Parasite manipulation of host phenotypes inferred from transcriptional analyses in a trematode-amphipod system.

Manipulation of host phenotypes by parasites is hypothesized to be an adaptive strategy enhancing parasite transmission across hosts and generations. Characterizing the molecular mechanisms of manipulation is important to advance our understanding of host-parasite coevolution. The trematode (Levinseniella byrdi) is known to alter the colour and behaviour of its amphipod host (Orchestia grillus) presumably increasing predation of amphipods which enhances trematode transmission through its life cycle. We sampled 24 infected and 24 uninfected amphipods from a salt marsh in Massachusetts to perform differential gene expression analysis. In addition, we constructed novel genomic tools for O. grillus including a de novo genome and transcriptome. We discovered that trematode infection results in upregulation of amphipod transcripts associated with pigmentation and detection of external stimuli, and downregulation of multiple amphipod transcripts implicated in invertebrate immune responses, such as vacuolar ATPase genes. We hypothesize that suppression of immune genes and the altered expression of genes associated with coloration and behaviour may allow the trematode to persist in the amphipod and engage in further biochemical manipulation that promotes transmission. The genomic tools and transcriptomic analyses reported provide new opportunities to discover how parasites alter diverse pathways underlying host phenotypic changes in natural populations.

Whole-genome phylogeography of the blue-faced honeyeater (Entomyzon cyanotis) and discovery and characterization of a neo-Z chromosome.

Whole-genome surveys of genetic diversity and geographic variation often yield unexpected discoveries of novel structural variation, which long-read DNA sequencing can help clarify. Here, we report on whole-genome phylogeography of a bird exhibiting classic vicariant geographies across Australia and New Guinea, the blue-faced honeyeater (Entomyzon cyanotis), and the discovery and characterization of a novel neo-Z chromosome by long-read sequencing. Using short-read genome-wide SNPs, we inferred population divergence events within E. cyanotis across the Carpentarian and other biogeographic barriers during the Pleistocene (~0.3-1.7 Ma). Evidence for introgression between nonsister populations supports a hypothesis of reticulate evolution around a triad of dynamic barriers around Pleistocene Lake Carpentaria between Australia and New Guinea. During this phylogeographic survey, we discovered a large (134 Mbp) neo-Z chromosome and we explored its diversity, divergence and introgression landscape. We show that, as in some sylvioid passerine birds, a fusion occurred between chromosome 5 and the Z chromosome to form a neo-Z chromosome; and in E. cyanotis, the ancestral pseudoautosomal region (PAR) appears nonrecombinant between Z and W, along with most of the fused chromosome 5. The added recombination-suppressed portion of the neo-Z (~37.2 Mbp) displays reduced diversity and faster population genetic differentiation compared with the ancestral-Z. Yet, the new PAR (~17.4 Mbp) shows elevated diversity and reduced differentiation compared to autosomes, potentially resulting from introgression. In our case, long-read sequencing helped clarify the genomic landscape of population divergence on autosomes and sex chromosomes in a species where prior knowledge of genome structure was still incomplete.

Impact of a tropical forest blowdown on aboveground carbon balance.

Field measurements demonstrate a carbon sink in the Amazon and Congo basins, but the cause of this sink is uncertain. One possibility is that forest landscapes are experiencing transient recovery from previous disturbance. Attributing the carbon sink to transient recovery or other processes is challenging because we do not understand the sensitivity of conventional remote sensing methods to changes in aboveground carbon density (ACD) caused by disturbance events. Here we use ultra-high-density drone lidar to quantify the impact of a blowdown disturbance on ACD in a lowland rain forest in Costa Rica. We show that the blowdown decreased ACD by at least 17.6%, increased the number of canopy gaps, and altered the gap size-frequency distribution. Analyses of a canopy-height transition matrix indicate departure from steady-state conditions. This event will initiate a transient sink requiring an estimated 24-49 years to recover pre-disturbance ACD. Our results suggest that blowdowns of this magnitude and extent can remain undetected by conventional satellite optical imagery but are likely to alter ACD decades after they occur.

Genome assemblies for two Neotropical trees: Jacaranda copaia and Handroanthus guayacan.

The lack of genomic resources for tropical canopy trees is impeding several research avenues in tropical forest biology. We present genome assemblies for two Neotropical hardwood species, Jacaranda copaia and Handroanthus (formerly Tabebuia) guayacan, that are model systems for research on tropical tree demography and flowering phenology. For each species, we combined Illumina short-read data with in vitro proximity-ligation (Chicago) libraries to generate an assembly. For Jacaranda copaia, we obtained 104X physical coverage and produced an assembly with N50/N90 scaffold lengths of 1.020/0.277 Mbp. For H. guayacan, we obtained 129X coverage and produced an assembly with N50/N90 scaffold lengths of 0.795/0.165 Mbp. J. copaia and H. guayacan assemblies contained 95.8% and 87.9% of benchmarking orthologs, although they constituted only 77.1% and 66.7% of the estimated genome sizes of 799 and 512 Mbp, respectively. These differences were potentially due to high repetitive sequence content (>59.31% and 45.59%) and high heterozygosity (0.5% and 0.8%) in each species. Finally, we compared each new assembly to a previously sequenced genome for Handroanthus impetiginosus using whole-genome alignment. This analysis indicated extensive gene duplication in H. impetiginosus since its divergence from H. guayacan.

Ecological Load and Balancing Selection in Circumboreal Barnacles.

Acorn barnacle adults experience environmental heterogeneity at various spatial scales of their circumboreal habitat, raising the question of how adaptation to high environmental variability is maintained in the face of strong juvenile dispersal and mortality. Here, we show that 4% of genes in the barnacle genome experience balancing selection across the entire range of the species. Many of these genes harbor mutations maintained across 2 My of evolution between the Pacific and Atlantic oceans. These genes are involved in ion regulation, pain reception, and heat tolerance, functions which are essential in highly variable ecosystems. The data also reveal complex population structure within and between basins, driven by the trans-Arctic interchange and the last glaciation. Divergence between Atlantic and Pacific populations is high, foreshadowing the onset of allopatric speciation, and suggesting that balancing selection is strong enough to maintain functional variation for millions of years in the face of complex demography.

Genomic Consequences of Long-Term Population Decline in Brown Eared Pheasant.

Population genetic theory and empirical evidence indicate that deleterious alleles can be purged in small populations. However, this viewpoint remains controversial. It is unclear whether natural selection is powerful enough to purge deleterious mutations when wild populations continue to decline. Pheasants are terrestrial birds facing a long-term risk of extinction as a result of anthropogenic perturbations and exploitation. Nevertheless, there are scant genomics resources available for conservation management and planning. Here, we analyzed comparative population genomic data for the three extant isolated populations of Brown eared pheasant (Crossoptilon mantchuricum) in China. We showed that C. mantchuricum has low genome-wide diversity and a contracting effective population size because of persistent declines over the past 100,000 years. We compared genome-wide variation in C. mantchuricum with that of its closely related sister species, the Blue eared pheasant (C. auritum) for which the conservation concern is low. There were detrimental genetic consequences across all C. mantchuricum genomes including extended runs of homozygous sequences, slow rates of linkage disequilibrium decay, excessive loss-of-function mutations, and loss of adaptive genetic diversity at the major histocompatibility complex region. To the best of our knowledge, this study is the first to perform a comprehensive conservation genomic analysis on this threatened pheasant species. Moreover, we demonstrated that natural selection may not suffice to purge deleterious mutations in wild populations undergoing long-term decline. The findings of this study could facilitate conservation planning for threatened species and help recover their population size.

When, why and how tumour clonal diversity predicts survival.

The utility of intratumour heterogeneity as a prognostic biomarker is the subject of ongoing clinical investigation. However, the relationship between this marker and its clinical impact is mediated by an evolutionary process that is not well understood. Here, we employ a spatial computational model of tumour evolution to assess when, why and how intratumour heterogeneity can be used to forecast tumour growth rate and progression-free survival. We identify three conditions that can lead to a positive correlation between clonal diversity and subsequent growth rate: diversity is measured early in tumour development; selective sweeps are rare; and/or tumours vary in the rate at which they acquire driver mutations. Opposite conditions typically lead to negative correlation. In cohorts of tumours with diverse evolutionary parameters, we find that clonal diversity is a reliable predictor of both growth rate and progression-free survival. We thus offer explanations-grounded in evolutionary theory-for empirical findings in various cancers, including survival analyses reported in the recent TRACERx Renal study of clear-cell renal cell carcinoma. Our work informs the search for new prognostic biomarkers and contributes to the development of predictive oncology.