Disease-driven top predator decline affects mesopredator population genomic structure.

Top predator declines are pervasive and often have dramatic effects on ecological communities via changes in food web dynamics, but their evolutionary consequences are virtually unknown. Tasmania's top terrestrial predator, the Tasmanian devil, is declining due to a lethal transmissible cancer. Spotted-tailed quolls benefit via mesopredator release, and they alter their behaviour and resource use concomitant with devil declines and increased disease duration. Here, using a landscape community genomics framework to identify environmental drivers of population genomic structure and signatures of selection, we show that these biotic factors are consistently among the top variables explaining genomic structure of the quoll. Landscape resistance negatively correlates with devil density, suggesting that devil declines will increase quoll genetic subdivision over time, despite no change in quoll densities detected by camera trap studies. Devil density also contributes to signatures of selection in the quoll genome, including genes associated with muscle development and locomotion. Our results provide some of the first evidence of the evolutionary impacts of competition between a top predator and a mesopredator species in the context of a trophic cascade. As top predator declines are increasing globally, our framework can serve as a model for future studies of evolutionary impacts of altered ecological interactions.

The Transmission Patterns of the Endosymbiont Wolbachia within the Hawaiian Drosophilidae Adaptive Radiation.

The evolution of endosymbionts and their hosts can lead to highly dynamic interactions with varying fitness effects for both the endosymbiont and host species. Wolbachia, a ubiquitous endosymbiont of arthropods and nematodes, can have both beneficial and detrimental effects on host fitness. We documented the occurrence and patterns of transmission of Wolbachia within the Hawaiian Drosophilidae and examined the potential contributions of Wolbachia to the rapid diversification of their hosts. Screens for Wolbachia infections across a minimum of 140 species of Hawaiian Drosophila and Scaptomyza revealed species-level infections of 20.0%, and across all 399 samples, a general infection rate of 10.3%. Among the 44 Wolbachia strains we identified using a modified Wolbachia multi-locus strain typing scheme, 30 (68.18%) belonged to supergroup B, five (11.36%) belonged to supergroup A, and nine (20.45%) had alleles with conflicting supergroup assignments. Co-phylogenetic reconciliation analysis indicated that Wolbachia strain diversity within their endemic Hawaiian Drosophilidae hosts can be explained by vertical (e.g., co-speciation) and horizontal (e.g., host switch) modes of transmission. Results from stochastic character trait mapping suggest that horizontal transmission is associated with the preferred oviposition substrate of the host, but not the host's plant family or island of occurrence. For Hawaiian Drosophilid species of conservation concern, with 13 species listed as endangered and 1 listed as threatened, knowledge of Wolbachia strain types, infection status, and potential for superinfection could assist with conservation breeding programs designed to bolster population sizes, especially when wild populations are supplemented with laboratory-reared, translocated individuals. Future research aimed at improving the understanding of the mechanisms of Wolbachia transmission in nature, their impact on the host, and their role in host species formation may shed light on the influence of Wolbachia as an evolutionary driver, especially in Hawaiian ecosystems.

Diversification processes in Gerp's mouse lemur demonstrate the importance of rivers and altitude as biogeographic barriers in Madagascar's humid rainforests.

Madagascar exhibits exceptionally high levels of biodiversity and endemism. Models to explain the diversification and distribution of species in Madagascar stress the importance of historical variability in climate conditions which may have led to the formation of geographic barriers by changing water and habitat availability. The relative importance of these models for the diversification of the various forest-adapted taxa of Madagascar has yet to be understood. Here, we reconstructed the phylogeographic history of Gerp's mouse lemur (Microcebus gerpi) to identify relevant mechanisms and drivers of diversification in Madagascar's humid rainforests. We used restriction site associated DNA (RAD) markers and applied population genomic and coalescent-based techniques to estimate genetic diversity, population structure, gene flow and divergence times among M. gerpi populations and its two sister species M. jollyae and M. marohita. Genomic results were complemented with ecological niche models to better understand the relative barrier function of rivers and altitude. We show that M. gerpi diversified during the late Pleistocene. The inferred ecological niche, patterns of gene flow and genetic differentiation in M. gerpi suggest that the potential for rivers to act as biogeographic barriers depended on both size and elevation of headwaters. Populations on opposite sides of the largest river in the area with headwaters that extend far into the highlands show particularly high genetic differentiation, whereas rivers with lower elevation headwaters have weaker barrier functions, indicated by higher migration rates and admixture. We conclude that M. gerpi likely diversified through repeated cycles of dispersal punctuated by isolation to refugia as a result of paleoclimatic fluctuations during the Pleistocene. We argue that this diversification scenario serves as a model of diversification for other rainforest taxa that are similarly limited by geographic factors. In addition, we highlight conservation implications for this critically endangered species, which faces extreme habitat loss and fragmentation.

Hybridization and range expansion in tamarisk beetles (Diorhabda spp.) introduced to North America for classical biological control.

With the global rise of human-mediated translocations and invasions, it is critical to understand the genomic consequences of hybridization and mechanisms of range expansion. Conventional wisdom is that high genetic drift and loss of genetic diversity due to repeated founder effects will constrain introduced species. However, reduced genetic variation can be countered by behavioral aspects and admixture with other distinct populations. As planned invasions, classical biological control (biocontrol) agents present important opportunities to understand the mechanisms of establishment and spread in a novel environment. The ability of biocontrol agents to spread and adapt, and their effects on local ecosystems, depends on genomic variation and the consequences of admixture in novel environments. Here, we use a biocontrol system to examine the genome-wide outcomes of introduction, spread, and hybridization in four cryptic species of a biocontrol agent, the tamarisk beetle (Diorhabda carinata, D. carinulata, D. elongata, and D. sublineata), introduced from six localities across Eurasia to control the invasive shrub tamarisk (Tamarix spp.) in western North America. We assembled a de novo draft reference genome and applied RADseq to over 500 individuals across laboratory cultures, the native ranges, and the introduced range. Despite evidence of a substantial genetic bottleneck among D. carinulata in N. America, populations continue to establish and spread, possibly due to aggregation behavior. We found that D. carinata, D. elongata, and D. sublineata hybridize in the field to varying extents, with D. carinata × D. sublineata hybrids being the most abundant. Genetic diversity was greater at sites with hybrids, highlighting potential for increased ability to adapt and expand. Our results demonstrate the complex patterns of genomic variation that can result from introduction of multiple ecotypes or species for biocontrol, and the importance of understanding them to predict and manage the effects of biocontrol agents in novel ecosystems.

Contemporary and historical selection in Tasmanian devils (Sarcophilus harrisii) support novel, polygenic response to transmissible cancer.

Tasmanian devils (Sarcophilus harrisii) are evolving in response to a unique transmissible cancer, devil facial tumour disease (DFTD), first described in 1996. Persistence of wild populations and the recent emergence of a second independently evolved transmissible cancer suggest that transmissible cancers may be a recurrent feature in devils. Here, we compared signatures of selection across temporal scales to determine whether genes or gene pathways under contemporary selection (six to eight generations) have also been subject to historical selection (65-85 Myr). First, we used targeted sequencing, RAD-capture, in approximately 2500 devils in six populations to identify genomic regions subject to rapid evolution. We documented genome-wide contemporary evolution, including 186 candidate genes related to cell cycling and immune response. Then we used a molecular evolution approach to identify historical positive selection in devils compared to other marsupials and found evidence of selection in 1773 genes. However, we found limited overlap across time scales, with only 16 shared candidate genes, and no overlap in enriched functional gene sets. Our results are consistent with a novel, multi-locus evolutionary response of devils to DFTD. Our results can inform conservation by identifying high priority targets for genetic monitoring and guiding maintenance of adaptive potential in managed populations.

Disease swamps molecular signatures of genetic-environmental associations to abiotic factors in Tasmanian devil (Sarcophilus harrisii) populations.

Landscape genomics studies focus on identifying candidate genes under selection via spatial variation in abiotic environmental variables, but rarely by biotic factors (i.e., disease). The Tasmanian devil (Sarcophilus harrisii) is found only on the environmentally heterogeneous island of Tasmania and is threatened with extinction by a transmissible cancer, devil facial tumor disease (DFTD). Devils persist in regions of long-term infection despite epidemiological model predictions of species' extinction, suggesting possible adaptation to DFTD. Here, we test the extent to which spatial variation and genetic diversity are associated with the abiotic environment (i.e., climatic variables, elevation, vegetation cover) and/or DFTD. We employ genetic-environment association analyses using 6886 SNPs from 3287 individuals sampled pre- and post-disease arrival across the devil's geographic range. Pre-disease, we find significant correlations of allele frequencies with environmental variables, including 365 unique loci linked to 71 genes, suggesting local adaptation to abiotic environment. The majority of candidate loci detected pre-DFTD are not detected post-DFTD arrival. Several post-DFTD candidate loci are associated with disease prevalence and were in linkage disequilibrium with genes involved in tumor suppression and immune response. Loss of apparent signal of abiotic local adaptation post-disease suggests swamping by strong selection resulting from the rapid onset of DFTD.

Identification of Gastrointestinal Microbiota in Hawaiian Green Turtles (Chelonia mydas).

Green turtles (Chelonia mydas) have a hindgut fermentation digestive tract, which uses cellulolytic microbes to break down plant matter in the cecum and proximal colon. Previous studies on bacterial communities of green turtles have not identified in situ hindgut microbiota, and never before in Hawaiian green turtles, which comprise an isolated metapopulation. Fresh samples using sterile swabs were taken from five locations along the gastrointestinal tracts of eight green turtles that had required euthanization. Bacteria were cultured, aerobically and anaerobically, on nutrient agar and four differential and selective media. Samples at three sections along the gastrointestinal tracts of two green turtles were analyzed using 16S metagenomics on an Ion Torrent Personal Genome Machine. More than half of the 4 532 104 sequences belonged to the phylum Firmicutes, followed by Bacteroidetes and Proteobacteria, which are characteristic of herbivore gut microbiota. Some microbiota variation existed between turtles and among gastrointestinal sections. The 16S sequence analysis provided a better representation of the total gastrointestinal bacterial community, much of which cannot be cultured using traditional microbial techniques. These metagenomic analyses serve as a foundation for a better understanding of the microbiome of green turtles in the Hawaiian Islands and elsewhere.

Phylogenetic Relationships, Breeding Implications, and Cultivation History of Hawaiian Taro (Colocasia Esculenta) Through Genome-Wide SNP Genotyping.

Taro, Colocasia esculenta, is one of the world's oldest root crops and is of particular economic and cultural significance in Hawai'i, where historically more than 150 different landraces were grown. We developed a genome-wide set of more than 2400 high-quality single nucleotide polymorphism (SNP) markers from 70 taro accessions of Hawaiian, South Pacific, Palauan, and mainland Asian origins, with several objectives: 1) uncover the phylogenetic relationships between Hawaiian and other Pacific landraces, 2) shed light on the history of taro cultivation in Hawai'i, and 3) develop a tool to discriminate among Hawaiian and other taros. We found that almost all existing Hawaiian landraces fall into 5 monophyletic groups that are largely consistent with the traditional Hawaiian classification based on morphological characters, for example, leaf shape and petiole color. Genetic diversity was low within these clades but considerably higher between them. Population structure analyses further indicated that the diversification of taro in Hawai'i most likely occurred by a combination of frequent somatic mutation and occasional hybridization. Unexpectedly, the South Pacific accessions were found nested within the clades mainly composed of Hawaiian accessions, rather than paraphyletic to them. This suggests that the origin of clades identified here preceded the colonization of Hawai'i and that early Polynesian settlers brought taro landraces from different clades with them. In the absence of a sequenced genome, this marker set provides a valuable resource towards obtaining a genetic linkage map and to study the genetic basis of phenotypic traits of interest to taro breeding such as disease resistance.

Polymorphic microsatellites in nene, the endangered Hawaiian goose (Branta sandvicensis).

The nene (Branta sandvicensis) is an endangered Hawaiian goose endemic to the Hawaiian Islands. The nene nearly went extinct in the mid-19.00s and the majority of the approximately 1300 individuals currently in Hawai'i are descendants from less than 30 birds. The low adult breeding success and juvenile survival is likely due, in part, to inbreeding depression in wild individuals. Thirty-eight microsatellite primer sets developed in nene, Canada goose, and waterfowl species provided 8 polymorphic loci. Four of these polymorphic loci exhibited only two alleles, which is likely a reflection of the high inbreeding in this species.