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Genetic and genomic data are increasingly used to aid conservation management of endangered species by providing insights into evolutionary histories, factors associated with extinction risks, and potential for future adaptation. For the ‘Alalā, or Hawaiian crow (Corvus hawaiiensis), genetic concerns include negative correlations between inbreeding and hatching success. However, it is unclear if low genetic diversity and inbreeding depression are consequences of a historical population bottleneck, or if ‘Alalā had historically low genetic diversity that predated human influence, perhaps as a result of earlier declines or founding events. In this study, we applied a hybridization-based sequence capture to generate a genome-wide single nucleotide polymorphism (SNP) dataset for comparing historical specimens collected in the 1890s, when ‘Alalā were more numerous, to samples taken between 1973 and 1998, when ‘Alalā population densities were near the lowest documented levels in the wild, prior to all individuals being collected for captive rearing. We found low genome-wide diversity in both sample groups, however, the modern sample group (1973 to 1998 cohort) exhibited relatively fewer polymorphic alleles, a lower proportion of polymorphic loci, and lower observed heterozygosity, consistent with a population decline and potential bottleneck effects. These results combined with a current low population size highlight the importance of continued efforts by conservation managers to mitigate inbreeding and maintain founder representation to preserve what genetic diversity remains.

 

The unprecedented rise in the number of new and emerging infectious diseases in the last quarter century poses direct threats to human and wildlife health. The introduction to the Hawaiian archipelago of Plasmodium relictum and the mosquito vector that transmits the parasite has led to dramatic losses in endemic Hawaiian forest bird species. Understanding how mechanisms of disease immunity to avian malaria may evolve is critical as climate change facilitates increased disease transmission to high elevation habitats where malaria transmission has historically been low and the majority of the remaining extant Hawaiian forest bird species now reside. Here, we compare the transcriptomic profiles of highly susceptible Hawai‘i ‘amakihi (Chlorodrepanis virens) experimentally infected with P. relictum to those of uninfected control birds from a naïve high elevation population. We examined changes in gene expression profiles at different stages of infection to provide an in-depth characterization of the molecular pathways contributing to survival or mortality in these birds. We show that the timing and magnitude of the innate and adaptive immune response differed substantially between individuals that survived and those that succumbed to infection, and likely contributed to the observed variation in survival. These results lay the foundation for developing gene-based conservation strategies for Hawaiian honeycreepers by identifying candidate genes and cellular pathways involved in the pathogen response that correlate with a bird’s ability to recover from malaria infection.

 

Connectivity among wildlife populations facilitates exchange of genetic material between groups. Changes to historical connectivity patterns resulting from anthropogenic activities can therefore have negative consequences for genetic diversity, particularly for small or isolated populations. DNA obtained from museum specimens can enable direct comparison of temporal changes in connectivity among populations, which can aid in conservation planning and contribute to the understanding of population declines. However, museum DNA can be degraded and only available in low quantities, rendering it challenging for use in population genomic analyses. Applications of genomic methodologies such as targeted sequencing address this issue by enabling capture of shared variable sites, increasing quantity and quality of recovered genomic information. We used targeted sequencing of ultra-conserved Elements (UCEs) to evaluate potential changes in connectivity and genetic diversity of roseate terns (Sterna dougallii) with a breeding distribution in the northwestern Atlantic and the Caribbean. Both populations experienced range contractions and population declines due to anthropogenic activity in the 20th century, which has the potential to alter historical connectivity regimes. Instead, we found that the two populations were differentiated historically as well as contemporaneously, with little evidence of migration between them for either time period. We also found no evidence for temporal changes in genetic diversity, although these interpretations may have been limited due to sequencing artifacts caused by the degraded nature of the museum samples. Population structuring in migratory seabirds is typically reflective of low rates of divergence and high connectivity among geographically segregated subpopulations. Our contrasting results suggest the potential presence of ecological mechanisms driving population differentiation, and highlight the value of targeted sequencing on DNA derived from museum specimens to uncover long-term patterns of genetic differentiation in wildlife populations.

 

Plasmodiumparasites that cause bird malaria occur in all continents except Antarctica and are primarily transmitted by mosquitoes in the genusCulex.Culex quinquefasciatus, the mosquito vector of avian malaria in Hawaiʻi, became established in the islands in the 1820s. While the deadly effects of malaria on endemic bird species have been documented for many decades, vector-parasite interactions in avian malaria systems are relatively understudied.

To evaluate the gene expression response of mosquitoes exposed to aPlasmodiuminfection intensity known to occur naturally in Hawaiʻi, offspring of wild-collected HawaiianCx. quinquefasciatuswere fed on a domestic canary infected with a fresh isolate ofPlasmodium relictumGRW4 from a wild-caught Hawaiian honeycreeper. Control mosquitoes were fed on an uninfected canary. Transcriptomes of five infected and three uninfected individual mosquitoes were sequenced at each of three stages of the parasite life cycle: 24 h post feeding (hpf) during ookinete invasion; 5 days post feeding (dpf) when oocysts are developing; 10 dpf when sporozoites are released and invade the salivary glands.

Differential gene expression analyses showed that during ookinete invasion (24 hpf), genes related to oxidoreductase activity and galactose catabolism had lower expression levels in infected mosquitoes compared to controls. Oocyst development (5 dpf) was associated with reduced expression of a gene with a predicted innate immune function. At 10 dpf, infected mosquitoes had reduced expression levels of a serine protease inhibitor, and further studies should assess its role as aPlasmodiumagonist inC. quinquefasciatus. Overall, the differential gene expression response of HawaiianCulexexposed to aPlasmodiuminfection intensity known to occur naturally in Hawaiʻi was low, but more pronounced during ookinete invasion.

This is the first analysis of the transcriptional responses of vectors to malaria parasites in non-mammalian systems. Interestingly, few similarities were found between the response ofCulexinfected with a birdPlasmodiumand those reported inAnophelesinfected with humanPlasmodium. The relatively small transcriptional changes observed in mosquito genes related to immune response and nutrient metabolism support conclusions of low fitness costs often documented in experimental challenges ofCulexwith avianPlasmodium.

 

Abstract The Hawai‘ian honeycreepers (drepanids) are a classic example of adaptive radiation: they adapted to a variety of novel dietary niches, evolving a wide range of bill morphologies. Here we investigated genomic diversity, demographic history, and genes involved in bill morphology phenotypes in 2 honeycreepers: the ‘akiapōlā‘au (Hemignathus wilsoni) and the Hawai‘i ‘amakihi (Chlorodrepanis virens). The ‘akiapōlā‘au is an endangered island endemic, filling the “woodpecker” niche by using a unique bill morphology, while the Hawai‘i ‘amakihi is a dietary generalist common on the islands of Hawai‘i and Maui. We de novo sequenced the ‘akiapōlā‘au genome and compared it to the previously sequenced ‘amakihi genome. The ‘akiapōlā‘au is far less heterozygous and has a smaller effective population size than the ‘amakihi, which matches expectations due to its smaller census population and restricted ecological niche. Our investigation revealed genomic islands of divergence, which may be involved in the honeycreeper radiation. Within these islands of divergence, we identified candidate genes (including DLK1, FOXB1, KIF6, MAML3, PHF20, RBP1, and TIMM17A) that may play a role in honeycreeper adaptations. The gene DLK1, previously shown to influence Darwin’s finch bill size, may be related to honeycreeper bill morphology evolution, while the functions of the other candidates remain unknown. 

Of the estimated 55 Hawaiian honeycreepers (subfamily Carduelinae) only 17 species remain, nine of which the International Union for Conservation of Nature considers endangered. Among the most pressing threats to honeycreeper survival is avian malaria, caused by the introduced blood parasitePlasmodium relictum, which is increasing in distribution in Hawaiʻi as a result of climate change. Preventing further honeycreeper decline will require innovative conservation strategies that confront malaria from multiple angles. Research on mammals has revealed strong connections between gut microbiome composition and malaria susceptibility, illuminating a potential novel approach to malaria control through the manipulation of gut microbiota. One honeycreeper species, Hawaiʻi ʻamakihi (Chlorodrepanis virens), persists in areas of high malaria prevalence, indicating they have acquired some level of immunity. To investigate if avian host‐specific microbes may be associated with malaria survival, we characterized cloacal microbiomes and malaria infection for 174 ʻamakihi and 172 malaria‐resistant warbling white‐eyes (Zosterops japonicus) from Hawaiʻi Island using 16S rRNA gene metabarcoding and quantitative polymerase chain reaction. Neither microbial alpha nor beta diversity covaried with infection, but 149 microbes showed positive associations with malaria survivors. Among these wereEscherichiaandLactobacillusspp., which appear to mitigate malaria severity in mammalian hosts, revealing promising candidates for future probiotic research for augmenting malaria immunity in sensitive endangered species.

 

The introduction of nonnative species and reductions in native biodiversity have resulted in substantial changes in vector and host communities globally, but the consequences for pathogen transmission are poorly understood. In lowland Hawaii, bird communities are composed of primarily introduced species, with scattered populations of abundant native species. We examined the influence of avian host community composition, specifically the role of native and introduced species, as well as host diversity, on the prevalence of avian malaria (Plasmodium relictum) in the southern house mosquito (Culex quinquefasciatus). We also explored the reciprocal effect of malaria transmission on native host populations and demography. Avian malaria infection prevalence in mosquitoes increased with the density and relative abundance of native birds, as well as host community competence, but was uncorrelated with host diversity. Avian malaria transmission was estimated to reduce population growth rates of Hawai‘i ʻamakihi (Chlorodrepanis virens) by 7–14%, but mortality from malaria could not explain gaps in this species’ distribution at our sites. Our results suggest that, in Hawaii, native host species increase pathogen transmission to mosquitoes, but introduced species can also support malaria transmission alone. The increase in pathogen transmission with native bird abundance leads to additional disease mortality in native birds, further increasing disease impacts in an ecological feedback cycle. In addition, vector abundance was higher at sites without native birds and this overwhelmed the effects of host community composition on transmission such that infected mosquito abundance was highest at sites without native birds. Higher disease risk at these sites due to higher vector abundance could inhibit recolonization and recovery of native species to these areas. More broadly, this work shows how differences in host competence for a pathogen among native and introduced taxa can influence transmission and highlights the need to examine this question in other systems to determine the generality of this result.