For the past two research highlights at Evolutionary Applications, I first covered a great paper summarizing the many way evolutionary theory can be applied to current issues by Scot Carroll and colleagues:

“As we highlight each month in this section, the application of evolutionary theory to issues affecting the health and well-being of human, agricultural, and natural populations is gaining increasing momentum. In a recent review article written for Science, Scott Carroll et al. take on the now monumental task of synthesizing the many ways that evolutionary biology can be used to address global challenges (Carroll et al. 2014). They comprehensively explore the main problems being tackled with an evolutionary approach, ranging from populations evolving too quickly (such as emerging pathogens or pests evolving resistance to treatment) to populations not evolving quickly enough (for example those being negatively affected by human-mediated change).

The authors begin by identifying what they see as the two key paradigms of applied evolutionary biology: (i) managing contemporary evolution (i.e., manipulating the rapid evolutionary response of short-lived organisms with large population sizes, such as bacterial pathogens) and (ii) altering the phenotype–environment mismatch (i.e., responding to populations of long-lived organisms such as trees that are no longer well adapted to their local environment due to shifts in climatic conditions or changes in biotic interactions). As a great example of such a mismatch, the authors highlight the increasing rates of obesity, diabetes, and heart disease in the human populations as a result of a more sedentary lifestyle with diets rich in sugars and fat. They then identify a number of promising research avenues that either have addressed or have the potential to address current global challenges, covering a wide range of approaches including the use of genetic engineering to more appropriately match genomes to their environment, the use of ‘refuges’ in agriculture and combination treatments against pests and pathogens to hinder the evolution of resistance, and introducing nonlocal genotypes which are predicted to perform better under given environmental conditions into natural populations to increase local adaptation.

The article nicely separates these conceptual approaches into strategies for slowing unwanted evolution or directly influencing fitness of pests and pathogens, strategies for reducing the mismatch between phenotype and the local environment, and strategies for increasing group performance by selecting on group-level traits. For example, the authors discuss the success of artificially selecting for group yield in agricultural plots rather than individual fitness as a means for decreasing competition among plants. Critically, the piece also emphasizes the need to take a unified approach in meeting international objectives for sustainable development and suggests a need for stricter enforcement of guidelines in order to ensure best practice is achieved despite temptation to put profit or immediate success ahead of sustainable solutions.

Overall, the review acts as a unique and remarkable resource both for researchers and students who are new to the field of applied evolution and those who actively contribute to the field.

Carroll, S. P.P. S. JørgensenM. T. KinnisonC. T. BergstromR. F. DenisonP. GluckmanT. B. Smith et al. 2014Applying evolutionary biology to address global challengesScience 346:1245993.”

And then discussed recent applications in molecular evolution, including two new papers using comparative genomics of mosquitos to better understand the evolution of these important disease vectors:

“The study of changing sequence composition of DNA, RNA and proteins over time has offered some of the most fundamental insights into the evolutionary process to date. From understanding how populations and ultimately species diverge to the study of how particular selection pressures affect changes in genotype and phenotype, our knowledge of evolution would be a fraction of what it is now without the major advances made in the field of molecular evolution. Recent technological and bioinformatical improvements have continued to expand these insights, and have also offered key applications such as the ability to model and predict pathogen evolution, monitor the effective population size of threatened species, and help understand what constitutes a healthy microbiome.

Two recent studies, both led by Nora Besansky and published in Science, emphasize the power and challenges of comparative genomics when working to understand the evolution of disease vectors. First, Daniel Neafsey and colleagues report the sequencing, assembly, and comparison of genomes from 16 Anopheles mosquito species (Neafsey et al. 2014). As 11 of these species are considered major disease vectors, comparison among the genomes allowed the researchers to examine underlying genes that may be associated with vectoring capacity. The results suggest that, relative to the Drosophila genus, the Anopholes’ genomes are remarkably flexible, with rapid rates of gene loss/gain, increased loss of introns, and shuffling of genes on the X chromosome. The data suggest a mechanism for the observed functional diversity across the species, especially in those traits such as chemosensory ability that are associated with adaptation to host feeding and therefore disease vectoring. However, comparison among genomes was hampered by what are most likely high levels of interspecific gene flow, or introgression, as described in a separate paper by Michael Fontaine and coauthors (Fontaine et al. 2014). Depending on which genomic segment the authors used to build phylogenetic trees, a remarkably different pattern emerged; trees based on autosomal sequences tended to group the three major vectors of malaria together, while those built using the X chromosome suggest early radiation of these three species and persistent introgression on the autosomes. Together, these studies offer tantalizing hypotheses for the adaptive significance of among-species gene flow and genomic plasticity in allowing the Anopholes genus to act as vectors for a wide array of pathogens.

In addition to the increasing power of genomics and phylogenomics, the use of transcriptional profiling has also proven invaluable to the field. A recent review of novel insights gained through transcriptomic analyses of natural populations by Mariano Alvarez and collaborators highlights the utility of this approach in testing how genotype translates to phenotype, and how this translation is influenced by environment-specific gene expression (Alvarez et al. 2014). Such variation can have dramatic implications for the process of adaptation as well as our ability to predict the response of populations to rapid environmental changes such as those resulting from pathogens, pollutants, or climate change. More recent advancement in transcriptomics includes the ability to profile gene expression of single cells, as discussed by Nicola Crosetto and coauthors in a new paper reviewing recent progress in spatiotemporal transcriptomics (Crosetto et al. 2015). Among the many applications of this powerful approach to unravelling among-cell expression differences is the ability to examine heterogeneity of tumour cells to predict drug sensitivity of various cancers.

The use of sequence data to infer evolutionary processes is not limited to single species. Indeed, the use of metagenomics to infer the composition of species from environmental samples has greatly enhanced our understanding of microbial diversity. In its simplest form, metagenomic analysis allows for a culture-independent characterization of microbial community composition. This type of analysis has gained much recent attention for its application in understanding the microbiomes of eukaryotic species. For example, recent work by Julia Goodrich and colleagues examined how human genetics shapes the relative abundances of various gut bacteria by comparing microbiotas across 416 pairs of twins (Goodrich et al. 2014). The authors first discovered a clear heritability for a subset of bacterial taxa, most notably those from the family Christensenellaceae, which were also correlated with low host body-mass index (BMI). The authors then went a step further by adding a particular species of Christensenellaceae into an obese-associated microbiome and inoculating sterile mice with either the unaltered or altered microbial community. In this way, they were able to demonstrate not only correlation with host metabolism in humans but also to infer causation, as mice supplemented with this species showed reduced weight gain relative to those not receiving the supplement.

The simultaneous analysis of multiple genomes within a single environmental sample also allows for assessment of selection acting on genes shared by members of the community. A terrific example of this comes from recent work by Molly Gibson and collaborators who examined the so-called ‘resistome’ of microbial communities from soil and the human gut, in this case focusing on the genes conferring resistance against 18 antibiotics typically used in clinical settings (Gibson et al. 2015). The authors used a new database of protein families to assign antibiotic resistance functions to each metagenomic segment, and were able to demonstrate that the antibiotic resistance genes found in environmental versus human-associated microbiota were functionally different, perhaps suggesting less gene flow among these communities than previously thought.

Overall, the recent advancements in both omics and bioinformatics have been game-changing for the field of molecular evolution, and the application of such new approaches and technologies have only begun to surface. The potential for advancement in clinical and agricultural settings is already being realized, and application to the management of natural populations, including the spread of disease, is already following.

Alvarez, M.A. W. Schrey, and C. L. Richards2014Ten years of transcriptomics in wild populations: what have we learned about their ecology and evolution? Molecular Ecology, doi: 10.1111/mec.13055

Crosetto, N.M. Bienko, and A. van Oudenaarden2015Spatially resolved transcriptomics and beyondNature Reviews Genetics16:5766

Fontaine, M. C.J. B. PeaseA. SteeleR. M. WaterhouseD. E. NeafseyI. V. SharakhovX. Jiang et al. 2014Extensive introgression in a malaria vector species complex revealed by phylogenomicsScience 125852:4

Gibson, M. K.K. J. Forsberg, and G. Dantas2015Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecologyThe ISME journal 9:207216

Goodrich, J. K.J. L. WatersA. C. PooleJ. L. SutterO. KorenR. BlekhmanM. Beaumont et al. 2014Human genetics shape the gut microbiomeCell 159:789799

Neafsey, D. E.R. M. WaterhouseM. R. AbaiS. S. AganezovM. A. AlekseyevJ. E. AllenJ. Amon et al. 2014Highly evolvable malaria vectors: the genomes of 16 Anopheles mosquitoesScience 347:1258522.”

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