Ebola virus is highly lethal for great apes. Estimated mortality rates up to 98% have reduced the global gorilla population by approximately one-third. As mountain gorillas ( Gorilla beringei beringei ) are endangered, with just over 1000 individuals remaining in the world, an outbreak could decimate the population. Simulation modeling was used to evaluate the potential impact of an Ebola virus outbreak on the mountain gorilla population of the Virunga Massif. Findings indicate that estimated contact rates among gorilla groups are high enough to allow rapid spread of Ebola, with less than 20% of the population projected to survive at 100 days post-infection of just one gorilla. Despite increasing survival with vaccination, no modeled vaccination strategy prevented widespread infection. However, the model projected that survival rates greater than 50% could be achieved by vaccinating at least half the habituated gorillas within 3 weeks of the first infectious individual.
Insurance populations can provide a short-term safeguard for at-risk species. The goal for all insurance populations should be to maintain a high welfare, genetically diverse, self-sustaining population that is available for eventual reintroduction of animals back into the wild when it is safe to do so. However, many insurance populations in zoos are not meeting sustainability goals, and there is a need for larger conservation centers and sanctuaries, a greater focus on threatened species, and metapopulation management between independently managed populations. Within North America, privately-owned ranches frequently maintain large populations of threatened ungulates that are presently managed independently from AZA-accredited zoos. Using a large set of single nucleotide polymorphisms, we generated empirical kinship and genetic distance estimates for AZA and private ranch populations of southern sable antelope (Hippotragus niger niger) and critically endangered addra gazelle (Nanger dama ruficollis). We used stochastic population models to project population mean kinship (mk) and founder genome equivalents (FGE) over time with and without genetic metapopulation management, using empirical kinships and genetic distances to guide transfers. Mean kinship-guided transfers were consistently beneficial for all study populations, for both species. Genetic distance-guided transfers, however, resulted in modest population mk increases for AZA populations, but predicted remarkable decreases in population mk for ranch populations. Although predicted benefits varied depending on management approach, our results show that a metapopulation management plan, whether mutually beneficial or altruistic, best supports species conservation by mitigating the loss of genetic diversity, minimizing the possibility of inbreeding, and yielding genetically diverse animals.
Maintaining the existing biodiversity of endangered species is a goal of conservation management programs, and a major component of many collaborative efforts undertaken by zoos, field biologists, and conservation scientists. Over the past 3 decades, the San Diego Zoo has performed long-term genetic studies in support of the recovery program for the critically endangered California Condor (Gymnogyps californianus). This work has included sex determination of hatchlings and parentage confirmation using microsatellite genotyping. This paper describes the genetic work associated with the California Condor recovery program, which aims to provide a highly accurate pedigree for making informed captive pairing and release recommendations. Initial genotyping began after reintroduced California Condors started reproducing, and the focus was on birds hatched from their wild-laid eggs. However, genetic analysis showed discrepancies relative to behavioral observations of wild birds and led to the species-wide testing of all available samples. This genetic study has resolved instances of individual misidentifications and parental misassignments, verified the first cases of extra-pair paternity in this species, identified parentage where chicks were observed being raised by trios, and found 2 apparent de novo mutations in the captive condor population. Correcting the California Condor pedigree according to genetic parental analysis has produced more accurate estimates of mean kinship values among living birds, ranking potential breeders according to their actual breeding value and helping managers to make informed decisions about captive pairing and release of condors in the wild.
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.
Maintaining a living plant collection is the most common method of ex situ conservation for plant species that cannot be seed banked (i.e., exceptional species). Viability of living collections, and their value for future conservation efforts, can be limited without coordinated efforts to track and manage individuals across institutions. Using a pedigree-focused approach, the zoological community has established an inter-institutional infrastructure to support long-term viability of captive animal populations. We assessed the ability of this coordinated metacollection infrastructure to support the conservation of 4 plant species curated in living collections at multiple botanic gardens around the world. Limitations in current practices include the inability to compile, share, and analyze plant collections data at the individual level, as well as difficulty in tracking original provenance of ex situ material. The coordinated metacollection framework used by zoos can be adopted by the botanical community to improve conservation outcomes by minimizing the loss of genetic diversity in collections. We suggest actions to improve ex situ conservation of exceptional plant species, including developing a central database to aggregate data and track unique individuals of priority threatened species among institutions and adapting a pedigree-based population management tool that incorporates life-history aspects unique to plants. If approached collaboratively across regional, national, and global scales, these actions could transform ex situ conservation of threatened plant species.
Effectively conserving biodiversity with limited resources requires scientifically informed and efficient strategies. Guidance is particularly needed on how many living plants are necessary to conserve a threshold level of genetic diversity in ex situ collections. We investigated this question for 11 taxa across five genera. In this first study analysing and optimizing ex situ genetic diversity across multiple genera, we found that the percentage of extant genetic diversity currently conserved varies among taxa from 40% to 95%. Most taxa are well below genetic conservation targets. Resampling datasets showed that ideal collection sizes vary widely even within a genus: one taxon typically required at least 50% more individuals than another (though Quercus was an exception). Still, across taxa, the minimum collection size to achieve genetic conservation goals is within one order of magnitude. Current collections are also suboptimal: they could remain the same size yet capture twice the genetic diversity with an improved sampling design. We term this deficiency the 'genetic conservation gap'. Lastly, we show that minimum collection sizes are influenced by collection priorities regarding the genetic diversity target. In summary, current collections are insufficient (not reaching targets) and suboptimal (not efficiently designed), and we show how improvements can be made.
Adaptation in nature is ubiquitous, yet characterizing its genomic basis is difficult because population demographics cause correlations with nonadaptive loci. Introduction events provide opportunities to observe adaptation over known spatial and temporal scales, facilitating the identification of genes involved in adaptation. The pathogen causing avian malaria, Plasmodium relictum, was introduced to Hawai'i in the 1930s and elicited extinctions and precipitous population declines in native honeycreepers. After a sharp initial population decline, the Hawai'i ‘amakihi (Chlorodrepanis virens) has evolved tolerance to the parasite at low elevations where P. relictum exists, and can sustain infection without major fitness consequences. High‐elevation, unexposed populations of ‘amakihi display little to no tolerance. To explore the genomic basis of adaptation to P. relictum in low‐elevation ‘amakihi, we genotyped 125 ‘amakihi from the island of Hawai'i via hybridization capture to 40,000 oligonucleotide baits containing SNPs and used the reference ‘amakihi genome to identify genes potentially under selection from malaria. We tested for outlier loci between low‐ and high‐elevation population pairs and identified loci with signatures of selection within low‐elevation populations. In some cases, genes commonly involved in the immune response (e.g., major histocompatibility complex) were associated with malaria presence in the population. We also detected several novel candidate loci that may be implicated in surviving malaria infection (e.g., beta‐defensin, glycoproteins and interleukin‐related genes). Our results suggest that rapid adaptation to pathogens may occur through changes in different immune genes, but in the same classes of genes, across populations.
Species loss due to human activities is occurring at an unprecedented pace ( Barnosky et al., 2011 ), and over the last few decades, botanic gardens have responded by expanding their conservation activities ( CBD, 2010 ). Botanic gardens play a particularly critical role in the development of ex situ (off -site) collections of threatened plant species, and the botanic garden community has helped develop current best practices for ex situ conservation and reintroduction (e.g., via the Center for Plant Conservation; Guerrant et al., 2004 ). Th e majority of plant species are amenable to seed banking or at least vegetative propagation (horticultural or tissue culture), which allows them to be preserved for decades or even centuries before regeneration is necessary and before genetic and demographic viability become an issue ( Havens et al., 2004 ). Consequently, much of the research geared to support ex situ plant conservation has focused on understanding how to effi ciently capture wild genetic diversity to enable successful future reintroduction eff orts ( Guerrant et al., 2004 ). However for “exceptional” plant species that either do not produce seeds or produce seeds that are recalcitrant (i.e., desiccation intolerant so they cannot be dried and frozen), maintaining demographic viability and genetic diversity ex situ can be particularly challenging ( Pence, 2014 ). To date, less effort has been dedicated to ensuring that these living collections, once brought into ex situ cultivation, remain genetically diverse and demographically viable over the long term to support reintroduction eff orts (but see Havens et al., 2004 ). For many exceptional species, living plant collections are the only currently available ex situ conservation option, and the maintenance of these living collections introduces numerous genetic and demographic challenges associated with small, isolated populations. If not curated correctly, these small populations are subject to founder eff ects, genetic drift , and inbreeding, and can experience selective pressure from biotic and abiotic conditions in the ex situ environment. Th ese factors could compromise future reintroduction eff orts and ultimately lead to loss of the species from ex situ collections altogether. In the future, cryopreservation and/or tissue culture may be viable ex situ approaches for exceptional species, thus minimizing immediate concerns about genetic and demographic losses. However, the techniques required for these alternative germplasm conservation approaches are oft en species-specifi c and currently unavailable for many threatened species ( Pence, 2014 ). In addition, capacity and resources to develop and maintain cryopreservation protocols is limited or lacking in many regions. Until research and resources reach a point where all exceptional species can be cryopreserved, living collection management will continue to be critical. Despite the value of ex situ collections, some threatened plant species and valuable genetic resources have already been lost from botanical collections ( Govaerts, 2010 ). Of 844 plant taxa identifi ed as extinct in the wild in 2010, 9% were curated in collections, while another 5% had been in collections but subsequently lost ( Govaerts, 2010 ). While the cause of these losses was not reported, it is likely that at least some were the result of genetic or demographic collapse. It is clear that an integrated and more collaborative approach is needed to eff ectively conserve threatened species ex situ. For example, Brighamia insignis (Campanulaceae), an endemic Hawaiian succulent species, is functionally extinct in the wild with only one remaining extant individual. It is cultivated ex situ in at least 57 botanical collections around the world, but in need of an integrated management plan. Th is species can be seed banked, but seeds lose 1 Manuscript received 30 June 2016; revision accepted 15 August 2016. 2 Department of Plant Science and Conservation, Chicago Botanic Garden, 1000 Lake Cook Road, Glencoe, Illinois 60035 USA; 3 Department of Science and Conservation, National Tropical Botanical Garden, 3530 Papalina Road, Kalāheo, Hawai‘i 96741 USA; 4 Department of Conservation Science, Chicago Zoological Society, Brookfi eld, Illinois 60513 USA; 5 International Center for Tropical Botany, Florida International University and the National Tropical Botanic Garden, Th e Kampong, 4013 South Douglas Road, Coconut Grove, Florida 33133 USA; and 6 Botanic Gardens Conservation International, 199 Kew Road, Richmond, Surrey TW9 3BW UK 7 Author for correspondence (e-mail: khavens@chicagobotanic.org) doi:10.3732/ajb.1600247 O N T H E N AT U R E O F T H I N G S : E S S AY S New Ideas and Directions in Botany
Here, we present a set of RNA-based probes for whole mitochondrial genome in-solution enrichment, targeting a diversity of mammalian mitogenomes. This probes set was designed from seven mammalian orders and tested to determine the utility for enriching degraded DNA. We generated 63 mitogenomes representing five orders and 22 genera of mammals that yielded varying coverage ranging from 0 to >5400X. Based on a threshold of 70% mitogenome recovery and at least 10× average coverage, 32 individuals or 51% of samples were considered successful. The estimated sequence divergence of samples from the probe sequences used to construct the array ranged up to nearly 20%. Sample type was more predictive of mitogenome recovery than sample age. The proportion of reads from each individual in multiplexed enrichments was highly skewed, with each pool having one sample that yielded a majority of the reads. Recovery across each mitochondrial gene varied with most samples exhibiting regions with gaps or ambiguous sites. We estimated the ability of the probes to capture mitogenomes from a diversity of mammalian taxa not included here by performing a clustering analysis of published sequences for 100 taxa representing most mammalian orders. Our study demonstrates that a general array can be cost and time effective when there is a need to screen a modest number of individuals from a variety of taxa. We also address the practical concerns for using such a tool, with regard to pooling samples, generating high quality mitogenomes and detail a pipeline to remove chimeric molecules.
BACKGROUND:The Hawaiian honeycreepers are an avian adaptive radiation containing many endangered and extinct species. They display a dramatic range of phenotypic variation and are a model system for studies of evolution, conservation, disease dynamics and population genetics. Development of a genome-scale resources for this group would augment the quality of research focusing on Hawaiian honeycreepers and facilitate comparative avian genomic research.RESULTS:We assembled the genome sequence of a Hawaii amakihi (Hemignathus virens),and identified ~3.9 million single nucleotide polymorphisms (SNPs) in the genome. Using the amakihi genome as a reference, we also identified ~156,000 SNPs in RAD tag (restriction site associated DNA) sequencing of five honeycreeper species (palila [Loxioides bailleui], Nihoa finch [Telespiza ultima], iiwi [Vestiaria coccinea], apapane [Himatione sanguinea], and amakihi). SNPs are distributed throughout the amakihi genome, and the individual sequenced shows several large regions of low heterozygosity on chromosomes 1, 5, 6, 8 and 11. SNPs from RAD tag sequencing were also found throughout the genome but were found to be more densely located on microchromosomes, apparently a result of differential distribution of the particular site recognized by restriction enzyme BseXI.CONCLUSIONS:The amakihi genome sequence will be useful for comparative avian genomics research and provides a significant resource for studies in such areas as disease ecology, evolution, and conservation genetics. The genome sequences will enable mapping of transcriptome data for honeycreepers and comparison of gene sequences between avian taxa. Researchers will be able to use the large number of SNP markers to genotype honeycreepers in regions of interest or across the whole genome. There are enough markers to enable use of methods such as genome-wide association studies (GWAS) that will allow researchers to make connections between phenotypic diversity of honeycreepers and specific genetic variants. Genome-wide markers will also help resolve phylogenetic and population genetic questions in honeycreepers.