#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

An inter-island comparison of Darwin’s finches reveals the impact of habitat, host phylogeny, and island on the gut microbiome


Autoři: Wesley T. Loo aff001;  Rachael Y. Dudaniec aff002;  Sonia Kleindorfer aff003;  Colleen M. Cavanaugh aff001
Působiště autorů: Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, United States of America aff001;  Department of Biological Sciences, Macquarie University, Sydney, New South Wales, Australia aff002;  College of Science and Engineering, Flinders University, Adelaide, South Australia, Australia aff003;  Konrad Lorenz Research Center for Behaviour and Cognition and Department of Behavioural Biology, University of Vienna, Vienna, Austria aff004
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0226432

Souhrn

Darwin’s finch species in the Galapagos Archipelago are an iconic adaptive radiation that offer a natural experiment to test for the various factors that influence gut microbiome composition. The island of Floreana has the longest history of human settlement within the archipelago and offers an opportunity to compare island and habitat effects on Darwin’s finch microbiomes. In this study, we compare gut microbiomes in Darwin’s finch species on Floreana Island to test for effects of host phylogeny, habitat (lowlands, highlands), and island (Floreana, Santa Cruz). We used 16S rRNA Illumina sequencing of fecal samples to assess the gut microbiome composition of Darwin’s finches, complemented by analyses of stable isotope values and foraging data to provide ecological context to the patterns observed. Overall bacterial composition of the gut microbiome demonstrated co-phylogeny with Floreana hosts, recapitulated the effect of habitat and diet, and showed differences across islands. The finch phylogeny uniquely explained more variation in the microbiome than did foraging data. Finally, there were interaction effects for island × habitat, whereby the same Darwin’s finch species sampled on two islands differed in microbiome for highland samples (highland finches also had different diets across islands) but not lowland samples (lowland finches across islands had comparable diet). Together, these results corroborate the influence of phylogeny, age, diet, and sampling location on microbiome composition and emphasize the necessity for comprehensive sampling given the multiple factors that influence the gut microbiome in Darwin’s finches, and by extension, in animals broadly.

Klíčová slova:

Animal phylogenetics – Bacteria – Birds – Finches – Foraging – Islands – Microbiome – Stable isotopes


Zdroje

1. McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA. 2013;110: 3229–3236. doi: 10.1073/pnas.1218525110 23391737

2. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. 2012;486: 207–214. doi: 10.1038/nature11234 22699609

3. Hall AB, Tolonen AC, Xavier RJ. Human genetic variation and the gut microbiome in disease. Nature Reviews Genetics. Nature Publishing Group; 2017;18: 690–699. doi: 10.1038/nrg.2017.63

4. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, et al. Evolution of mammals and their gut microbes. Science. 2008;320: 1647–1651. doi: 10.1126/science.1155725 18497261

5. Muegge BD, Kuczynski J, Knights D, Clemente JC, Gonzalez A, Fontana L, et al. Diet Drives Convergence in Gut Microbiome Functions Across Mammalian Phylogeny and Within Humans. Science. 2011;332: 970–974. doi: 10.1126/science.1198719 21596990

6. Groussin M, Mazel F, Sanders JG, Smillie CS, Lavergne S, Thuiller W, et al. Unraveling the processes shaping mammalian gut microbiomes over evolutionary time. Nat Comms. Nature Publishing Group; 2017;8: ncomms14319. doi: 10.1038/ncomms14319 28230052

7. Caro TM, O’Doherty G. On the Use of Surrogate Species in Conservation Biology. Conservation Biology. Wiley/Blackwell (10.1111); 1999;13: 805–814. doi: 10.1046/j.1523-1739.1999.98338.x

8. Kropáčková L, Těšický M, Albrecht T, Kubovčiak J, Čížková D, Tomášek O, et al. Co-diversification of gastrointestinal microbiota and phylogeny in passerines is not explained by ecological divergence. Mol Ecol. 2017. doi: 10.1111/mec.14144 28401612

9. Hird SM, Sánchez C, Carstens BC, Brumfield RT. Comparative Gut Microbiota of 59 Neotropical Bird Species. Front Microbiol. 2015;6: 1403. doi: 10.3389/fmicb.2015.01403 26733954

10. Nayfach S, Rodriguez-Mueller B, Garud N, Pollard KS. An integrated metagenomics pipeline for strain profiling reveals novel patterns of bacterial transmission and biogeography. Genome Research. Cold Spring Harbor Lab; 2016;26: 1612–1625. doi: 10.1101/gr.201863.115 27803195

11. van Dongen WF, White J, Brandl HB, Moodley Y, Merkling T, Leclaire S, et al. Age-related differences in the cloacal microbiota of a wild bird species. BMC Ecol. BioMed Central Ltd; 2013;13: 11. doi: 10.1186/1472-6785-13-11 23531085

12. Barbosa A, Balagué V, Valera F, Martínez A, Benzal J, Motas M, et al. Age-Related Differences in the Gastrointestinal Microbiota of Chinstrap Penguins (Pygoscelis antarctica). Peter H-U, editor. PLoS ONE. Public Library of Science; 2016;11: e0153215. doi: 10.1371/journal.pone.0153215 27055030

13. Lucas FS, Heeb P. Environmental factors shape cloacal bacterial assemblages in great tit Parus major and blue tit P. caeruleus nestlings. J Avian Biol. Wiley Online Library; 2005;36: 510–516.

14. Hird SM, Carstens BC, Cardiff SW, Dittmann DL, Brumfield RT. Sampling locality is more detectable than taxonomy or ecology in the gut microbiota of the brood-parasitic Brown-headed Cowbird (Molothrus ater). PeerJ. PeerJ Inc; 2014;2: e321. doi: 10.7717/peerj.321 24711971

15. Moeller AH, Suzuki TA, Lin D, Lacey EA, Wasser SK, Nachman MW. Dispersal limitation promotes the diversification of the mammalian gut microbiota. Proc Natl Acad Sci USA. National Academy of Sciences; 2017;114: 13768–13773. doi: 10.1073/pnas.1700122114 29229828

16. Dudaniec RY, Tesson SVM. Applying landscape genetics to the microbial world. Mol Ecol. Wiley/Blackwell (10.1111); 2016;25: 3266–3275. doi: 10.1111/mec.13691 27146426

17. Grant PR. Ecology and Evolution of Darwin’s Finches. Princeton, NJ: Princeton University Press; 1999.

18. Michel AJ, Ward LM, Goffredi SK, Dawson KS, Baldassarre DT, Brenner A, et al. The gut of the finch: uniqueness of the gut microbiome of the Galápagos vampire finch. Microbiome. BioMed Central; 2018;6: 167. doi: 10.1186/s40168-018-0555-8 30231937

19. Knutie SA, Chaves JA, Gotanda KM. Human activity can influence the gut microbiota of Darwin’s finches in the Galapagos Islands. Mol Ecol. 2019;19: 1565–10. doi: 10.1111/mec.15088 31021499

20. Loo W. T., Loor J. G., Dudaniec R. Y., Kleindorfer S., Cavanaugh C. M. Host phylogeny, diet, and habitat differentiate the gut microbiomes of Darwin’s finches on Santa Cruz Island. Scientific Reports; 2019.

21. Dvorak M, Nemeth E, Wendelin B, Herrera P, Mosquera D, Anchundia D, et al. Conservation status of landbirds on Floreana: the smallest inhabited Galápagos Island. Journal of Field Ornithology. Wiley/Blackwell (10.1111); 2017;88: 132–145. doi: 10.1111/jofo.12197

22. Steadman DW. Holocene Vertebrate Fossils from Isla Floreana, Galápagos. 1986.

23. Curry R. Whatever happened to the Floreana mockingbird? Noticias de Galapagos. 1986;43: 13–15.

24. Grant PR, Grant BR, Petren K, Keller LF. Extinction behind our backs: the possible fate of one of the Darwin’s finch species on Isla Floreana, Galápagos. Biological Conservation. Elsevier; 2005;122: 499–503. doi: 10.1016/j.biocon.2004.09.001

25. Kleindorfer S, O’Connor JA, Dudaniec RY, Myers SA, Robertson J, Sulloway FJ. Species collapse via hybridization in Darwin’s tree finches. Am Nat. 2014;183: 325–341. doi: 10.1086/674899 24561597

26. Fessl B, Tebbich S. Philornis downsi–a recently discovered parasite on the Galápagos archipelago–a threat for Darwin’s finches? Ibis. 2002;144: 445–451.

27. Kleindorfer S, Dudaniec RY. Host-parasite ecology, behavior and genetics: a review of the introduced fly parasite Philornis downsi and its Darwin’s finch hosts. BMC Zoology. BioMed Central; 2016;1: 1. doi: 10.1186/s40850-016-0003-9

28. O’Connor JA, Sulloway FJ, Robertson J, Kleindorfer S. Philornis downsi parasitism is the primary cause of nestling mortality in the critically endangered Darwin’s medium tree finch (Camarhynchus pauper). Biodiversity and Conservation. 2nd ed. Springer Netherlands; 2009;19: 853–866. doi: 10.1007/s10531-009-9740-1

29. Peters KJ, Myers SA, Dudaniec RY, O’Connor JA, Kleindorfer S. Females drive asymmetrical introgression from rare to common species in Darwin’s tree finches. J Evol Biol. 2017;16: 613. doi: 10.1111/jeb.13167 28833876

30. O’Connor JA, Dudaniec RY, Kleindorfer S. Parasite infestation and predation in Darwin’s small ground finch: contrasting two elevational habitats between islands. Journal of Tropical Ecology. Cambridge University Press; 2010;26: 285–292. doi: 10.1017/S0266467409990678

31. O’Connor JA, Robertson J, Kleindorfer S. Video analysis of host–parasite interactions in nests of Darwin’s finches. Oryx. Cambridge University Press; 2010;44: 588–594. doi: 10.1017/S0030605310000086

32. Kleindorfer S, Peters KJ, Custance G, Dudaniec RY. Changes in Philornis infestation behavior threaten Darwin’s finch survival. Curr Zool. 2014;: 1–9. http://www.rufford.org/files/Current%20Zoology%2060%20(4)%20542%E2%80%93550,%202014.pdf

33. O’Connor JA, Robertson J, Kleindorfer S. Darwin’s Finch Begging Intensity Does Not Honestly Signal Need in Parasitised Nests. Herberstein M, editor. Ethology. 2nd ed. Wiley/Blackwell (10.1111); 2014;120: 228–237. doi: 10.1111/eth.12196

34. Christensen R, Kleindorfer S. Assortative pairing and divergent evolution in Darwin’s Small Tree Finch, Camarhynchus parvulus. J Ornithol. 2007.

35. Peters KJ, Kleindorfer S. Avian population trends in Scalesia forest on Floreana Island (2004–2013): Acoustical surveys cannot detect hybrids of Darwin’s tree finches Camarhynchus spp. Bird Conservation International. Cambridge University Press; 2017;38: 1–17. doi: 10.1017/S0959270916000630

36. Kleindorfer S, Custance G, Peters KJ, Sulloway FJ. Introduced parasite changes host phenotype, mating signal and hybridization risk: Philornis downsieffects on Darwin’s finch song. Proc Biol Sci. 2019;286: 20190461–9. doi: 10.1098/rspb.2019.0461 31185871

37. Peters KJ, Kleindorfer S. Divergent foraging behavior in a hybrid zone: Darwin’s tree finches (Camarhynchus spp.) on Floreana Island. Current Zoology. 2015;61: 181–190.

38. Peters KJ, Evans C, Aguirre JD, Kleindorfer S. Genetic admixture predicts parasite intensity: evidence for increased hybrid performance in Darwin’s tree finches. Open Science. 2019;6: 181616–8. doi: 10.1098/rsos.181616 31183118

39. Loo, Wesley T. Host speciation and microbiomes: ecological and evolutionary factors shaping gut microbial communities in Darwin’s finches. 2018. Doctoral dissertation, Harvard University, Graduate School of Arts & Sciences.

40. Lack D. Darwin’s Finches. Cambridge Univ Press; 1947.

41. Kleindorfer S, Chapman TW. Adaptive divergence in contiguous populations of Darwin’s small ground finch (Geospiza fuliginosa). Evol Ecol Res. 2006.

42. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microb. 2013;79: 5112–5120. doi: 10.1128/AEM.01043-13 23793624

43. Vo A-TE, Jedlicka JA. Protocols for metagenomic DNA extraction and Illumina amplicon library preparation for faecal and swab samples. Mol Ecol Resour. 2014;14: 1183–1197. doi: 10.1111/1755-0998.12269 24774752

44. Salter SJ, Cox MJ, Turek EM, Calus ST, Cookson WO, Moffatt MF, et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biology. 2014;12: 118. doi: 10.1186/s12915-014-0087-z 25387460

45. R Core Team. R: A language and environment for statistical computing. Vienna, Austria. URL http://www.R-project.org/. 2014.

46. Callahan BJ, Sankaran K, Fukuyama JA, McMurdie PJ, Holmes SP. Bioconductor Workflow for Microbiome Data Analysis: from raw reads to community analyses. F1000Res. 2016;5: 1492. doi: 10.12688/f1000research.8986.1 27508062

47. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, et al. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. Oxford University Press; 2009;37: D141–D145. doi: 10.1093/nar/gkn879 19004872

48. Davis NM, Proctor D, Holmes SP, Relman D, Callahan BJ. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. bioRxiv. 2017. doi: 10.1101/221499

49. Fox J, Weisberg S. An R Companion to Applied Regression. SAGE; 2011.

50. McMurdie PJ, Holmes S. Waste Not, Want Not: Why Rarefying Microbiome Data Is Inadmissible. McHardy AC, editor. PLoS Comp Biol. Public Library of Science; 2014;10: e1003531. doi: 10.1371/journal.pcbi.1003531 24699258

51. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE. 2013;8: e61217. doi: 10.1371/journal.pone.0061217 23630581

52. Pavoine S, Dufour A-B, Chessel D. From dissimilarities among species to dissimilarities among communities: a double principal coordinate analysis. J Theor Biol. 2004;228: 523–537. doi: 10.1016/j.jtbi.2004.02.014 15178200

53. Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R. UniFrac: an effective distance metric for microbial community comparison. ISME J. 2010;5: 169–172. doi: 10.1038/ismej.2010.133 20827291

54. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. Vegan: Community ecology package. 2017.

55. Balbuena JA, Míguez-Lozano R, Blasco-Costa I. PACo: A Novel Procrustes Application to Cophylogenetic Analysis. Moreau CS, editor. PLoS ONE. Public Library of Science; 2013;8: e61048. doi: 10.1371/journal.pone.0061048 23580325

56. Lamichhaney S, Berglund J, Almén MS, Maqbool K, Grabherr M, Martinez-Barrio A, et al. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature. Nature Publishing Group; 2015;518: 371–375. doi: 10.1038/nature14181 25686609

57. Hutchinson MC, Cagua EF, Balbuena JA, Stouffer DB, Poisot T. paco: implementing Procrustean Approach to Cophylogeny in R. Fitzjohn R, editor. Methods Ecol Evol. 2017;69: 82. doi: 10.1111/2041-210X.12736

58. Legendre P. Studying beta diversity: ecological variation partitioning by multiple regression and canonical analysis. J Plant Ecol. Oxford University Press; 2008;1: 3–8. doi: 10.1093/jpe/rtm001

59. Loo WT, Loor JG, Dudaniec RY, Kleindorfer S, Cavanaugh CM. Host phylogeny, diet, and habitat differentiate the gut microbiomes of Darwin’s finches on Santa Cruz Island. Scientific Reports. 2019.

60. Rakotondranary SJ, Struck U, Knoblauch C, Ganzhorn JU. Regional, seasonal and interspecific variation in 15N and 13C in sympatric mouse lemurs. Naturwissenschaften. Springer-Verlag; 2011;98: 909–917. doi: 10.1007/s00114-011-0840-x 21881908

61. Herrera LG, Hobson KA, Rodríguez M, Hernandez P. Trophic partitioning in tropical rain forest birds: insights from stable isotope analysis. Oecologia. Springer-Verlag; 2003;136: 439–444. doi: 10.1007/s00442-003-1293-5 12802673

62. Caemmerer von S, Ghannoum O, Pengelly JJL, Cousins AB. Carbon isotope discrimination as a tool to explore C4 photosynthesis. Journal of Experimental Botany. 2014;65: 3459–3470. doi: 10.1093/jxb/eru127 24711615

63. Cernusak LA, Ubierna N, Winter K, Holtum JAM, Marshall JD, Farquhar GD. Environmental and physiological determinants of carbon isotope discrimination in terrestrial plants. New Phytologist. Wiley/Blackwell (10.1111); 2013;200: 950–965. doi: 10.1111/nph.12423 23902460

64. Kelly JF. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool. 2000;78: 1–27. doi: 10.1139/z99-165

65. Grant PR, Grant BR. The secondary contact phase of allopatric speciation in Darwin’s finches. Proc Natl Acad Sci USA. 2009;106: 20141–20148. doi: 10.1073/pnas.0911761106 19918081

66. McMullen CK. Flowering Plants of the Galàpagos. Ithaca, NY: Cornell University Press; 1999.

67. Eliasson U. Native climax forests. In: Perry R, editor. Key Environments Galapagos. 1984. pp. 101–114.


Článek vyšel v časopise

PLOS One


2019 Číslo 12
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#