Research ArticleEVOLUTIONARY ECOLOGY

Glaciation as a migratory switch

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Science Advances  20 Sep 2017:
Vol. 3, no. 9, e1603133
DOI: 10.1126/sciadv.1603133
  • Fig. 1 Plot of midpoint of current range versus midpoint of estimated LGM range derived from niche modeling (LDM-LDM represents species that was an LDM at both periods).

    All points are at or below the dashed line, which represents the expectation if ranges at the two time periods were the same and shows that although most species’ ranges were shifted south at the LGM, it was not to a consistent degree. Many long-distance migratory species have LGM ranges centered well south of the current range.

  • Fig. 2 Examples of predicted breeding (red) and wintering (blue) distributions at the LGM for the hermit thrush (Catharus guttatus) and veery (Catharus fuscescens).

    The hermit thrush apparently maintained migratory status at the LGM (A and B), whereas too little predicted breeding area is present for the veery (C) to have maintained breeding populations in North America, and it is inferred that this species became a tropical sedentary resident during this glacial maximum. See fig. S17 for the regions thought to consist of unsuitable habitat at the LGM.

  • Fig. 3 Example of a species for which too little predicted distribution existed at the LGM to allow breeding in (and migration to and from) North America, but for which predicted winter distribution was substantial, suggesting that the species adopted a sedentary tropical range during the glacial advance.

    Breeding distribution estimated by ecological niche modeling for mourning warbler (Geothlypis philadelphia) at the LGM (A), showing two small predicted areas (arrows) considered unlikely to be a sufficient area for breeding throughout a glacial period (and habitat in Beringia was not suitable), and wintering distributions at the LGM (B) and the present (C), showing an expanded winter range at the LGM.

  • Fig. 4 Mapping migratory behavior on a phylogenetic tree to infer evolutionary transitions between migratory states.

    Reconstructed history (13) of sedentary (white), SDM (gray), and LDM (black) assuming the present (A) or the LGM migratory state (B) using stochastic character mapping. Stars indicate positions along the branches where niche modeling suggested a switch in state at the LGM but was not reconstructed by the model. The two hypotheses suggest different frequencies of transitions among states, showing that reconstruction of migratory behavior must account for the potential of transitions occurring on a temporal scale of glacial cycles and not speciation events.

  • Fig. 5 Phylogenetic hypothesis of warbler relationships [from the study of Winger et al. (13)] showing reconstructed ancestral areas based on distributions at the LGM (left) and the present (right).

    Colors indicate different areas, and stars mark inferred vicariant events. Key to areas: A (North America), B (northern North America), C (western North America), D (eastern North America), E (southern North America), F (Central America), G (South America), H (Sonoran Desert), I (central Texas), and J (Caribbean).

  • Table 1 Summary of changes in migration status between the condition at the present and that at the LGM.

    See appendix S2.

    Present
    LGMLDMSDMNot migratory
    LDM300
    SDM4170
    Not migratory2075

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/3/9/e1603133/DC1

    appendix S1. Maps showing predicted distribution of breeding and wintering season climatic niches at the LGM.

    fig. S1A. Broad-winged hawk (Buteo platypterus) predicted breeding distribution at the LGM.

    fig. S1B. Broad-winged hawk predicted wintering distribution at the LGM.

    fig. S2A. Swainson’s hawk (Buteo swainsoni) predicted breeding distribution at the LGM.

    fig. S2B. Swainson’s hawk predicted wintering distribution at the LGM.

    fig. S3A. Rough-legged hawk (Buteo lagopus) predicted breeding distribution at the LGM.

    fig. S3B. Rough-legged hawk predicted wintering distribution at the LGM.

    fig. S4A. Swainson’s thrush (Catharus ustulatus) predicted breeding distribution at the LGM.

    fig. S4B. Swainson’s thrush predicted wintering distribution at the LGM.

    fig. S5A. Macgillivray’s warbler (Geothlypis tolmiei) predicted breeding distribution at the LGM

    fig. S5B. Macgillivray’s warbler predicted wintering distribution at the LGM.

    fig. S6A. Yellow warbler (S. petechia) predicted breeding distribution at the LGM.

    fig. S6B. Yellow warbler predicted wintering distribution at the LGM.

    fig. S7A. Black-throated blue warbler (S. caerulescens) predicted breeding distribution at the LGM.

    fig. S7B. Black-throated blue warbler predicted wintering distribution at the LGM.

    fig. S8A. Bullock’s oriole (Icterus bullockii) predicted breeding distribution at the LGM.

    fig. S8B. Bullock’s oriole predicted wintering distribution at the LGM.

    fig. S9A. Orange-crowned warbler (Vermivora celata) predicted breeding distribution at the LGM.

    fig. S9B. Orange-crowned warbler predicted wintering distribution at the LGM.

    fig. S10A. Colima warbler (Oreothlypis crissalis) predicted breeding distribution at the LGM.

    fig. S10B. Colima warbler predicted wintering distribution at the LGM.

    fig. S11A. Virginia warbler (Leiothlypis virginiae) predicted breeding distribution at the LGM.

    fig. S11B. Virginia warbler predicted wintering distribution at the LGM.

    fig. S12A. Nashville warbler (Leiothlypis ruficapilla) predicted breeding distribution at the LGM.

    fig. S12B. Nashville warbler predicted wintering distribution at the LGM.

    fig. S13A. Audubon’s warbler (S. auduboni) predicted breeding distribution at the LGM.

    fig. S13B. Audubon’s warbler predicted wintering distribution at the LGM.

    fig. S14A. Myrtle warbler (S. coronata) predicted breeding distribution at the LGM.

    fig. S14B. Myrtle warbler predicted wintering distribution at the LGM.

    fig. S15A. Lincoln’s sparrow (Melospiza lincolnii) predicted breeding distribution at the LGM.

    fig. S15B. Lincoln’s sparrow predicted wintering distribution at the LGM.

    fig. S16. Gray-cheeked thrush (Catharus bicknelli/minimus) predicted wintering distribution at the LGM.

    fig. S17. Veery (Catharus fuscescens) predicted wintering distribution at the LGM.

    fig. S18A. Wood thrush (Hylocichla mustelina) predicted breeding distribution at the LGM.

    fig. S18B. Wood thrush predicted wintering distribution at the LGM.

    fig. S19A. Orchard oriole (Icturus spurius) predicted breeding distribution at the LGM.

    fig. S19B. Orchard oriole predicted wintering distribution at the LGM.

    fig. S20A. Baltimore oriole (Icterus galbula) predicted breeding distribution (arrow) at the LGM.

    fig. S20B. Baltimore oriole predicted wintering distribution at the LGM.

    fig. S21A. Blue-winged warbler (Vermivora cyanoptera) predicted breeding distribution (arrows) at the LGM.

    fig. S21B. Blue-winged warbler predicted wintering distribution at the LGM.

    fig. S22. Golden-winged warbler (Vermivora chrysoptera) predicted wintering distribution at the LGM.

    fig. S23A. Tennessee warbler (Oreothlypis peregrina) predicted breeding distribution at the LGM.

    fig. S23B. Tennessee warbler predicted wintering distribution at the LGM.

    fig. S24. Connecticut warbler (Oporonis agilis) predicted wintering distribution at the LGM.

    fig. S25. Mourning warbler (Geothlypis philadelphia) predicted wintering distribution at the LGM.

    fig. S26. Kentucky warbler (Geothlypis formosa) predicted wintering distribution at the LGM.

    fig. S27A. Blackpoll warbler (S. striata) predicted breeding distribution at the LGM.

    fig. S27B. Blackpoll warbler predicted wintering distribution at the LGM.

    fig. S28. Magnolia warbler (S. magnolia) predicted wintering distribution at the LGM.

    fig. S29. Cape May warbler (S. tigrina) predicted wintering distribution at the LGM.

    fig. S30. Bay-breasted warbler (S. castanea) predicted wintering distribution at the LGM.

    fig. S31. Blackburnian warbler (S. fusca) predicted wintering distribution at the LGM.

    fig. S32. Chestnut-sided warbler (S. pensylvanica) predicted wintering distribution at the LGM.

    fig. S33A. Palm warbler (S. palmarum) predicted breeding distribution at the LGM.

    fig. S33B. Palm warbler predicted wintering distribution at the LGM.

    fig. S34. Black-throated green warbler (S. virens) predicted wintering distribution at the LGM.

    fig. S35. Canada warbler (Cardellina canadensis) predicted wintering distribution at the LGM.

    fig. S36A. Wilson’s warbler (Cardellina pusilla) predicted breeding distribution at the LGM.

    fig. S36B. Wilson’s warbler predicted wintering distribution at the LGM.

    fig. S37A. Hermit thrush (Catharus guttatus) predicted breeding distribution at the LGM.

    fig. S37B. Hermit thrush predicted wintering distribution at the LGM.

    fig. S38A. Hooded oriole (Icterus cucullatus nelsoni) predicted breeding distribution at the LGM.

    fig. S38B. Hooded oriole predicted wintering distribution at the LGM.

    fig. S39A. Abeile’s oriole (Icturus abellei) predicted breeding distribution at the LGM.

    fig. S39B. Abeile’s oriole predicted wintering distribution at the LGM.

    fig. S40A. Lucy’s warbler (Oreothlypis luciae) predicted breeding distribution at the LGM.

    fig. S40B. Lucy’s warbler predicted wintering distribution at the LGM.

    fig. S41A. Yellow-throated warbler (S. dominica) predicted breeding distribution at the LGM.

    fig. S41B. Yellow-throated warbler (S. dominica) predicted wintering distribution at the LGM.

    fig. S42A. Pine warbler (S. pinus) predicted breeding distribution at the LGM.

    fig. S42B. Pine warbler predicted wintering distribution at the LGM.

    fig. S43A. Black-throated gray warbler (S. nigrescens) predicted breeding distribution at the LGM.

    fig. S43B. Black-throated gray warbler predicted wintering distribution at the LGM.

    fig. S44A. Hermit warbler (S. occidentalis) predicted breeding distribution at the LGM.

    fig. S44B. Hermit warbler predicted wintering distribution at the LGM.

    fig. S45A. Townsend’s warbler (S. townsendi) predicted breeding distribution at the LGM.

    fig. S45B. Townsend’s warbler predicted wintering distribution at the LGM.

    fig. S46A. Grace’s warbler (S. graciae) predicted breeding distribution at LGM.

    fig. S46B. Grace’s warbler predicted wintering distribution at the LGM.

    fig. S47A. Common yellowthroat (Geothylpis trichas) predicted breeding distribution at the LGM.

    fig. S47B. Common yellowthroat predicted wintering distribution at the LGM.

    fig. S48. Golden-cheeked warbler (S. chrysoparia) predicted wintering distribution at the LGM.

    fig. S49. Prairie warbler (S. discolor) predicted wintering distribution at the LGM.

    fig. S50A. Swamp sparrow (Melospiza georgiana) predicted breeding distribution at the LGM.

    fig. S50B. Swamp sparrow predicted wintering distribution at the LGM.

    fig. S51. Song sparrow (Melospiza melodia; eastern migratory populations only) predicted wintering distribution at the LGM.

    appendix S2. Species studied, migratory status at present and LGM, samples sizes, latitudinal midpoint of ranges at present and LGM, and climate layers important in distribution models.

  • Supplementary Materials

    This PDF file includes:

    • appendix S1. Maps showing predicted distribution of breeding and wintering season climatic niches at the LGM.
    • fig. S1A. Broad-winged hawk (Buteo platypterus) predicted breeding distribution at the LGM.
    • fig. S1B. Broad-winged hawk predicted wintering distribution at the LGM.
    • fig. S2A. Swainson’s hawk (Buteo swainsoni) predicted breeding distribution at the LGM.
    • fig. S2B. Swainson’s hawk predicted wintering distribution at the LGM.
    • fig. S3A. Rough-legged hawk (Buteo lagopus) predicted breeding distribution at the LGM.
    • fig. S3B. Rough-legged hawk predicted wintering distribution at the LGM.
    • fig. S4A. Swainson’s thrush (Catharus ustulatus) predicted breeding distribution at the LGM.
    • fig. S4B. Swainson’s thrush predicted wintering distribution at the LGM.
    • fig. S5A. Macgillivray’s warbler (Geothlypis tolmiei) predicted breeding distribution at the LGM.
    • fig. S5B. Macgillivray’s warbler predicted wintering distribution at the LGM.
    • fig. S6A. Yellow warbler (S. petechia) predicted breeding distribution at the LGM.
    • fig. S6B. Yellow warbler predicted wintering distribution at the LGM.
    • fig. S7A. Black-throated blue warbler (S. caerulescens) predicted breeding distribution at the LGM.
    • fig. S7B. Black-throated blue warbler predicted wintering distribution at the LGM.
    • fig. S8A. Bullock’s oriole (Icterus bullockii) predicted breeding distribution at the LGM.
    • fig. S8B. Bullock’s oriole predicted wintering distribution at the LGM.
    • fig. S9A. Orange-crowned warbler (Vermivora celata) predicted breeding distribution at the LGM.
    • fig. S9B. Orange-crowned warbler predicted wintering distribution at the LGM.
    • fig. S10A. Colima warbler (Oreothlypis crissalis) predicted breeding distribution at the LGM.
    • fig. S10B. Colima warbler predicted wintering distribution at the LGM.
    • fig. S11A. Virginia warbler (Leiothlypis virginiae) predicted breeding distribution at the LGM.
    • fig. S11B. Virginia warbler predicted wintering distribution at the LGM.
    • fig. S12A. Nashville warbler (Leiothlypis ruficapilla) predicted breeding distribution at the LGM.
    • fig. S12B. Nashville warbler predicted wintering distribution at the LGM.
    • fig. S13A. Audubon’s warbler (S. auduboni) predicted breeding distribution at the LGM.
    • fig. S13B. Audubon’s warbler predicted wintering distribution at the LGM.
    • fig. S14A. Myrtle warbler (S. coronata) predicted breeding distribution at the LGM.
    • fig. S14B. Myrtle warbler predicted wintering distribution at the LGM.
    • fig. S15A. Lincoln’s sparrow (Melospiza lincolnii) predicted breeding distribution at the LGM.
    • fig. S15B. Lincoln’s sparrow predicted wintering distribution at the LGM.
    • fig. S16. Gray-cheeked thrush (Catharus bicknelli/minimus) predicted wintering distribution at the LGM.
    • fig. S17. Veery (Catharus fuscescens) predicted wintering distribution at the LGM.
    • fig. S18A. Wood thrush (Hylocichla mustelina) predicted breeding distribution at the LGM.
    • fig. S18B. Wood thrush predicted wintering distribution at the LGM.
    • fig. S19A. Orchard oriole (Icturus spurius) predicted breeding distribution at the LGM.
    • fig. S19B. Orchard oriole predicted wintering distribution at the LGM.
    • fig. S20A. Baltimore oriole (Icterus galbula) predicted breeding distribution (arrow) at the LGM.
    • fig. S20B. Baltimore oriole predicted wintering distribution at the LGM.
    • fig. S21A. Blue-winged warbler (Vermivora cyanoptera) predicted breeding distribution (arrows) at the LGM.
    • fig. S21B. Blue-winged warbler predicted wintering distribution at the LGM.
    • fig. S22. Golden-winged warbler (Vermivora chrysoptera) predicted wintering distribution at the LGM.
    • fig. S23A. Tennessee warbler (Oreothlypis peregrina) predicted breeding distribution at the LGM.
    • fig. S23B. Tennessee warbler predicted wintering distribution at the LGM.
    • fig. S24. Connecticut warbler (Oporonis agilis) predicted wintering distribution at the LGM.
    • fig. S25. Mourning warbler (Geothlypis philadelphia) predicted wintering distribution at the LGM.
    • fig. S26. Kentucky warbler (Geothlypis formosa) predicted wintering distribution at the LGM.
    • fig. S27A. Blackpoll warbler (S. striata) predicted breeding distribution at the LGM.
    • fig. S27B. Blackpoll warbler predicted wintering distribution at the LGM.
    • fig. S28. Magnolia warbler (S. magnolia) predicted wintering distribution at the LGM.
    • fig. S29. Cape May warbler (S. tigrina) predicted wintering distribution at the LGM.
    • fig. S30. Bay-breasted warbler (S. castanea) predicted wintering distribution at the LGM.
    • fig. S31. Blackburnian warbler (S. fusca) predicted wintering distribution at the LGM.
    • fig. S32. Chestnut-sided warbler (S. pensylvanica) predicted wintering distribution at the LGM.
    • fig. S33A. Palm warbler (S. palmarum) predicted breeding distribution at the LGM.
    • fig. S33B. Palm warbler predicted wintering distribution at the LGM.
    • fig. S34. Black-throated green warbler (S. virens) predicted wintering distribution at the LGM.
    • fig. S35. Canada warbler (Cardellina canadensis) predicted wintering distribution at the LGM.
    • fig. S36A. Wilson’s warbler (Cardellina pusilla) predicted breeding distribution at the LGM.
    • fig. S36B. Wilson’s warbler predicted wintering distribution at the LGM.
    • fig. S37A. Hermit thrush (Catharus guttatus) predicted breeding distribution at the LGM.
    • fig. S37B. Hermit thrush predicted wintering distribution at the LGM.
    • fig. S38A. Hooded oriole (Icterus cucullatus nelsoni) predicted breeding distribution at the LGM.
    • fig. S38B. Hooded oriole predicted wintering distribution at the LGM.
    • fig. S39A. Abeile’s oriole (Icturus abellei) predicted breeding distribution at the LGM.
    • fig. S39B. Abeile’s oriole predicted wintering distribution at the LGM.
    • fig. S40A. Lucy’s warbler (Oreothlypis luciae) predicted breeding distribution at the LGM.
    • fig. S40B. Lucy’s warbler predicted wintering distribution at the LGM.
    • fig. S41A. Yellow-throated warbler (S. dominica) predicted breeding distribution at the LGM.
    • fig. S41B. Yellow-throated warbler (S. dominica) predicted wintering distribution at the LGM.
    • fig. S42A. Pine warbler (S. pinus) predicted breeding distribution at the LGM.
    • fig. S42B. Pine warbler predicted wintering distribution at the LGM.
    • fig. S43A. Black-throated gray warbler (S. nigrescens) predicted breeding distribution at the LGM.
    • fig. S43B. Black-throated gray warbler predicted wintering distribution at the LGM.
    • fig. S44A. Hermit warbler (S. occidentalis) predicted breeding distribution at the LGM.
    • fig. S44B. Hermit warbler predicted wintering distribution at the LGM.
    • fig. S45A. Townsend’s warbler (S. townsendi) predicted breeding distribution at the LGM.
    • fig. S45B. Townsend’s warbler predicted wintering distribution at the LGM.
    • fig. S46A. Grace’s warbler (S. graciae) predicted breeding distribution at LGM.
    • fig. S46B. Grace’s warbler predicted wintering distribution at the LGM.
    • fig. S47A. Common yellowthroat (Geothylpis trichas) predicted breeding distribution at the LGM.
    • fig. S47B. Common yellowthroat predicted wintering distribution at the LGM.
    • fig. S48. Golden-cheeked warbler (S. chrysoparia) predicted wintering distribution at the LGM.
    • fig. S49. Prairie warbler (S. discolor) predicted wintering distribution at the LGM.
    • fig. S50A. Swamp sparrow (Melospiza georgiana) predicted breeding distribution at the LGM.
    • fig. S50B. Swamp sparrow predicted wintering distribution at the LGM.
    • fig. S51. Song sparrow (Melospiza melodia; eastern migratory populations only) predicted wintering distribution at the LGM.

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    Other Supplementary Material for this manuscript includes the following:

    • appendix S2 (Microsoft Excel format). Species studied, migratory status at present and LGM, samples sizes, latitudinal midpoint of ranges at present and LGM, and climate layers important in distribution models.

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