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 sanguínea) and iiwi (Vestiaria coccínea), 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 alíele distributions. We found that amakihi in lowland areas are, and have historically been, differentiated from birds at high elevations and had unique alíeles 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 armually. 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.

Avian malaria in Hawaiian forest birds: infection and population impacts across species and elevations

“…These spatial differences in parasite-mediated selection pressure coupled with spatial host genetic structure and gene flow can significantly influence host adaptation or maintaining genetic diversity (Poulin 2007, Wolinska andKing 2009). In Hawaii, the spatial gradient in selection pressure has apparently produced two opposing outcomes-local adaptation of low-elevation Amakihi for malaria-tolerance (Woodworth et al 2005, Foster et al 2007, Atkinson et al 2013 or local extinction of highly susceptible species like Iiwi from low and mid-elevation forests (van Riper et al 1986). As climate warms and malaria infection risk increases in Hawai'i (Benning et al 2002, Atkinson and LaPointe 2009b, Atkinson et al 2014 it is uncertain whether other endemic v www.esajournals.org honeycreepers will be able to evolve tolerance to malaria.…”

Stepping stone speciation in Hawaii’s flycatchers: molecular divergence supports new island endemics within the elepaio

“…Mitochondrial loci have been the most useful molecular markers for examining phylogenetic relationships, in part because of their shorter coalescence times, but it is often desirable to corroborate mtDNA results using nuclear loci (Zink and Barrowclough 2008). LDH was useful in distinguishing population level variation in Hawaii amakihi (Foster et al 2007), but was not useful for this purpose in elepaio because divergence among elepaio occurred too recently.…”

“…We chose the mtDNA gene NADH dehydrogenase subunit 2 (ND2) because it was useful in elucidating phylogeny of other Pacific island monarchs (Filardi and Moyle 2005;Filardi and Smith 2005). We chose the nuclear gene lactate dehydrogenase (LDH) because it was useful in distinguishing population-level variation in Hawaii amakihi (Hemignathus virens; Foster et al 2007). …”

Evidence that disease-induced population decline changes genetic structure and alters dispersal patterns in the Tasmanian devil

“…The former is predicted to occur first, because rare alleles that contribute little to heterozygosity are more easily lost during population size reductions (Nei et al, 1975;Cornuet and Luikart, 1996). The few empirical studies investigating the genetic consequences of disease-induced bottlenecks reveal that although some populations do lose genetic diversity following disease impacts (Trudeau et al, 2004;Foster et al, 2007), others do not (Queney et al, 2000;Teacher et al, 2009); this result has also been found for populations that have undergone bottlenecks not associated with disease (Carson, 1990;Flagstad et al, 2003;Hailer et al, 2006). Indeed, the impact of a population size reduction on genetic diversity depends on the intensity of the perturbation, the length of time before recovery and the rate of recovery to original population numbers (England et al, 2003).…”