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Research | Open Access

No signature of selection on the C-terminal region of glucose transporter 2 with the evolution of avian nectarivory

Alexander M. Myrka1,†, Tooba Shah2,†, Jason T. Weir2,3, Kenneth C. Welch Jr.2,3( )
Department of Cell and Systems Biology, University of Toronto, 25 Harbord St., Toronto, ON, M5S 3G5, Canada
Department of Biological Sciences, University of Toronto Scarborough, 1265 Military Trail, Toronto, ON, M1C 1A4, Canada
Department of Ecology and Evolutionary Biology, University of Toronto Scarborough, 1265 Military Trail, Toronto, ON, M1C 1A4, Canada

†Alexander M. Myrka and Tooba Shah co-first authors

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Abstract

Background

Flying birds, especially those that hover, need to meet high energetic demands. Birds that meet this demand through nectarivory face the added challenges of maintaining homeostasis in the face of spikes in blood sugar associated with nectar meals, as well as transporting that sugar to energetically demanding tissues. Nectarivory has evolved many times in birds and we hypothesized thatthe challenges of this dietary strategy would exert selective pressure on key aspects of metabolic physiology. Specifically, we hypothesized we would find convergent or parallel amino acid substitutions among different nectarivorous lineages in a protein important to sensing, regulating, and transporting glucose, glucose transporter 2 (GLUT2).

Methods

Genetic sequences for GLUT2 were obtained from ten pairs of nectarivorous and non-nectarivorous sister taxa. We performed PCR amplification of the intracellular C-terminal domain of GLUT2 and adjacent protein domains due to the role of this region in determination of transport rate, substrate specificity and glucosensing.

Results

Our findings have ruled out the C-terminal regulatory region of GLUT2 as a target for selection by sugar-rich diet among avian nectarivores, though selection among hummingbirds, the oldest avian nectarivores, cannot be discounted.

Conclusion

Our results indicate future studies should examine down-stream targets of GLUT2-mediated glucosensing and insulin secretion, such as insulin receptors and their targets, as potential sites of selection by nectarivory in birds.

Keywords

GlucoseDietAvianGLUT2NectarivoryGlucosensingInsulin signalling

References

 

Ali RS, Morag FD, Muhammad S, Sarver D, Hou L, Wong GW, et al. Glucose transporter expression and regulation following a fast in the ruby-throated hummingbird Archilochus colubris. J Exp Biol. 2020; 22: 9989. . https://doi.org/10.1242/jeb.229989
Crossref Google Scholar
 

Baker HG, Baker I, Hodges SA. Sugar composition of nectars and fruits consumed by birds and bats in the tropics and subtropics. Biotropica. 1998; 30: 559–86.
Crossref Google Scholar
 

Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL. GenBank. Nucleic Acids Res. 2005; 33: D34–8.
Crossref Google Scholar
 

Beuchat CA, Chong CR. Hyperglycemia in hummingbirds and its consequences for hemoglobin glycation. Comp Biochem Physiol A Mol Integr Physiol. 1998; 120: 409–16.
Crossref Google Scholar
 

Blem CR. Patterns of lipid storage and utilization in birds. Integr Comp Biol. 1976; 16: 671–84.
Crossref Google Scholar
 

Braun EJ, Sweazea KL. Glucose regulation in birds. Comp Biochem Physiol B Biochem Mol Biol. 2008; 151: 1–9.
Crossref Google Scholar
 

Burns KJ, Hackett SJ, Klein NK. Phylogenetic relationships of Neotropical honeycreepers and the evolution of feeding morphology. J Avian Biol. 2003; 34: 360–70.
Crossref Google Scholar
 

Byers M, Bohannon-Stewart A, Khwatenge C, Alqureish C, Alhathlol A, Nahashon S, et al. Absolute quantification of tissue specific expression of glucose transporters in chickens. J Mol Cell Biol. 2018; 1: 1–8.
Google Scholar
 

Carver FM, Shibley IA Jr, Pennington JS, Pennington SN. Differential expression of glucose transporters during chick embryogenesis. Cell Mol Life Sci CMLS. 2001; 58: 645–52.
Crossref Google Scholar
 

Duchêne S, Audouin E, Crochet S, Duclos MJ, Dupont J, Tesseraud S. Involvement of the ERK1/2 MAPK pathway in insulin-induced S6K1 activation in avian cells. Domest Anim Endocrinol. 2008; 34: 63–73.
Crossref Google Scholar
 

Dupont J, Dagou C, Derouet M, Simon J, Taouis M. Early steps of insulin receptor signaling in chicken and rat: apparent refractoriness in chicken muscle. Domest Anim Endocrinol. 2004; 26: 127–42.
Crossref Google Scholar
 

Dupont J, Tesseraud S, Simon J. Insulin signaling in chicken liver and muscle. Gen Comp Endocrinol. 2009; 163: 52–7.
Crossref Google Scholar
 

Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 2003; 31: 3784–8.
Crossref Google Scholar
 

Gaster M, Handberg A, Beck-Nielsen H, Schroder HD. Glucose transporter expression in human skeletal muscle fibers. Am J Physiol Endocrinol Metab. 2000; 279: E529–38.
Crossref Google Scholar
 

Guillemain G, Loizeau M, Pincon-Raymond M, Girard J, Leturque A. The large intracytoplasmic loop of the glucose transporter GLUT2 is involved in glucose signaling in hepatic cells. J Cell Sci. 2000; 113: 841–7.
Crossref Google Scholar
 

Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, et al. A phylogenomic study of birds reveals their evolutionary history. Science. 2008; 320: 1763–8.
Crossref Google Scholar
 

Hazelwood RL. The avian endocrine pancreas. Am Zool. 1973; 13: 699–709.
Crossref Google Scholar
 
Hedges SB, Kumar S. The timetree of life. New York: OUP Oxford; 2009.
 

Huang S, Czech MP. The GLUT4 glucose transporter. Cell Metab. 2007; 5: 237–52.
Crossref Google Scholar
 

Irestedt M, Ohlson JI. The division of the major songbird radiation into Passerida and 'core Corvoidea' (Aves: Passeriformes)— the species tree vs. gene trees. Zool Scr. 2008; 37: 305–13.
Crossref Google Scholar
 

Jetz W, Thomas GM, Joy JB, Hartmann K, Mooers AO. The global diversity of birds in space and time. Nature. 2012; 491: 444–8.
Crossref Google Scholar
 

Jønsson KA, Bowie RCK, Moyle RG, Irestedt M, Norman JA, Fjeldså J. Phylogeny and biogeography of Oriolidae (Aves: Passeriformes). Ecography. 2010; 33: 232–41.
Google Scholar
 

Katagiri H, Asano T, Ishihara H, Tsukuda K, Lin JL, Inukai K, et al. Replacement of intracellular C-terminal domain of GLUT1 glucose transporter with that of GLUT2 increases Vmax and Km of transport activity. J Biol Chem. 1992; 267: 22550–5.
Crossref Google Scholar
 

Kono T, Nishida M, Nishiki Y, Seki Y, Sato K, Akiba Y. Characterisation of glucose transporter (GLUT) gene expression in broiler chickens. Br Poult Sci. 2005; 46: 510–5.
Crossref Google Scholar
 

Leturque A, Brot-Laroche E, Gall ML. GLUT2 mutations, translocation, and receptor function in diet sugar managing. Am J Physiol-Endocrinol Metab. 2009; 296: E985–92.
Crossref Google Scholar
 

Long W, Cheeseman CI. Structure of, and functional insight into the GLUT family of membrane transporters. Cell Health Cytoskeleton. 2015; 7: 167–83.
Crossref Google Scholar
 

MacDonald JR, Ziman R, Yuen RKC, Feuk L, Scherer SW. The database of genomic variants: a curated collection of structural variation in the human genome. Nucleic Acids Res. 2014; 42: D986–92.
Crossref Google Scholar
 
Maddison WP, Maddison DR. Mesquite: a modular system for evolutionary analysis. Version 3.61. 2019. https://www.mesquiteproject.org.
 

Moyle R, Taylor S, Oliveros C, Lim H, Haines CL, Abdul Rahman M, et al. Diversification of an endemic Southeast Asian genus: phylogenetic relationships of the spiderhunters (Nectariniidae: Arachnothera). Auk. 2011; 128: 777–88.
Crossref Google Scholar
 

Mueckler M, Thorens B. The SlC2 (GLUT) family of membrane transporters. Mol Aspects Med. 2013; 34: 121–38.
Crossref Google Scholar
 

Nicolson SW, Fleming PA. Nectar as food for birds: the physiological consequences of drinking dilute sugar solutions. Plant Syst Evol. 2003; 238: 139–53.
Crossref Google Scholar
 

OsorIo-Fuentealba C, Contreras-Ferrat AE, Altamirano F, Espinosa A, Li Q, Niu W, et al. Electrical stimuli release ATP to increase GLUT4 translocation and glucose uptake via PI3K[gamma]-Akt-AS160 in skeletal muscle cells. Diabetes. 2013; 62: 1519–26.
Crossref Google Scholar
 

Polakof S, Mommsen TP, Soengas JL. Glucosensing and glucose homeostasis: from fish to mammals. Comp Biochem Physiol B Biochem Mol Biol. 2011; 160: 123–49.
Crossref Google Scholar
 
R Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2020. URL https://www.R-project.org/.
 

Reding DM, Foster JT, James HF, Pratt HD, Fleischer RC. Convergent evolution of 'creepers' in the Hawaiian honeycreeper radiation. Biol Lett. 2009; 5: 221–4.
Crossref Google Scholar
 

Rideau N, Derouet M, Grimsby J, Simon J. Glucokinase activation induces potent hypoglycemia without recruiting insulin and inhibits food intake in chicken. Gen Comp Endocrinol. 2010; 169: 276–83.
Crossref Google Scholar
 

Roberts MW. Hummingbirds' nectar concentration preferences at low volume: the importance of time scale. Anim Behav. 1996; 52: 361–70.
Crossref Google Scholar
 
Schuchmann K-L. Handbook of the birds of the world. Barcelona: Lynx Editions; 2015.
 

Seatter MJ, De la Rue SA, Porter LM, Gould GW. QLS motif in transmembrane helix Ⅶ of the glucose transporter family interacts with the C-1 position of D-glucose and is involved in substrate selection at the exofacial binding site. Biochemistry. 1998; 37: 1322–6.
Crossref Google Scholar
 

Sedano RE, Burns KJ. Are the Northern Andes a species pump for Neotropical birds? Phylogenetics and biogeography of a clade of Neotropical tanagers (Aves: Thraupini). J Biogeogr. 2010; 37: 325–43.
Crossref Google Scholar
 

Seki Y, Sato K, Kono T, Abe H, Akiba Y. Broiler chickens (Ross strain) lack insulin-responsive glucose transporter GLUT4 and have GLUT8 cDNA. Gen Comp Endocrinol. 2003; 133: 80–7.
Crossref Google Scholar
 

Shen B, Han X, Zhang J, Rossiter SJ, Zhang S. Adaptive evolution in the glucose transporter 4 gene Slc2a4 in Old World fruit bats (family: Pteropodidae). PLoS ONE. 2012; 7: e33197.
Crossref Google Scholar
 

Shepherd PR, Kahn BB. Glucose transporters and insulin action— implications for insulin resistance and diabetes mellitus. N Engl J Med. 1999; 341: 248–57.
Crossref Google Scholar
 

Sweazea KL, Braun EJ. Glucose transporter expression in English sparrows (Passer domesticus). Comp Biochem Physiol B Biochem Mol Biol. 2006; 144: 263–70.
Crossref Google Scholar
 

Taniguchi CM, Emanuelli B, Kahn CR. Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol. 2006; 7: 85–96.
Crossref Google Scholar
 

Thorens B. Glucose transporters in the regulation of intestinal, renal, and liver glucose fluxes. Am J Physiol-Gastrointest Liver Physiol. 1996; 270: G541–53.
Crossref Google Scholar
 

Thorens B. GLUT2 glucose sensing and glucose homeostasis. Diabetologia. 2015; 58: 221–32.
Crossref Google Scholar
 

Thorens B, Mueckler M. Glucose transporters in the 21st Century. Am J Physiol-Endocrinol Metab. 2010; 298: E141–5.
Crossref Google Scholar
 

Uldry M, Thorens B. The SLC2 family of facilitated hexose and polyol transporters. Pflüg Arch. 2004; 447: 480–9.
Crossref Google Scholar
 

Wals PA, Katz J. Glucokinase in bird liver a membrane bound enzyme. Biochem Biophys Res Commun. 1981; 100: 1543–8.
Crossref Google Scholar
 

Warren BH, Bermingham E, Prys-Jones RP, Thébaud C. Immigration, species radiation and extinction in a highly diverse songbird lineage: white-eyes on Indian Ocean islands. Mol Ecol. 2006; 15: 3769–86.
Crossref Google Scholar
 

Weir JT, Bermingham E, Schluter D. The Great American Biotic Interchange in birds. Proc Natl Acad Sci. 2009; 106: 21737–42.
Crossref Google Scholar
 

Witteveen M, Brown M, Downs CT. Does sugar content matter? Blood plasma glucose levels in an occasional and specialist avian nectarivore. Comp Biochem Physiol Part A Mol Integr Physiol. 2014; 167: 40–4.
Crossref Google Scholar
 

Workman RE, Myrka AM, Wong GW, Tseng E, Welch KC, Timp W. Single-molecule, full-length transcript sequencing provides insight into the extreme metabolism of the ruby-throated hummingbird Archilochus colubris. GigaScience. 2018; 7: 1–12.
Crossref Google Scholar
 

Wright TF, Schirtzinger EE, Matsumoto T, Eberhard JR, Graves JR, Sanchez JJ. A multilocus molecular phylogeny of the parrots (Psittaciformes): support for a Gondwanan origin during the Cretaceous. Mol Biol Evol. 2008; 25: 2141–56.
Crossref Google Scholar
 

Wu L, Fritz JD, Powers AC. Different functional domains of GLUT2 glucose transporter are required for glucose affinity and substrate specificity. Endocrinology. 1998; 139: 4205–12.
Crossref Google Scholar
 

Zhang S, Yang L, Yang X, Yang J. Molecular phylogeny of the yuhinas (Sylviidae: Yuhina): A paraphyletic group of babblers including Zosterops and Philippine Stachyris. J Ornithol. 2007; 148: 417–26.
Crossref Google Scholar
 

Zhang W, Sumners LH, Siegel PB, Cline MA, Gilbert ER. Quantity of glucose transporter and appetite-associated factor mRNA in various tissues after insulin injection in chickens selected for low or high body weight. Physiol Genomics. 2013; 45: 1084–94.
Crossref Google Scholar
 

Zhao F-Q, Keating AF. Functional properties and genomics of glucose transporters. Curr Genomics. 2007; 8: 113–28.
Crossref Google Scholar
 

Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003; 31: 3406–15.
Crossref Google Scholar
Avian Research
Volume 11 Issue 1,
January 2020
Article number: 44
DOI: 10.1186/s40657-020-00231-8
Cite this article:
Myrka AM, Shah T, Weir JT, et al. No signature of selection on the C-terminal region of glucose transporter 2 with the evolution of avian nectarivory. Avian Research, 2020, 11(1): 44. https://doi.org/10.1186/s40657-020-00231-8

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Received: 17 April 2020
Accepted: 28 October 2020
Published: 06 November 2020
© The Author(s) 2020.

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