UM BIOL 561 - Effects of precipitation and soil water potential on drought deciduous phenology in the Kalahari

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Molecular Ecology (2007) 16, 4738–4746 doi: 10.1111/j.1365-294X.2007.03550.x© 2007 The AuthorsJournal compilation © 2007 Blackwell Publishing LtdBlackwell Publishing LtdGenetic structure and evolved malaria resistance in Hawaiian honeycreepersJEFFREY T. FOSTER,*† BETHANY L. WOODWORTH,‡ LORI E. EGGERT,*§ PATRICK J. HART,¶** DANIELLE PALMER,* DAVID C. DUFFY†† and ROBERT C. FLEISCHER**Genetics Program, National Museum of Natural History and National Zoological Park, Smithsonian Institution, 3001 Connecticut Ave NW, Washington, DC 20008, USA ‡Pacific Island Ecosystems Research Center, US Geological Survey, Kilauea Field Station, PO Box 44, Hawaii National Park, HI 96718, USA, ¶Pacific Cooperative Studies Unit, US Geological Survey, Kilauea Field Station, PO Box 44, Hawaii National Park, HI 96718, USA, ††Pacific Cooperative Studies Unit, Department of Botany, University of Hawaii at Manoa, 3190 Maile Way, Honolulu, HI 96822, USAAbstractInfectious diseases now threaten wildlife populations worldwide but population recoveryfollowing local extinction has rarely been observed. In such a case, do resistant individualsrecolonize from a central remnant population, or do they spread from small, perhaps over-looked, 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 about1000 m tolerates malaria and has initiated a remarkable and rapid recovery. We assessed mito-chondrial and nuclear DNA markers from amakihi and two other Hawaiian honeycreepers,apapane (Himatione sanguinea) and iiwi (Vestiaria coccinea), at nine primary study sites from2001 to 2003 to determine the source of re-establishing birds. In addition, we obtained sequencesfrom tissue from amakihi museum study skins (1898 and 1948–49) to assess temporal changesin 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; thatis, their genetic signature was not a subset of the genetic variation at higher elevations. Wesuggest 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 scatteredremnant populations. Low-elevation amakihi are currently isolated from higher elevations(> 1000 m) where disease emergence and transmission rates appear to vary seasonally andannually. In contrast to results from amakihi, no genetic differentiation between elevationswas found in apapane and iiwi, indicating that slight variation in genetic or life-historyattributes can determine disease resistance and population recovery. Determining the condi-tions that allow for the development of resistance to disease is essential to understandinghow species evolve resistance across a landscape of varying disease pressures.Keywords: Avian malaria, introduced disease, Plasmodium relictum, population structureReceived 27 May 2007; revision accepted 15 August 2007IntroductionAlthough pathogens have afflicted wildlife for millennia,anthropogenic change and the global introductions of specieshave dramatically altered the frequency, distribution andimpact of disease (Daszak et al. 2000; Dobson & Foufopoulos2001). Infectious diseases threaten the extinction of wildlifepopulations worldwide (e.g. LaDeau et al. 2007), but rarelyhave we had a chance to observe population recoveryCorrespondence: Jeffrey Foster, Fax: +1 928 523 0639; E-mail:[email protected]†Present address: Center for Microbial Genetics and Genomics,Northern Arizona University, PO Box 5640, Flagstaff, AZ 86011, USA.§Present address: Department of Biology, University of Missouri,Columbia, MO 65211, USA.**Present address: Department of Biology, University of Hawaii,Hilo, HI 96720, USA.MALARIA EFFECTS ON HAWAIIAN BIRD POPULATIONS 4739© 2007 The AuthorsJournal compilation © 2007 Blackwell Publishing Ltd(Cleaveland et al. 2002). Determining population-leveleffects of pathogens on genetic structure is essential forunderstanding disease impacts on host abundance anddistribution (Sorci et al. 1997; Uller et al. 2003). Why do somepopulations persist while others go extinct? Furthermore,to determine the genesis of disease resistance in wildlifewe must understand how disease impacts populationsacross the landscape (Real et al. 2005). Where are the sourcesof resistant individuals and how do they repopulate whendisease has decimated local populations?Avian blood parasites (Haemosporidia) infect birdpopulations globally (Beadell et al. 2006) but long-termpopulation effects have rarely been documented. In contrast,avian malaria (Plasmodium relictum) appears to have beena major factor in the extinction and decline of nativeHawaiian birds over at least the past 60 years, particularlyat low elevations (below ca. 1200 m) (Warner 1968; vanRiper et al. 1986). Endemic forest birds of the HawaiianIslands, particularly honeycreepers (Drepanidinae), arebroadly susceptible to malarial infection, with drepanidmortality rates of 65–90% depending upon species vanRiper et al. 1986; Atkinson et al. 1995, 2001b; Yorinks &Atkinson 2000). Birds that do not immediately die sustainlow-level chronic infections that can decrease long-termsurvival (Kilpatrick 2006), and these resistant birds serve asa reservoir to infect mosquitoes and continue the diseasecycle (Atkinson et al. 2001a; Jarvi et al. 2001, 2002). Wedefine malaria resistance as the ability of birds to contractand survive the disease, although some individuals maynever completely clear the parasite from their systems. Asa result of disease, populations of native forest birds areprimarily restricted to mid and high elevations, wheremalaria is rare due to physiological (thermal) constraintson the primary vector (Culex quinquefasciatus) and themalaria parasite (van Riper et al. 1986; LaPointe 2000).Malaria is, in fact, the second wave of disease in Hawaiianbirds; avian pox (Poxvirus avium) arrived in the late 1800sand appears to have devastated native bird populations(van Riper et al. 2002). The relationship between malariaand pox remains unclear, but pox may have been the firstselective disease pressure on lowland native birds.Despite the prevalence of malaria and mosquitoes inlow-elevation habitats, small


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