Genetic structure and evolved malaria resistance in Hawaiian honeycreepers

Jeffrey T Foster, Bethany L. Woodworth, Lori E. Eggert, Patrick J. Hart, Danielle Palmer, David C. Duffy, Robert C. Fleischer

Research output: Contribution to journalArticle

53 Citations (Scopus)

Abstract

Infectious diseases now threaten wildlife populations worldwide but population recovery following local extinction has rarely been observed. In such a case, do resistant individuals recolonize from a central remnant population, or do they spread from small, perhaps overlooked, populations of resistant individuals? Introduced avian malaria (Plasmodium relictum) has devastated low-elevation populations of native birds in Hawaii, but at least one species (Hawaii amakihi, Hemignathus virens) that was greatly reduced at elevations below about 1000 m tolerates malaria and has initiated a remarkable and rapid recovery. We assessed mitochondrial and nuclear DNA markers from amakihi and two other Hawaiian honeycreepers, apapane (Himatione sanguinea) and iiwi (Vestiaria coccinea), at nine primary study sites from 2001 to 2003 to determine the source of re-establishing birds. In addition, we obtained sequences from tissue from amakihi museum study skins (1898 and 1948-49) to assess temporal changes in allele distributions. We found that amakihi in lowland areas are, and have historically been, differentiated from birds at high elevations and had unique alleles retained through time; that is, their genetic signature was not a subset of the genetic variation at higher elevations. We suggest that high disease pressure rapidly selected for resistance to malaria at low elevation, leaving small pockets of resistant birds, and this resistance spread outward from the scattered remnant populations. Low-elevation amakihi are currently isolated from higher elevations (> 1000 m) where disease emergence and transmission rates appear to vary seasonally and annually. In contrast to results from amakihi, no genetic differentiation between elevations was found in apapane and iiwi, indicating that slight variation in genetic or life-history attributes can determine disease resistance and population recovery. Determining the conditions that allow for the development of resistance to disease is essential to understanding how species evolve resistance across a landscape of varying disease pressures.

Original languageEnglish (US)
Pages (from-to)4738-4746
Number of pages9
JournalMolecular Ecology
Volume16
Issue number22
DOIs
StatePublished - Nov 2007

Fingerprint

Genetic Structures
malaria
genetic structure
Malaria
Birds
Population
Disease Resistance
bird
birds
Recovery
Hawaii
genetic variation
Avian Malaria
Alleles
allele
avian malaria
alleles
Pressure
Museums
Plasmodium

Keywords

  • Avian malaria
  • Introduced disease
  • Plasmodium relictum
  • Population structure

ASJC Scopus subject areas

  • Ecology
  • Biochemistry, Genetics and Molecular Biology(all)
  • Biochemistry

Cite this

Foster, J. T., Woodworth, B. L., Eggert, L. E., Hart, P. J., Palmer, D., Duffy, D. C., & Fleischer, R. C. (2007). Genetic structure and evolved malaria resistance in Hawaiian honeycreepers. Molecular Ecology, 16(22), 4738-4746. https://doi.org/10.1111/j.1365-294X.2007.03550.x

Genetic structure and evolved malaria resistance in Hawaiian honeycreepers. / Foster, Jeffrey T; Woodworth, Bethany L.; Eggert, Lori E.; Hart, Patrick J.; Palmer, Danielle; Duffy, David C.; Fleischer, Robert C.

In: Molecular Ecology, Vol. 16, No. 22, 11.2007, p. 4738-4746.

Research output: Contribution to journalArticle

Foster, JT, Woodworth, BL, Eggert, LE, Hart, PJ, Palmer, D, Duffy, DC & Fleischer, RC 2007, 'Genetic structure and evolved malaria resistance in Hawaiian honeycreepers', Molecular Ecology, vol. 16, no. 22, pp. 4738-4746. https://doi.org/10.1111/j.1365-294X.2007.03550.x
Foster, Jeffrey T ; Woodworth, Bethany L. ; Eggert, Lori E. ; Hart, Patrick J. ; Palmer, Danielle ; Duffy, David C. ; Fleischer, Robert C. / Genetic structure and evolved malaria resistance in Hawaiian honeycreepers. In: Molecular Ecology. 2007 ; Vol. 16, No. 22. pp. 4738-4746.
@article{68e84db72992485eb0a79d647846e45a,
title = "Genetic structure and evolved malaria resistance in Hawaiian honeycreepers",
abstract = "Infectious diseases now threaten wildlife populations worldwide but population recovery following local extinction has rarely been observed. In such a case, do resistant individuals recolonize from a central remnant population, or do they spread from small, perhaps overlooked, populations of resistant individuals? Introduced avian malaria (Plasmodium relictum) has devastated low-elevation populations of native birds in Hawaii, but at least one species (Hawaii amakihi, Hemignathus virens) that was greatly reduced at elevations below about 1000 m tolerates malaria and has initiated a remarkable and rapid recovery. We assessed mitochondrial and nuclear DNA markers from amakihi and two other Hawaiian honeycreepers, apapane (Himatione sanguinea) and iiwi (Vestiaria coccinea), at nine primary study sites from 2001 to 2003 to determine the source of re-establishing birds. In addition, we obtained sequences from tissue from amakihi museum study skins (1898 and 1948-49) to assess temporal changes in allele distributions. We found that amakihi in lowland areas are, and have historically been, differentiated from birds at high elevations and had unique alleles retained through time; that is, their genetic signature was not a subset of the genetic variation at higher elevations. We suggest that high disease pressure rapidly selected for resistance to malaria at low elevation, leaving small pockets of resistant birds, and this resistance spread outward from the scattered remnant populations. Low-elevation amakihi are currently isolated from higher elevations (> 1000 m) where disease emergence and transmission rates appear to vary seasonally and annually. In contrast to results from amakihi, no genetic differentiation between elevations was found in apapane and iiwi, indicating that slight variation in genetic or life-history attributes can determine disease resistance and population recovery. Determining the conditions that allow for the development of resistance to disease is essential to understanding how species evolve resistance across a landscape of varying disease pressures.",
keywords = "Avian malaria, Introduced disease, Plasmodium relictum, Population structure",
author = "Foster, {Jeffrey T} and Woodworth, {Bethany L.} and Eggert, {Lori E.} and Hart, {Patrick J.} and Danielle Palmer and Duffy, {David C.} and Fleischer, {Robert C.}",
year = "2007",
month = "11",
doi = "10.1111/j.1365-294X.2007.03550.x",
language = "English (US)",
volume = "16",
pages = "4738--4746",
journal = "Molecular Ecology",
issn = "0962-1083",
publisher = "Wiley-Blackwell",
number = "22",

}

TY - JOUR

T1 - Genetic structure and evolved malaria resistance in Hawaiian honeycreepers

AU - Foster, Jeffrey T

AU - Woodworth, Bethany L.

AU - Eggert, Lori E.

AU - Hart, Patrick J.

AU - Palmer, Danielle

AU - Duffy, David C.

AU - Fleischer, Robert C.

PY - 2007/11

Y1 - 2007/11

N2 - Infectious diseases now threaten wildlife populations worldwide but population recovery following local extinction has rarely been observed. In such a case, do resistant individuals recolonize from a central remnant population, or do they spread from small, perhaps overlooked, populations of resistant individuals? Introduced avian malaria (Plasmodium relictum) has devastated low-elevation populations of native birds in Hawaii, but at least one species (Hawaii amakihi, Hemignathus virens) that was greatly reduced at elevations below about 1000 m tolerates malaria and has initiated a remarkable and rapid recovery. We assessed mitochondrial and nuclear DNA markers from amakihi and two other Hawaiian honeycreepers, apapane (Himatione sanguinea) and iiwi (Vestiaria coccinea), at nine primary study sites from 2001 to 2003 to determine the source of re-establishing birds. In addition, we obtained sequences from tissue from amakihi museum study skins (1898 and 1948-49) to assess temporal changes in allele distributions. We found that amakihi in lowland areas are, and have historically been, differentiated from birds at high elevations and had unique alleles retained through time; that is, their genetic signature was not a subset of the genetic variation at higher elevations. We suggest that high disease pressure rapidly selected for resistance to malaria at low elevation, leaving small pockets of resistant birds, and this resistance spread outward from the scattered remnant populations. Low-elevation amakihi are currently isolated from higher elevations (> 1000 m) where disease emergence and transmission rates appear to vary seasonally and annually. In contrast to results from amakihi, no genetic differentiation between elevations was found in apapane and iiwi, indicating that slight variation in genetic or life-history attributes can determine disease resistance and population recovery. Determining the conditions that allow for the development of resistance to disease is essential to understanding how species evolve resistance across a landscape of varying disease pressures.

AB - Infectious diseases now threaten wildlife populations worldwide but population recovery following local extinction has rarely been observed. In such a case, do resistant individuals recolonize from a central remnant population, or do they spread from small, perhaps overlooked, populations of resistant individuals? Introduced avian malaria (Plasmodium relictum) has devastated low-elevation populations of native birds in Hawaii, but at least one species (Hawaii amakihi, Hemignathus virens) that was greatly reduced at elevations below about 1000 m tolerates malaria and has initiated a remarkable and rapid recovery. We assessed mitochondrial and nuclear DNA markers from amakihi and two other Hawaiian honeycreepers, apapane (Himatione sanguinea) and iiwi (Vestiaria coccinea), at nine primary study sites from 2001 to 2003 to determine the source of re-establishing birds. In addition, we obtained sequences from tissue from amakihi museum study skins (1898 and 1948-49) to assess temporal changes in allele distributions. We found that amakihi in lowland areas are, and have historically been, differentiated from birds at high elevations and had unique alleles retained through time; that is, their genetic signature was not a subset of the genetic variation at higher elevations. We suggest that high disease pressure rapidly selected for resistance to malaria at low elevation, leaving small pockets of resistant birds, and this resistance spread outward from the scattered remnant populations. Low-elevation amakihi are currently isolated from higher elevations (> 1000 m) where disease emergence and transmission rates appear to vary seasonally and annually. In contrast to results from amakihi, no genetic differentiation between elevations was found in apapane and iiwi, indicating that slight variation in genetic or life-history attributes can determine disease resistance and population recovery. Determining the conditions that allow for the development of resistance to disease is essential to understanding how species evolve resistance across a landscape of varying disease pressures.

KW - Avian malaria

KW - Introduced disease

KW - Plasmodium relictum

KW - Population structure

UR - http://www.scopus.com/inward/record.url?scp=36249009517&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=36249009517&partnerID=8YFLogxK

U2 - 10.1111/j.1365-294X.2007.03550.x

DO - 10.1111/j.1365-294X.2007.03550.x

M3 - Article

VL - 16

SP - 4738

EP - 4746

JO - Molecular Ecology

JF - Molecular Ecology

SN - 0962-1083

IS - 22

ER -