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

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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.

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References

  • Barlow JC (1967) A bill deformity in a European tree sparrow, Passer montanus (Linnaeus). Can J Zool 456:889–890

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Blanco G, Tella JL, Potti J (1997) Feather mites on group-living red-billed choughs: a non-parasitic interaction? J Avian Biol 28:197–206

    Article  Google Scholar 

  • Booth DT, Clayton DH, Block BA (1993) Experimental demonstration of the energetic cost of parasitism, in free-ranging hosts. Proc R Soc Lond B 253:125–129

    Article  Google Scholar 

  • Bronstein JL (1994) Conditional outcomes in mutualistic interactions. Trends Ecol Evol 9:214–217

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bush SE, Clayton DH (2018) Anti-parasite behaviour of birds. Philos Trans R Soc B. https://doi.org/10.1098/rstb.2017.0196

    Article  Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM, Shostak AM et al (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583

    Article  CAS  Google Scholar 

  • Clayton DH (1990) Mate choice in experimentally parasitized rock doves: Lousy males lose. Am Zool 30:251–262

    Article  Google Scholar 

  • 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 258–289

    Google Scholar 

  • Clayton DH, Walther BA (2001) Influence of host ecology and morphology on the diversity of Neotropical bird lice. Oikos 94:455–467

    Article  Google Scholar 

  • Clayton DH, Lee PLM, Tompkins DM, Brodie ED III (1999) Reciprocal natural selection on host-parasite phenotypes. Am Nat 154:261–270

    PubMed  Google Scholar 

  • 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 272:811–817

    Article  Google Scholar 

  • 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 515–526

    Google Scholar 

  • Clayton DH, Bush SE, Johnson KP (2016) Coevolution of life on hosts: integrating ecology and history. University of Chicago Press, Chicago

    Google Scholar 

  • 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 542:344–347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Freed LA, Cann C, Bodner GR (2008) Explosive increase in ectoparasites in Hawaiian forest birds. J Parasitol 94:1009–1021

    Article  PubMed  Google Scholar 

  • 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 43:001–007

    Article  Google Scholar 

  • Grant PR (1986) Ecology and evolution of Darwin’s finches. Princeton University Press, Princeton

    Google Scholar 

  • Grant PR, Grant BR (2014) 40 years of evolution: Darwin’s finches on Daphne Major Island. Princeton University Press, Princeton

    Google Scholar 

  • 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 25:1–39

    Article  Google Scholar 

  • 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 127:882–898

    Article  Google Scholar 

  • Harper DGC (1999) Feather mites, pectoral muscle condition, wing length and plumage coloration of passerines. Anim Behav 58:553–562

    Article  CAS  PubMed  Google Scholar 

  • 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 139:53–59

    Article  CAS  PubMed  Google Scholar 

  • Jovani R, Doña J, MdelM Labrador, Serrano D (2017) Opening the doors of parasitology journals to other symbionts. Trends Parasitol 33:578–579

    Article  PubMed  Google Scholar 

  • 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

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Matthysen E (1989) Seasonal variation in bill morphology of nuthatches Sitta europaea: dietary adaptations or consequences? ARDEA 77:117–125

    Google Scholar 

  • Moyer BR, Peterson AT, Clayton DH (2002a) Influence of bill shape on ectoparasite load in Western scrub-jays. Condor 104:675–678

    Article  Google Scholar 

  • Moyer BR, Drown DM, Clayton DH (2002b) Low humidity reduces ectoparasite pressure: implications for host life history evolution. Oikos 97:223–228

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Palma RL, Peck SB (2013) An annotated checklist of parasitic lice (Insecta: Phthiraptera) from the Galapagos Islands. Zootaxa 3627:001–087

    Article  Google Scholar 

  • Palma RL, Price RD (2010) The species of Myrsidea Waterston (Insecta: Phthiraptera: Menoponidae) from the Galapagos Islands, with descriptions of new taxa. Tuhinga 21:135–146

    Google Scholar 

  • Poulin R (2007) Evolutionary ecology of parasites, 2nd edn. Princeton University Press, Princeton

    Google Scholar 

  • Proctor H, Owens I (2010) Mites and birds: diversity, parasitism and coevolution. Trends Ecol Evol 15:358–364

    Article  Google Scholar 

  • R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org

  • 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 149:270–294

    Article  Google Scholar 

  • 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 48:686–694

    Article  PubMed  Google Scholar 

  • Villa SM, Le Bohec C, Koop JAH, Proctor HC, Clayton DH (2013) Diversity of feather mites (Acari: Astigmata) on Darwin’s finches. J Parasitol 99:756–762

    Article  PubMed  PubMed Central  Google Scholar 

  • Weiner J (1994) The beak of the finch. Cambridge University Press, Cambridge

    Google Scholar 

Download references

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.

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Correspondence to Scott M. Villa.

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Villa, S.M., Koop, J.A.H., Le Bohec, C. et al. Beak of the pinch: anti-parasite traits are similar among Darwin’s finch species. Evol Ecol 32, 443–452 (2018). https://doi.org/10.1007/s10682-018-9949-0

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