Predictable evolution toward flightlessness in volant island birds

Edited by James A. Estes, University of California, Santa Cruz, CA, and approved March 9, 2016 (received for review November 19, 2015)
April 11, 2016
113 (17) 4765-4770

Significance

Predictable evolutionary trends illuminate mechanisms that affect the diversity of traits and species on the tree of life. We show that when birds colonize islands, they undergo predictable changes in body shape. Small-island bird populations evolve smaller flight muscles and longer legs. These shifts in investment from wings to legs, although often subtle, are qualitatively similar to changes that have occurred in flightless bird lineages. Islands with fewer predator species were associated with more dramatic shifts toward flightlessness, implicating reduced predation pressure as the most likely cause of this trend. These predictable evolutionary changes likely exacerbate the vulnerability of flighted island birds to introduced predators and reduce the potential for small-island species to give rise to subsequent radiations.

Abstract

Birds are prolific colonists of islands, where they readily evolve distinct forms. Identifying predictable, directional patterns of evolutionary change in island birds, however, has proved challenging. The “island rule” predicts that island species evolve toward intermediate sizes, but its general applicability to birds is questionable. However, convergent evolution has clearly occurred in the island bird lineages that have undergone transitions to secondary flightlessness, a process involving drastic reduction of the flight muscles and enlargement of the hindlimbs. Here, we investigated whether volant island bird populations tend to change shape in a way that converges subtly on the flightless form. We found that island bird species have evolved smaller flight muscles than their continental relatives. Furthermore, in 366 populations of Caribbean and Pacific birds, smaller flight muscles and longer legs evolved in response to increasing insularity and, strikingly, the scarcity of avian and mammalian predators. On smaller islands with fewer predators, birds exhibited shifts in investment from forelimbs to hindlimbs that were qualitatively similar to anatomical rearrangements observed in flightless birds. These findings suggest that island bird populations tend to evolve on a trajectory toward flightlessness, even if most remain volant. This pattern was consistent across nine families and four orders that vary in lifestyle, foraging behavior, flight style, and body size. These predictable shifts in avian morphology may reduce the physical capacity for escape via flight and diminish the potential for small-island taxa to diversify via dispersal.

Continue Reading

Data Availability

Data deposition: The data are included in SI Appendix, have been deposited in figshare (https://doi.org/10.6084/m9.figshare.3123148.v1), and are available, along with all code needed to replicate all results and figures, at https://github.com/coereba/islands.

Acknowledgments

J. Dean, C. Milensky, and J. Saucier (Smithsonian National Museum of Natural History); M. Robbins (University of Kansas Biodiversity Institute and Natural History Museum); R. Faucett (Burke Museum of Natural History and Culture); and P. Sweet (American Museum of Natural History) granted access to bird collections. J. Long, B. O. Wolf, J. H. Brown, E. J. Beckman, M. J. Andersen, A. B. Johnson, and three anonymous reviewers provided helpful feedback on this manuscript. A. W. Kratter and J. J. Kirchman collected many of the island specimens with flight muscle data used in this study. We thank C. E. Gunning and J. Long for help with R and statistical advice. The American Ornithologists’ Union, National Science Foundation (NSF) Grants DEB-1146491 (to C.C.W.) and BCS-1118369 (to D.W.S.), and R. W. Dickerman provided funding support. N.A.W. was supported by NIH National Institute of Biomedical Imaging and Bioengineering Award T32EB009414 and a Drollinger-Dial postdoctoral fellowship.

Supporting Information

Appendix (PDF)
Supporting Information
pnas.1522931113.sd01.xlsx
pnas.1522931113.sd02.xlsx

References

1
C Darwin On the Origin of Species (Murray, London, 1859).
2
AR Wallace Island Life (Macmillan, London, 1881).
3
PR Grant, BR Grant, Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296, 707–711 (2002).
4
SM Clegg, IP Owens, The ‘island rule’ in birds: Medium body size and its ecological explanation. Proc Biol Sci 269, 1359–1365 (2002).
5
PR Grant, The adaptive significance of some size trends in island birds. Evolution 19, 355–367 (1965).
6
AG Boyer, W Jetz, Biogeography of body size in Pacific island birds. Ecography 33, 369–379 (2010).
7
MV Lomolino, Body size evolution in insular vertebrates: Generality of the island rule. J Biogeogr 32, 1683–1699 (2005).
8
CR McClain, PA Durst, AG Boyer, CD Francis, Unravelling the determinants of insular body size shifts. Biol Lett 9, 20120989 (2013).
9
S Meiri, N Cooper, A Purvis, The island rule: Made to be broken? Proc Biol Sci 275, 141–148 (2008).
10
S Meiri, T Dayan, D Simberloff, The generality of the island rule reexamined. J Biogeogr 33, 1571–1577 (2006).
11
S Meiri, P Raia, AB Phillimore, Slaying dragons: Limited evidence for unusual body size evolution on islands. J Biogeogr 38, 89–100 (2011).
12
B Leisler, H Winkler, Evolution of island warblers: Beyond bills and masses. J Avian Biol 46, 236–244 (2015).
13
JJ Kirchman, Genetic tests of rapid parallel speciation of flightless birds from an extant volant ancestor. Biol J Linn Soc Lond 96, 601–616 (2009).
14
B Slikas, SL Olson, RC Fleisher, Rapid, independent evolution of flightlessness in four species of Pacific Island rails (Rallidae): An analysis based on mitochondrial sequence data. J Avian Biol 33, 5–14 (2002).
15
BC Livezey, Evolution of flightlessness in rails (Gruiformes: Rallidae): phylogenetic, ecomorphological, and ontogenetic perspectives. Ornithol Monogr 53, 1–654 (2003).
16
DW Steadman Extinction and Biogeography of Tropical Pacific Birds (Univ of Chicago Press, Chicago, 2006).
17
DW Steadman, JR Morris, NA Wright, A new species of Late Pleistocene rail (Aves: Rallidae) from Abaco, the Bahamas. Paleontol J 47, 1355–1364 (2013).
18
SL Olson, Evolution of the rails of the South Atlantic islands (Aves: Rallidae). Smithson Contrib Zool 152, 1–53 (1973).
19
BK McNab, Energy conservation and the evolution of flightlessness in birds. Am Nat 144, 628–642 (1994).
20
BK McNab, Minimizing energy expenditure facilitates vertebrate persistence on oceanic islands. Ecol Lett 5, 693–704 (2002).
21
RH MacArthur, EO Wilson The Theory of Island Biogeography (Princeton Univ Press, Princeton, NJ, 1967).
22
RH MacArthur Geographical Ecology: Patterns in the Distribution of Species (Princeton Univ Press, Princeton, NJ, 1972).
23
NA Wright, DW Steadman, Insular avian adaptations on two Neotropical continental islands. J Biogeogr 39, 1891–1899 (2012).
24
NA Wright, TR Gregory, CC Witt, Metabolic 'engines' of flight drive genome size reduction in birds. Proc Roy Soc B 281, 20132780 (2014).
25
AM Heers, KP Dial, Wings versus legs in the avian bauplan: Development and evolution of alternative locomotor strategies. Evolution 69, 305–320 (2015).
26
J Franklin, DW Steadman, Prehistoric species richness of birds on oceanic islands. Oikos 117, 1885–1891 (2008).
27
H Raffaele, J Wiley, O Garrido, A Keith, J Raffaele A Guide to the Birds of the West Indies (Princeton Univ Press, Princeton, NJ, 1998).
28
KD Earls, Kinematics and mechanics of ground take-off in the starling Sturnis vulgaris and the quail Coturnix coturnix. J Exp Biol 203, 725–739 (2000).
29
BW Tobalske, DL Altshuler, DR Powers, Take-off mechanics in hummingbirds (Trochilidae). J Exp Biol 207, 1345–1352 (2004).
30
BW Tobalske, TL Hedrick, KP Dial, AA Biewener, Comparative power curves in bird flight. Nature 421, 363–366 (2003).
31
P Feinsinger, LA Swarm, “Ecological release,” seasonal variation in food supply, and the hummingbird Amazilia tobaci on Trinidad and Tobago. Ecology 63, 1574–1587 (1982).
32
T Keeler-Wolf, The Barred Antshrike (Thamnophilus doliatus) on Trinidad and Tobago: Habitat niche expansion of a generalist forager. Oecologia 70, 309–317 (1986).
33
RA McCall, S Nee, PH Harvey, The role of wing length in the evolution of avian flightlessness. Evol Ecol 12, 569–580 (1998).
34
JM Diamond, Flightlessness and fear of flying in island species. Nature 293, 507–508 (1981).
35
Jr WE Cooper, RA Pyron, Jr T Garland, Island tameness: Living on islands reduces flight initiation distance. Proc Roy Soc B 281, 20133019 (2014).
36
D Lack Darwin’s Finches (Cambridge Univ Press, Cambridge, UK, 1983).
37
TM Blackburn, P Cassey, RP Duncan, KL Evans, KJ Gaston, Avian extinction and mammalian introductions on oceanic islands. Science 305, 1955–1958 (2004).
38
RE Ricklefs, E Bermingham, The concept of the taxon cycle in biogeography. Glob Ecol Biogeogr 11, 353–361 (2002).
39
R ffrench A Guide to the Birds of Trinidad and Tobago (Cornell Univ Press, Ithaca, NY, 1991).
40
JE duPont South Pacific Birds (Delaware Mus Nat Hist, Greenville, DE, 1976).
41
RS Kennedy, PC Gonzales, EC Dickinson, H Miranda, TH Fisher A Guide to the Birds of the Philippines (Oxford Univ Press, New York, 2000).
42
D Lepage, AviBase—bird checklists of the world. Available at avibase.bsc-eoc.org/avibase.jsp?lang=EN. Accessed June 11, 2014. (2014).
43
; R Core Team R: A Language and Environment for Statistical Computing (R Found Stat Comput, Vienna, 2012).
44
E Paradis, J Claude, K Strimmer, ape: Analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).
45
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Development Core Team (2012) nlme: Linear and nonlineaer mixed effects models. R package version 3.1-104.
46
W Jetz, GH Thomas, JB Joy, K Hartmann, AO Mooers, The global diversity of birds in space and time. Nature 491, 444–448 (2012).
47
SJ Hackett, et al., A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763–1768 (2008).
48
E Bellemain, E Bermingham, RE Ricklefs, The dynamic evolutionary history of the bananaquit (Coereba flaveola) in the Caribbean revealed by a multigene analysis. BMC Evol Biol 8, 240 (2008).
49
MJ Andersen, CH Oliveros, CE Filardi, RG Moyle, Phylogeography of the Variable Dwarf-Kingfisher Ceyx lepidus (Aves: Alcedinidae) inferred from mitochondrial and nuclear DNA sequences. Auk 130, 118–131 (2013).
50
MJ Andersen, Diversification of the tropical Pacific avifauna. Ph.D thesis (University of Kansas, Lawrence, KS). (2013).
51
MJ Andersen, et al., Molecular systematics of the world’s most polytypic bird: The Pachycephala pectoralis/melanura(Aves: Pachycephalidae) species complex. Zool J Linn Soc 170, 566–588 (2014).
52
PA Hosner, LA Sánchez-González, AT Peterson, RG Moyle, Climate-driven diversification and Pleistocene refugia in Philippine birds: Evidence from phylogeographic structure and paleoenvironmental niche modeling. Evolution 68, 2658–2674 (2014).
53
LA Sánchez-González, RG Moyle, Molecular systematics and species limits in the Philippine fantails (Aves: Rhipidura). Mol Phylogenet Evol 61, 290–299 (2011).
54
MJ Andersen, et al., Rapid diversification and secondary sympatry in Australo-Pacific kingfishers (Aves: Alcedinidae: Todiramphus). R Soc Open Sci 2, 140375–140375 (2015).
55
TW Arnold, Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manage 74, 1175–1178 (2010).

Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 113 | No. 17
April 26, 2016
PubMed: 27071105

Classifications

Data Availability

Data deposition: The data are included in SI Appendix, have been deposited in figshare (https://doi.org/10.6084/m9.figshare.3123148.v1), and are available, along with all code needed to replicate all results and figures, at https://github.com/coereba/islands.

Submission history

Published online: April 11, 2016
Published in issue: April 26, 2016

Keywords

  1. birds
  2. islands
  3. morphology
  4. flight
  5. island rule

Acknowledgments

J. Dean, C. Milensky, and J. Saucier (Smithsonian National Museum of Natural History); M. Robbins (University of Kansas Biodiversity Institute and Natural History Museum); R. Faucett (Burke Museum of Natural History and Culture); and P. Sweet (American Museum of Natural History) granted access to bird collections. J. Long, B. O. Wolf, J. H. Brown, E. J. Beckman, M. J. Andersen, A. B. Johnson, and three anonymous reviewers provided helpful feedback on this manuscript. A. W. Kratter and J. J. Kirchman collected many of the island specimens with flight muscle data used in this study. We thank C. E. Gunning and J. Long for help with R and statistical advice. The American Ornithologists’ Union, National Science Foundation (NSF) Grants DEB-1146491 (to C.C.W.) and BCS-1118369 (to D.W.S.), and R. W. Dickerman provided funding support. N.A.W. was supported by NIH National Institute of Biomedical Imaging and Bioengineering Award T32EB009414 and a Drollinger-Dial postdoctoral fellowship.

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Natalie A. Wright1 [email protected]
Department of Biology and Museum of Southwestern Biology, University of New Mexico, Albuquerque, NM 87131-0001;
Division of Biological Sciences, University of Montana, Missoula, MT 59812;
David W. Steadman
Florida Museum of Natural History, University of Florida, Gainesville, FL 32611-7800
Christopher C. Witt
Department of Biology and Museum of Southwestern Biology, University of New Mexico, Albuquerque, NM 87131-0001;

Notes

1
To whom correspondence should be addressed. Email: [email protected].
Author contributions: N.A.W., D.W.S., and C.C.W. designed research; N.A.W. and D.W.S. performed research; N.A.W. analyzed data; and N.A.W., D.W.S., and C.C.W. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

Metrics & Citations

Metrics

Note: The article usage is presented with a three- to four-day delay and will update daily once available. Due to ths delay, usage data will not appear immediately following publication. Citation information is sourced from Crossref Cited-by service.


Citation statements

Altmetrics

Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

Cited by

    Loading...

    View Options

    View options

    PDF format

    Download this article as a PDF file

    DOWNLOAD PDF

    Get Access

    Login options

    Check if you have access through your login credentials or your institution to get full access on this article.

    Personal login Institutional Login

    Recommend to a librarian

    Recommend PNAS to a Librarian

    Purchase options

    Purchase this article to get full access to it.

    Single Article Purchase

    Predictable evolution toward flightlessness in volant island birds
    Proceedings of the National Academy of Sciences
    • Vol. 113
    • No. 17
    • pp. 4543-E2471

    Media

    Figures

    Tables

    Other

    Share

    Share

    Share article link

    Share on social media