami tastes.Nature,495:223-226.
Thompson R D, Elias D J, Shumake S A, Gaddis S E.1982.Taste preferences of the common vampire bat (Desmodus rotundus).Journal of Chemical Ecology,8:715-721.
Turner D.1975.The Vampire Bat,A Field Study in Behavior and Ecology.Baltimore and London: The Johns Hopkins University Press.
Volokhov D, Becker D,Bergner L,Camus M S,Orton R J,Chizhikov V E,Altizer S M,Streicker D G.2017.Novel hemotropic mycoplasmas are widespread and genetically diverse in vampire bats.Epidemiol Infect,145:3154-3167.
Zepeda Mendoza M L, Xiong Z, Escalera-Zamudio M,Runge A,Gilbert M.2018.Hologenomic adaptations underlying the evolution of sanguivory in the common vampire bat.Nature Ecology and Evolution,2:659-668.
Zhang Y, Hoon M, Chandrashekar J, Mueller K L, Cook B, Wu D, Zuker C S, Ryba N J.2003.Coding of sweet, bitter, and umami tastes:different receptor cells sharing similar signaling pathways.Cell,112:293-301.
Zhao H, Li J, Zhang J.2015.Molecular evidence for the loss of three basic tastes in penguins.Current Biology,25:R141-R142.
Zhao H, Xu D, Zhang S, Zhang J.2012.Genomic and genetic evidence for the loss of umami taste in bats.Genome Biology and Evolution,4:73-79.
Zhao H, Zhou Y, Pinto C, Charles-Dominique P, Galindo-González J, Zhang S, Zhang J.2010.Evolution of the sweet taste receptor gene Tas1r2 in bats.Molecular Biology and Evolution,27:2642-2650.