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Evolutionary Ecology

, Volume 32, Issue 5, pp 443–452 | Cite as

Beak of the pinch: anti-parasite traits are similar among Darwin’s finch species

  • Scott M. VillaEmail author
  • Jennifer A. H. Koop
  • Céline Le Bohec
  • Dale H. Clayton
Article

Abstract

Darwin’s finches are an iconic example of adaptive radiation. The size and shape of the beaks of different finch species are diversified for feeding on different size seeds and other food resources. However, beaks also serve other functions, such as preening for the control of ectoparasites. In diverse groups of birds, the effectiveness of preening is governed by the length of the overhanging tip of the upper mandible of the beak. This overhang functions as a template against which the tip of the lower mandible generates a pinching force sufficient to damage or kill ectoparasites. Here we compare feeding versus preening components of the beak morphology of small, medium, and large ground finches that share a single parasite community. Despite adaptive divergence in beak morphology related to feeding, the three species have nearly identical relative mandibular overhang lengths. Moreover, birds with intermediate length overhangs have the lowest feather mite loads. These results suggest that Darwin’s finches maintain an optimal beak morphology to effectively control their ectoparasites.

Keywords

Preening Feather mites Geospiza Principal component analysis Overhang 

Notes

Acknowledgements

We thank S. Bush, D. Feener, E. Diblasi, J. Ruff, S. McNew, T. White, and the two anonymous reviewers for comments that greatly strengthened the manuscript. We also thank J. Podos and K. Gotanda for use of their photographs. All procedures were approved by University of Utah Institutional Animal Care and Use Committee (protocol #07-08004) and with permission from the Galapagos National Park (PC-04-10: #0054411). This work was funded by the National Science Foundation DEB-0816877 to DHC and Sigma Xi Grants-in-aid of Research to JAHK.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10682_2018_9949_MOESM1_ESM.docx (44 kb)
Supplementary material 1 (DOCX 43 kb)

References

  1. Barlow JC (1967) A bill deformity in a European tree sparrow, Passer montanus (Linnaeus). Can J Zool 456:889–890CrossRefGoogle Scholar
  2. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  3. Blanco G, Tella JL, Potti J (1997) Feather mites on group-living red-billed choughs: a non-parasitic interaction? J Avian Biol 28:197–206CrossRefGoogle Scholar
  4. Booth DT, Clayton DH, Block BA (1993) Experimental demonstration of the energetic cost of parasitism, in free-ranging hosts. Proc R Soc Lond B 253:125–129CrossRefGoogle Scholar
  5. Bronstein JL (1994) Conditional outcomes in mutualistic interactions. Trends Ecol Evol 9:214–217CrossRefPubMedGoogle Scholar
  6. Bulgarella M, Palma RL (2017) Coextinction dilemma in the Galapagos Islands: Can Darwin’s finches and their native ectoparasites survive the control of the introduced fly Philornis downsi? Insect Conserv Div.  https://doi.org/10.1111/icad.12219 CrossRefGoogle Scholar
  7. Bush SE, Clayton DH (2018) Anti-parasite behaviour of birds. Philos Trans R Soc B.  https://doi.org/10.1098/rstb.2017.0196 CrossRefGoogle Scholar
  8. Bush AO, Lafferty KD, Lotz JM, Shostak AM et al (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583CrossRefGoogle Scholar
  9. Clayton DH (1990) Mate choice in experimentally parasitized rock doves: Lousy males lose. Am Zool 30:251–262CrossRefGoogle Scholar
  10. Clayton DH (1991) Coevolution of avian grooming and ectoparasite avoidance. In: Loye JE, Zuk M (eds) Bird-parasite interactions: ecology, evolution, and behaviour. Oxford University Press, Oxford, pp 258–289Google Scholar
  11. Clayton DH, Walther BA (2001) Influence of host ecology and morphology on the diversity of Neotropical bird lice. Oikos 94:455–467CrossRefGoogle Scholar
  12. Clayton DH, Lee PLM, Tompkins DM, Brodie ED III (1999) Reciprocal natural selection on host-parasite phenotypes. Am Nat 154:261–270PubMedGoogle Scholar
  13. Clayton DH, Moyer BR, Bush SE, Jones TG, Gardiner DW, Rhodes BB, Goller F (2005) Adaptive significance of avian beak morphology for ectoparasite control. Proc R Soc Lond B 272:811–817CrossRefGoogle Scholar
  14. Clayton DH, Adams RJ, Bush SE (2008) Phthiraptera, the Chewing Lice. In: Atkinson CT, Thomas NJ, Hunter DB (eds) Parasitic diseases of wild birds. Wiley, Ames, pp 515–526Google Scholar
  15. Clayton DH, Bush SE, Johnson KP (2016) Coevolution of life on hosts: integrating ecology and history. University of Chicago Press, ChicagoGoogle Scholar
  16. Cooney CR, Bright JA, Capp EJR, Chira AM, Hughes EC, Moody CJA, Nouri LO, Varley ZK, Thomas GH (2017) Mega-evolutionary dynamics of the adaptive radiation of birds. Nature 542:344–347CrossRefPubMedPubMedCentralGoogle Scholar
  17. Doña J, Proctor H, Serrano D, Johnson KP, Oploo AO, Huguet-Tapia JC, Ascunce MS, Jovani R (2018) Feather mites play a role in cleaning host feathers: new insights from DNA metabarcoding and microscopy. Mol Ecol.  https://doi.org/10.1111/mec.14581 CrossRefPubMedGoogle Scholar
  18. Freed LA, Cann C, Bodner GR (2008) Explosive increase in ectoparasites in Hawaiian forest birds. J Parasitol 94:1009–1021CrossRefPubMedGoogle Scholar
  19. Galván I, Aguilera E, Atiénzar F, Barba E, Blanco G, Cantó JL, Cortés V, Frías Ó, Kovács I, Meléndez L, Møller AP, Monrós JS, Pap PL, Piculo R, Senar JC, Serrano D, Tella JL, Vágási CI, Vögeli M, Jovani R (2012) Feather mites (Acari: Astigmata) and body condition of their avian hosts: a large correlative study. J Avian Biol 43:001–007CrossRefGoogle Scholar
  20. Grant PR (1986) Ecology and evolution of Darwin’s finches. Princeton University Press, PrincetonGoogle Scholar
  21. Grant PR, Grant BR (2014) 40 years of evolution: Darwin’s finches on Daphne Major Island. Princeton University Press, PrincetonGoogle Scholar
  22. Grant PR, Abbott I, Schluter D, Curry RL, Abbott LK (1985) Variation in the size and shape of Darwin’s finches. Biol J Linn Soc 25:1–39CrossRefGoogle Scholar
  23. Handel CM, Pajot LM, Matsuoka SM, Hemert CV, Terenzi J, Talbot SL, Mulcahy DM, Meteyer CU, Trust KA (2010) Epizootic of beak deformities among wild birds in Alaska: an emerging disease in North America? Auk 127:882–898CrossRefGoogle Scholar
  24. Harper DGC (1999) Feather mites, pectoral muscle condition, wing length and plumage coloration of passerines. Anim Behav 58:553–562CrossRefPubMedGoogle Scholar
  25. Hoi H, Kristofik J, Darolova A, Hoi C (2012) Experimental evidence for costs due to chewing lice in the Europefan bee-eater (Merops apiaster). Parasitology 139:53–59CrossRefPubMedGoogle Scholar
  26. Jovani R, Doña J, MdelM Labrador, Serrano D (2017) Opening the doors of parasitology journals to other symbionts. Trends Parasitol 33:578–579CrossRefPubMedGoogle Scholar
  27. Kuznetsova A, Brockhoff PB, Haubo R, Christensen B (2016) lmerTest Package: tests in linear mixed effects models. R package version 2.0–30, https://CRAN.Rproject.org/package=lmerTest
  28. Matthews AE, Larking JL, Raybuck DW, Slevin MC, Stoleson SH, Boves TJ (2017) Feather mite abundance varies by symbiotic nature of mite-host relationship does not differ between two ecologically dissimilar warblers. Ecol Evol.  https://doi.org/10.1002/ece3.3738 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Matthysen E (1989) Seasonal variation in bill morphology of nuthatches Sitta europaea: dietary adaptations or consequences? ARDEA 77:117–125Google Scholar
  30. Moyer BR, Peterson AT, Clayton DH (2002a) Influence of bill shape on ectoparasite load in Western scrub-jays. Condor 104:675–678CrossRefGoogle Scholar
  31. Moyer BR, Drown DM, Clayton DH (2002b) Low humidity reduces ectoparasite pressure: implications for host life history evolution. Oikos 97:223–228CrossRefGoogle Scholar
  32. Olsen AM (2017) Feeding ecology is the primary driver of beak shape diversification in waterfowl. Funct Ecol.  https://doi.org/10.1111/1365-2435.12890 CrossRefGoogle Scholar
  33. Palma RL, Peck SB (2013) An annotated checklist of parasitic lice (Insecta: Phthiraptera) from the Galapagos Islands. Zootaxa 3627:001–087CrossRefGoogle Scholar
  34. Palma RL, Price RD (2010) The species of Myrsidea Waterston (Insecta: Phthiraptera: Menoponidae) from the Galapagos Islands, with descriptions of new taxa. Tuhinga 21:135–146Google Scholar
  35. Poulin R (2007) Evolutionary ecology of parasites, 2nd edn. Princeton University Press, PrincetonGoogle Scholar
  36. Proctor H, Owens I (2010) Mites and birds: diversity, parasitism and coevolution. Trends Ecol Evol 15:358–364CrossRefGoogle Scholar
  37. R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org
  38. Thompson CW, Hillgarth N, Leu M, McClure HE (1997) High parasite load in house finches (Carpodacus mexicanus) is correlated with reduced expression of a sexually selected trait. Am Nat 149:270–294CrossRefGoogle Scholar
  39. Van Hemert C, Handel CM, O’Hara TM (2012) Evidence of accelerated beak growth associated with avian keratin disorder in black-capped chickadees (Poecile atricapillus). J Wildl Dis 48:686–694CrossRefPubMedGoogle Scholar
  40. Villa SM, Le Bohec C, Koop JAH, Proctor HC, Clayton DH (2013) Diversity of feather mites (Acari: Astigmata) on Darwin’s finches. J Parasitol 99:756–762CrossRefPubMedPubMedCentralGoogle Scholar
  41. Weiner J (1994) The beak of the finch. Cambridge University Press, CambridgeGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Scott M. Villa
    • 1
    Email author
  • Jennifer A. H. Koop
    • 1
    • 2
  • Céline Le Bohec
    • 1
    • 3
    • 4
  • Dale H. Clayton
    • 1
  1. 1.Department of BiologyUniversity of UtahSalt Lake CityUSA
  2. 2.Department of BiologyUniversity of Massachusetts-DartmouthDartmouthUSA
  3. 3.CNRS, IPHC UMR 7178Université de StrasbourgStrasbourgFrance
  4. 4.Département de Biologie PolaireCentre Scientifique de MonacoMonacoPrincipality of Monaco

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