Fruits and flies: a genomics perspective of an invertebrate model organism.

The increasing number of species for which a full genome sequence is available offers rich pickings for geneticists, but comparative analysis and assembly of information gathered across species does not always lead to answers about the function of a particular gene. This paper aims to place the invertebrate model system--the fly Drosophila melanogaster--into this playing field and to discuss how the organism arrived at its position in functional genetic analysis. Indeed, despite the wealth of knowledge on how a fly lives, breathes and flies, this organism is likely to remain a player in the analysis of biological, disease and pharmaceutical processes. The fast genetics Drosophila offers, combined with a well-annotated genome and a wealth of techniques facilitating gene function discovery, will ensure its place in functional genomics for some time to come. Although the fly cannot speak, it certainly can tell a tale.     

Boechera, a model system for ecological genomics

The selection and development of a study system for evolutionary and ecological functional genomics (EEFG) depend on a variety of factors. Here, we present the genus Boechera as an exemplary system with which to address ecological and evolutionary questions. Our focus on Boechera is based on several characteristics as follows: (i) native populations in undisturbed habitats where current environments reflect historical conditions over several thousand years; (ii) functional genomics benefitting from its close relationship to Arabidopsis thaliana; (iii) inbreeding tolerance enabling development of recombinant inbred lines, near-isogenic lines and positional cloning; (iv) interspecific crosses permitting mapping for genetic analysis of speciation; (v) apomixis (asexual reproduction by seeds) in a genetically tractable diploid; and (vi) broad geographic distribution in North America, permitting ecological genetics for a large research community. These characteristics, along with the current sequencing of three Boechera species by the Joint Genome Institute, position Boechera as a rapidly advancing system for EEFG studies.     

The locus of sexual selection: moving sexual selection studies into the post‐genomics era

Sexual selection drives fundamental evolutionary processes such as trait elaboration and speciation. Despite this importance, there are surprisingly few examples of genes unequivocally responsible for variation in sexually selected phenotypes. This lack of information inhibits our ability to predict phenotypic change due to universal behaviours, such as fighting over mates and mate choice. Here, we discuss reasons for this apparent gap and provide recommendations for how it can be overcome by adopting contemporary genomic methods, exploiting underutilized taxa that may be ideal for detecting the effects of sexual selection and adopting appropriate experimental paradigms. Identifying genes that determine variation in sexually selected traits has the potential to improve theoretical models and reveal whether the genetic changes underlying phenotypic novelty utilize common or unique molecular mechanisms. Such a genomic approach to sexual selection will help answer questions in the evolution of sexually selected phenotypes that were first asked by Darwin and can furthermore serve as a model for the application of genomics in all areas of evolutionary biology.     

Evolutionary and ecological functional genomics,from lab to the wild

Plant phenotypes are the result of both genetic and environmental forces that act to modulate trait expression. Over the last few years, numerous approaches in functional genomics and systems biology have led to a greater understanding of plant phenotypic variation and plant responses to the environment. These approaches, and the questions that they can address, have been loosely termed evolutionary and ecological functional genomics (EEFG), and have been providing key insights on how plants adapt and evolve. In particular, by bringing these studies from the laboratory to the field, EEFG studies allow us to gain greater knowledge of how plants function in their natural contexts.     

Towards the era of comparative evolutionary genomics in Brassicaceae

The vast genetic diversity, specific genome organization and sequencing of the Arabidopsis thaliana genome made crucifers an ideal group for comparative genomic studies. Arabidopsis genomic resources have greatly expedited comparative genomics within Brassicaceae and fostered the establishment of new Arabidopsis relative model systems (ARMS). The extent of genome colinearity, modes and evolutionary rates of genome alterations are being analyzed by genetic mapping with ever increasing levels of precision. Comparative cytogenetic studies in Brassicaceae are employing various chromosome landmarks and cytogenetic techniques, including localization of rDNA, variation in centromeric satellite repeats, genomic in situ hybridization (GISH), fluorescence ISH using bacterial artificial chromosomes (BAC FISH), and large-scale comparative chromosome painting. Some genome alterations may represent rare genomic changes (RGCs) and thus have the potential to resolve complex/conflicting phylogenetic relationships inferred from DNA sequencing. Comparative genomics should increasingly be integrated with molecular phylogenetics and population genetics to elucidate the processes responsible for genetic variation in Brassicaceae.     

A guide to the genomics of ecological speciation in natural animal populations

Interest in ecological speciation is growing, as evidence accumulates showing that natural selection can lead to rapid divergence between subpopulations. However, whether and how ecological divergence can lead to the buildup of reproductive isolation remains under debate. What is the relative importance of natural selection vs. neutral processes? How does adaptation generate reproductive isolation? Can ecological speciation occur despite homogenizing gene flow? These questions can be addressed using genomic approaches, and with the rapid development of genomic technology, will become more answerable in studies of wild populations than ever before. In this article, we identify open questions in ecological speciation theory and suggest useful genomic methods for addressing these questions in natural animal populations. We aim to provide a practical guide for ecologists interested in incorporating genomic methods into their research programs. An increased integration between ecological research and genomics has the potential to shed novel light on the origin of species.     

合成基因组学：设计与合成的艺术

随着基因组相关技术(测序、编辑、合成等)和知识(功能基因组学)的日益成熟,合成基因组学在本世纪迎得了发展的契机。病毒、原核生物的全基因组相继被化学合成并支持生命的存活,第1个真核生物合成基因组计划已经完成过半,人类基因组编写计划提上日程。在基因组合成的实践过程中,研究者们不断探索对基因组进行重编和设计所应遵循的规则,提高从头合成、组装和替换基因组的技术手段。合成基因组在工业、环境、健康和基础研究领域有着广阔的应用前景,同时也带来了相应的伦理问题。结合在Sc2.0计划中的基因组合成研究和近期合成基因组学所取得的重大进展,本文综述了基因组设计和合成相关的科学、技术和伦理内容,并探讨了未来发展所面对的挑战。作为合成生物学最重要的领域之一,合成基因组学方兴未艾。     

Drosophila melanogaster: the model organism

In the 20th century, there were two decades during which Drosophila melanogaster was the most significant model organism and each decade led to the establishment of new scientific disciplines. The first decade was roughly from 1910 and during this period a small group at Columbia University, headed by Thomas Hunt Morgan, established the rules of transmission genetics with which we are all familiar. In the second decade, roughly from 1970, many of the principles and techniques of the earlier period were used to determine the genetic control of basic aspects of the biology of organisms, notably their development and their behaviour. In this review I will show that it was not only the genius of the research workers (five were awarded Nobel Prizes and it has been argued, with justification, that at least one more should have been awarded) but also the special features of D. melanogaster that led to these advances. While Drosophila is still a significant model organism, the advent of molecular biology permits the investigation of organisms less amenable to genetic analysis, but the principles applied in these investigations were in the main principles laid down during the earlier work on Drosophila.     

Evolutionary and ecological genomics of non‐model plants

Abstract Dissecting evolutionary dynamics of ecologically important traits is a long‐term challenge for biologists. Attempts to understand natural variation and molecular mechanisms have motivated a move from laboratory model systems to non‐model systems in diverse natural environments. Next generation sequencing methods, along with an expansion of genomic resources and tools, have fostered new links between diverse disciplines, including molecular biology, evolution, ecology, and genomics. Great progress has been made in a few non‐model wild plants, such as Arabidopsis relatives, monkey flowers, and wild sunflowers. Until recently, the lack of comprehensive genomic information has limited evolutionary and ecological studies to larger QTL (quantitative trait locus) regions rather than single gene resolution, and has hindered recognition of general patterns of natural variation and local adaptation. Further efforts in accumulating genomic data and developing bioinformatic and biostatistical tools are now poised to move this field forward. Integrative national and international collaborations and research communities are needed to facilitate development in the field of evolutionary and ecological genomics.     

A genome-wide set of 106 microsatellite markers for the blue tit (Cyanistes caeruleus)

We have characterized a set of 106 microsatellite markers in 26-127 individual blue tits (Cyanistes caeruleus), and assigned their location on the zebra finch (Taeniopygia guttata) and on the chicken (Gallus gallus) genome on the basis of sequence homology. Thirty-one markers are newly designed from zebra finch EST (expressed sequence tags) sequences, 22 markers were developed by others from EST sequences using different methods and the remaining 53 loci were previously designed or modified passerine markers. The 106 microsatellite markers are distributed over 26 and 24 chromosomes in the zebra finch and in the chicken genome respectively and the number of alleles varies between 2 and 49. Eight loci deviate significantly from Hardy-Weinberg equilibrium and show a high frequency of null alleles, and three pairs of markers located in the same chromosome appear to be in linkage disequilibrium. With the exception of these few loci, the polymorphic microsatellite markers presented here provide a useful genome-wide resource for population and evolutionary genetic studies of the blue tit, in addition to their potential utility in other passerine birds.     

Integrating population genetics and conservation biology in the era of genomics

As one of the final activities of the ESF-CONGEN Networking programme, a conference entitled ‘Integrating Population Genetics and Conservation Biology’ was held at Trondheim, Norway, from 23 to 26 May 2009. Conference speakers and poster presenters gave a display of the state-of-the-art developments in the field of conservation genetics. Over the five-year running period of the successful ESF-CONGEN Networking programme, much progress has been made in theoretical approaches, basic research on inbreeding depression and other genetic processes associated with habitat fragmentation and conservation issues, and with applying principles of conservation genetics in the conservation of many species. Future perspectives were also discussed in the conference, and it was concluded that conservation genetics is evolving into conservation genomics, while at the same time basic and applied research on threatened species and populations from a population genetic point of view continues to be emphasized.     

Population genomics and the causes of local differentiation

Exactly 50 years ago, a revolution in empirical population genetics began with the introduction of methods for detecting allelic variation using protein electrophoresis (Throckmorton 1962; Hubby 1963; Lewontin & Hubby 1966). These pioneering scientists showed that populations are chock‐full of genetic variation. This variation was a surprise that required a re‐thinking of evolutionary genetic heuristics. Understanding the causes for the maintenance of this variation became and remains a major area of research. In the process of addressing the causes, this same group of scientists documented geographical genetic structure (Prakash et al. 1969), spawning the continued accumulation of what is now a huge case study catalogue of geographical differentiation (e.g. Loveless & Hamrick 1984; Linhart & Grant 1996). Geographical differentiation is clearly quite common. Yet, a truly general understanding of the patterns in and causes of spatial genetic structure across the genome remains elusive. To what extent is spatial structure driven by drift and phylogeography vs. geographical differences in environmental sources of selection? What proportion of the genome participates? A general understanding requires range‐wide data on spatial patterning of variation across the entire genome. In this issue of Molecular Ecology, Lasky et al. (2012) make important strides towards addressing these issues, taking advantage of three contemporary revolutions in evolutionary biology. Two are technological: high‐throughput sequencing and burgeoning computational power. One is cultural: open access to data from the community of scientists and especially data sets that result from large collaborative efforts. Together, these developments may at last put answers within reach.     

Population genomics of the inbred Scandinavian wolf

The Scandinavian wolf population represents one of the genetically most well-characterized examples of a severely bottlenecked natural population (with only two founders), and of how the addition of new genetic material (one immigrant) can at least temporarily provide a 'genetic rescue'. However, inbreeding depression has been observed in this population and in the absence of additional immigrants, its long-term viability is questioned. To study the effects of inbreeding and selection on genomic diversity, we performed a genomic scan with approximately 250 microsatellite markers distributed across all autosomes and the X chromosome. We found linkage disequilibrium (LD) that extended up to distances of 50 Mb, exceeding that of most outbreeding species studied thus far. LD was particularly pronounced on the X chromosome. Overall levels of observed genomic heterozygosity did not deviate significantly from simulations based on known population history, giving no support for a general selection for heterozygotes. However, we found evidence supporting balancing selection at a number of loci and also evidence suggesting directional selection at other loci. For markers on chromosome 23, the signal of selection was particularly strong, indicating that purifying selection against deleterious alleles may have occurred even in this very small population. These data suggest that population genomics allows the exploration of the effects of neutral and non-neutral evolution on a finer scale than what has previously been possible.     

The relevance of pedigrees in the conservation genomics era

Over the past 50 years conservation genetics has developed a substantive toolbox to inform species management. One of the most long-standing tools available to manage genetics—the pedigree—has been widely used to characterize diversity and maximize evolutionary potential in threatened populations. Now, with the ability to use high throughput sequencing to estimate relatedness, inbreeding, and genome-wide functional diversity, some have asked whether it is warranted for conservation biologists to continue collecting and collating pedigrees for species management. In this perspective, we argue that pedigrees remain a relevant tool, and when combined with genomic data, create an invaluable resource for conservation genomic management. Genomic data can address pedigree pitfalls (e.g., founder relatedness, missing data, uncertainty), and in return robust pedigrees allow for more nuanced research design, including well-informed sampling strategies and quantitative analyses (e.g., heritability, linkage) to better inform genomic inquiry. We further contend that building and maintaining pedigrees provides an opportunity to strengthen trusted relationships among conservation researchers, practitioners, Indigenous Peoples, and Local Communities.     

The genome of the Paleogene relic tree Bretschneidera sinensis: insights into trade-offs in gene family evolution,demographic history,and adaptive SNPs

Among relic species, genomic information may provide the key to inferring their long-term survival. Therefore, in this study, we investigated the genome of the Paleogene relic tree species, Bretschneidera sinensis, which is a rare endemic species within southeastern Asia. Specifically, we assembled a high-quality genome for B. sinensis using PacBio high-fidelity and high-throughput chromosome conformation capture reads and annotated it with long and short RNA sequencing reads. Using the genome, we then detected a trade-off between active and passive disease defences among the gene families. Gene families involved in salicylic acid and MAPK signalling pathways expanded as active defence mechanisms against disease, but families involved in terpene synthase activity as passive defences contracted. When inferring the long evolutionary history of B. sinensis, we detected population declines corresponding to historical climate change around the Eocene–Oligocene transition and to climatic fluctuations in the Quaternary. Additionally, based on this genome, we identified 388 single nucleotide polymorphisms (SNPs) that were likely under selection, and showed diverse functions in growth and stress responses. Among them, we further found 41 climate-associated SNPs. The genome of B. sinensis and the SNP dataset will be important resources for understanding extinction/diversification processes using comparative genomics in different lineages.     

A chromosomal genomics approach to assess and validate the desi and kabuli draft chickpea genome assemblies

With the expansion of next‐generation sequencing technology and advanced bioinformatics, there has been a rapid growth of genome sequencing projects. However, while this technology enables the rapid and cost‐effective assembly of draft genomes, the quality of these assemblies usually falls short of gold standard genome assemblies produced using the more traditional BAC by BAC and Sanger sequencing approaches. Assembly validation is often performed by the physical anchoring of genetically mapped markers, but this is prone to errors and the resolution is usually low, especially towards centromeric regions where recombination is limited. New approaches are required to validate reference genome assemblies. The ability to isolate individual chromosomes combined with next‐generation sequencing permits the validation of genome assemblies at the chromosome level. We demonstrate this approach by the assessment of the recently published chickpea kabuli and desi genomes. While previous genetic analysis suggests that these genomes should be very similar, a comparison of their chromosome sizes and published assemblies highlights significant differences. Our chromosomal genomics analysis highlights short defined regions that appear to have been misassembled in the kabuli genome and identifies large‐scale misassembly in the draft desi genome. The integration of chromosomal genomics tools within genome sequencing projects has the potential to significantly improve the construction and validation of genome assemblies. The approach could be applied both for new genome assemblies as well as published assemblies, and complements currently applied genome assembly strategies.     

Plant eco-devo: the potential of poplar as a model organism

Ecological developmental genetics is the study of how ecologically significant traits originate in the genome and how the allelic combinations responsible are maintained in populations and species. Plant development involves a continuous feedback between growth and environment and the success of individual genotype x environment interactions determines the passage of alleles to the next generation: the adaptive recursion. Outbreeding plants contain a large amount of genetic variation, mostly in the form of single nucleotide polymorphisms (SNPs). One of the challenges of eco-devo is to distinguish neutral SNPs from those with ecological consequences. The complete genome sequence of Populus trichocarpa Torr. & A. Gray will be a significant aid in this endeavour. Occurring from California to Alaska, this is the first ecologically 'keystone' species to be sequenced. It has a rich natural history and is an obligate outbreeder. The individual sequenced, Nisqually-1, appears to be heterozygous on average about every 100 bp over the c. 500 million bp of the genome. Overlaid on this within-individual variation is some ecologically based between-individual genotypic variation evident across the distribution of the species. The synthesis of information from genomics and ecology is now in prospect. This 'ecomolecular synthesis' is likely to provide a rich insight into the genomic basis of plant adaptation.